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Processes underlying the effect of mycorrhizal symbiosis on plant-plant interactions

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Processes underlying the effect of mycorrhizal symbiosis on plant-plant interactions

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Fungal DNA Barcoding with Dr. Liz Bowman

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Fungal DNA Barcoding with Dr. Liz Bowman

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Positive citation bias and overinterpreted results lead to misinformation on common mycorrhizal networks in forests

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Positive citation bias and overinterpreted results lead to misinformation on common mycorrhizal networks in forests

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Dr. Laura Bogar on Systems Biology and Mycorrhizal Dynamics 

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Dr. Laura Bogar on Systems Biology and Mycorrhizal Dynamics 

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Ten Ways to make a mushroom- Sporocarp development morphology 

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Ten Ways to make a mushroom- Sporocarp development morphology 

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12.4 Ten ways to make a mushroom

There seem to be ten ways to make this mushroom shape (Watling & Moore, 1994) and these are illustrated in the diagrammatic vertical sections shown in Figs 3-9. Sometimes the cap simply grows out of the top of the stem and as the stem increases in height, the cap increases in radius. The hymenium (spore-bearing tissue) forms on the lower surface of the developing cap, but is exposed to the elements from the earliest stages.

Fig. 3. Schematic diagrams showing gymnocarpic development, where the hymenium (dark shading in these vertical section diagrams) simply grows out of the top of the stem, being naked at first appearance and developing to maturity exposed to the elements on the fruit body surface. Modified from Moore (1998a).

This is called gymnocarpic development; gymnos is the Greek word for 'naked' and carpos is Greek for fruit (Fig. 3). For some explanations of Latin and Greek derivations of words used in science see our Resources Box.

Some protection for the young hymenium results when the cap tissues arise shaped like a lid closely applied to the apex of the stem. In this case hymenial tissue arises in an annular cavity formed between the cap and the stem. This cavity eventually expands to completely separate cap and stem but in the early stages the tissue ( veil, from the Greek velus, a 'skin or parchment') formed between the stem and the closely applied cap protects the hymenium (Fig. 4.). This is called gymnovelangiocarpic development, the word combining gymnos for 'naked' (because it becomes naked as development proceeds) and angio which is derived from a Greek word meaning 'vessel' or 'receptacle' (particularly one containing seed), because the hymenium is enclosed by the veil when first formed.

Fig. 4. During gymnovelangiocarpic development the hymenium is protected by a much reduced veil, seen only during adolescence, which is formed between the stem and the closely applied cap. From Moore (1998a).

In other cases the margin or rim of the cap is curled over to protect the hymenium, this is known as pilangiocarpic development ('hat-receptacle-fruit' in Greek, see Fig. 5; the word pileus being derived from the Greek pilos which was a close-fitting, brimless hat worn by the ancient Greek sailors). Another variation is that the base of the stem (which is called a stipe, the word deriving from the Latin stipes, meaning a tree trunk or post) may be elaborated into a protective flap (called a volva) that covers the developing hymenium in the early stages (called stipitangiocarpic development, or 'stipe-receptacle-fruit' in Greek) (Fig. 6).

Fig. 5. In pilangiocarpic development, the hymenium (black in the diagram) is protected by tissue extending downwards from the margin of the cap to enclose the spore-bearing tissue in the earliest stages and then curling in around the cap margin to protect the youngest hymenium as the fruit body matures. Modified from Moore (1998a).

Fig. 6. Stipitoangiocarpic development describes an arrangement in which the hymenium is protected by tissue extending upwards from the stem base. This does not enclose the whole primordium and the cap bursts through as it matures, often leaving a cup-shaped remnant of tissue at the base of the stem which is called a volva (which comes from a Latin word meaning 'a covering'). Modified from Moore (1998a).

The most extreme expression of this latter form of protection is bulbangiocarpic development, where the tissue protecting the hymenium is largely derived from the basal bulb of the stem and initially completely encloses the primordium (Fig. 7).

Fig. 7. At its most extreme, the volva may extend right over the top of the fruit body and completely enclose it. This is called bulbangiocarpic development, and is the basic structure of the Paddy Straw Mushroom, Volvariella volvacea, and its relatives (see Fig. 27). Modified from Moore (1998a).

The key feature, and the key function, in these descriptions so far has been protection of the hymenium, and the protective tissues may have different anatomical origins but are most often called veils. This has led to the recognition of four types of velangiocarpic development where one or more special covering tissues (the veils) specifically cover the hymenium (Fig. 8). There may be a single ( universal) veil enveloping the primordium in monovelangiocarpic types; or an inner ( partial) veil specifically covering the hymenium in addition to the enveloping universal veil in the bivelangiocarpic type. There is also a paravelangiocarpic type in which the veil is reduced and often lost at maturity; and a metavelangiocarpic type, where a union of secondary tissues emerging from the cap and/or stem forms an analogue of the universal veil.

Fig. 8. Four types of velangiocarpic development shown as diagrammatic vertical sections through immature fruit bodies. In velangiocarpic fruit bodies the hymenium (shown black in the diagrams) is protected by veil tissue (shaded grey) until the spores mature and it then becomes exposed. Monovelangiocarpic types have a single ( universal) veil enveloping the primordium. In the bivelangiocarpic type there is an inner ( partial) veil (dark grey) in addition to the enveloping universal veil. In paravelangiocarpic types the veil (dark grey) is reduced and often lost at maturity (the Greek prefix para- meaning 'closely resembling' or 'almost'). In the metavelangiocarpic type a union of secondary tissues emerging from the cap and/or stem forms an analogue of the universal veil (the prefix meta- in this context comes from the Greek and means 'with' or 'among'). Modified from Moore (1998a).

And finally there are several groups in which the fruit body structure is so modified that it does not develop as a mushroom at all, but may emerge as an even more peculiar fruit body, like a stinkhorn, or a puffball, or a truffle. This is called endocarpic development (from the Greek endon 'within' or 'inside') and it results in a fruit body in which the hymenium is enclosed or covered over. Three patterns of this sort are shown as diagrammatic vertical sections through mature fruit bodies in Fig. 9.

Fig. 9. Endocarpic development produces a fruit body in which the mature hymenium is enclosed or covered over. Three patterns of this gasteromycetous form of fruit body are shown here as diagrammatic vertical sections through mature fruit bodies. Modified from Moore (1998a).

These fruit bodies, most of which are buried in the soil ( hypogeous) or at least at the soil surface, were for many years assigned to a specific taxonomic group, the gasteromycetes ('stomach fungi', from the Greek gaster, meaning 'stomach' or 'belly'). However, it became evident that far from defining a natural taxon, the hypogeous fruit body represented a specialisation along many distinct phylogenetic lines. There are some species that produce hypogeous fruit bodies as a departure from their normal epigeous form to cope with adverse environmental conditions (particularly drought and desiccation).

The above discussion is intended to introduce you to the notion that differential growth of different tissues can and does generate a tremendous range of morphological diversity in fungal fruit bodies. This diversity is amplified when you add features like size, pigmentation, symmetry, regular or irregular relationships between the sizes of the component organs, and whether the hymenium is borne on gills, pores or teeth (and whether these are thick or large, thin or small, and/or numerous or few). So if you count up the names assigned to our descriptions above you will find that there are, indeed, ten ways to make a mushroom ( CLICK HERE to download a summary diagram of all these as a PDF page); but in numerical terms, that's just the start of the equation and we hope our descriptions will enable you to think just a little more deeply about the mushrooms in your garden, or those in your mushroom risotto or stir-fry, or alongside your steak.

In and around the British Isles there are 101 known species of mammal, 603 species of birds, 2,951 species of vascular plant, but more than 15,000 species of fungi, a number that rivals the insects (22,500 British species).That's biodiversity.

From this point we are going to concentrate on cellular details of development and most of the account will deal with an ink cap mushroom now called Coprinopsis cinerea. It is an unfortunate fact of life for those who work with this fungus that it has been misidentified on a number of occasions, so several specific names appear in the literature to which we will refer, including Coprinus cinereus, Coprinus lagopus and Coprinus macrorhizus. They all refer to the same fungus, the different names being the result of misidentifications. Some of the problems of identification are discussed by Moore et al. (1979) who also give a general description of the morphological aspects of fruit body development in the organism. Subsequently, Redhead et al. (2001) used molecular sequence analyses to revise the taxonomy of the whole group that had been called ' Coprinus' and subdivided it into Coprinus (in the family Agaricaceae), and Coprinellus, Coprinopsis, and Parasola in the new family Psathyrellaceae. This is how Coprinus cinereus became Coprinopsis cinerea.

Updated July, 2019

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David Moore, Geoffrey D. Robson and Anthony P.J. Trinci

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Development fungal fruit body. Development. Morphogenesis. Developmental biology. Ways to make a mushroom. Competence, regional patterning. Coprinopsis fruit body, making hymenia. Coprinopsis, Volvariella gills, polypores make tubes, pores. Coprinopsis fruit body, making stem, stipe, stalk. Cell inflation, maturing fruit body. Mushroom mechanics. Metabolic regulation-morphogenesis. Developmental commitment. Genetics development, genomic data mining, genomic systems analysis.

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Fomitopsis betulina (formerly Piptoporus betulinus): the Iceman’s polypore fungus with modern biotechnological potential

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Fomitopsis betulina (formerly Piptoporus betulinus): the Iceman’s polypore fungus with modern biotechnological potential

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As a library, NLM provides access to scientific literature. Inclusion in an NLM database does not imply endorsement of, or agreement with, the contents by NLM or the National Institutes of Health.
Learn more: PMC Disclaimer | PMC Copyright Notice

World J Microbiol Biotechnol. 2017; 33(5): 83.

Abstract

Higher Basidiomycota have been used in natural medicine throughout the world for centuries. One of such fungi is Fomitopsis betulina (formerly Piptoporus betulinus), which causes brown rot of birch wood. Annual white to brownish fruiting bodies of the species can be found on trees in the northern hemisphere but F. betulina can also be cultured as a mycelium and fruiting body. The fungus has a long tradition of being applied in folk medicine as an antimicrobial, anticancer, and anti-inflammatory agent. Probably due to the curative properties, pieces of its fruiting body were carried by Ötzi the Iceman. Modern research confirms the health-promoting benefits of F. betulina. Pharmacological studies have provided evidence supporting the antibacterial, anti-parasitic, antiviral, anti-inflammatory, anticancer, neuroprotective, and immunomodulating activities of F. betulina preparations. Biologically active compounds such as triterpenoids have been isolated. The mushroom is also a reservoir of valuable enzymes and other substances such as cell wall (1→3)-α-d-glucan which can be used for induction of microbial enzymes degrading cariogenic dental biofilm. In conclusion, F. betulina can be considered as a promising source for the development of new products for healthcare and other biotechnological uses.

Biological activity, Cultivation, Keywords: Fomitopsis betulina, Phytochemistry, Piptoporus betulinus

Introduction

In 1991, a mummified body was discovered in the Val Senales glacier in Italy. The man (named Ӧtzi the Iceman), who lived 5300 years ago, carried two fragments of a fruiting body of Fomitopsis betulina (formerly Piptoporus betulinus). Some scientists believe that Ӧtzi might have used the fungus for medical purposes (Capasso 1998) and, although the idea arouses some controversy (Pöder 2005), the long tradition of the use of F. betulina in folk medicine is a fact (Reshetnikov et al. 2001; Wasser 2010). Infusion from F. betulina fruiting bodies was popular, especially in Russia, Baltic countries, Hungary, Romania for its nutritional and calming properties. Fungal tea was used against various cancer types, as an immunoenhancing, anti-parasitic agent, and a remedy for gastrointestinal disorders (Grienke et al. 2014; Lucas 1960; Peintner and Pöder 2000; Semerdžieva and Veselský 1986; Shamtsyan et al. 2004). Antiseptic and anti-bleeding dressings made from fresh F. betulina fruiting body were applied to wounds and the powder obtained from dried ones was used as a painkiller (Grienke et al. 2014; Papp et al. 2015; Rutalek 2002).

In the present paper, we have shown the current knowledge of the fungus F. betulina, including its lifestyle, chemical composition, and potential in biotechnology.

Taxonomy and characteristics

Piptoporus betulinus (Bull.) P. Karst. (known as birch polypore, birch bracket, or razor strop) is a common Basidiomycota brown rot macrofungus growing on decaying birch wood. Homobasidiomycetes were divided into eight clades. The family Polyporaceae with the genus Piptoporus was classified to the polyporoid clade, and then the antrodia clade-the Fomitopsis-Daedalea-Piptoporus group comprising brown rot fungi was identified within this clade (Hibbett and Donoghue 2001; Hibbett and Thorn 2001). Further studies of the phylogenetic relationships among members of the antrodia clade revealed polyphyly of the Fomitopsis genus and suggested that P. betulinus was phylogenetically closer to Fomitopsis than to Piptoporus (Kim et al. 2005; Ortiz-Santana et al. 2013). Recently, P. betulinus (Bull.) P. Karst. has been transferred to Fomitopsis (Han et al. 2016) and, according to Index Fungorum ( 2016), is classified in the genus Fomitopsis, family Fomitopsidaceae, order Polyporales, class Agaricomycetes, division Basidiomycota, kingdom Fungi, with the current name Fomitopsis betulina (Bull.) B.K. Cui, M.L. Han and Y.C. Dai, comb.nov. (MycoBank no.: MB 812646).

Fomitopsis betulina is characterized by annual, sessile to effused-reflexed, tough to woody hard basidiocarps, white to tan or pinkish-colored pore surface with mostly small and regular pores. Fruiting bodies grow singly or in small groups, are covered with a laccate, glabrous crust, never zonate, young cream to white, later ochraceous-brown to greyish brown (Fig. 1 a). The mycelium of F. betulina developing on agar media is white, relatively homogeneous, downy-felt, with regular colony edges (Fig. 1 b). The hyphae develop radially. The hyphal system is mostly dimitic. The clamped generative hyphae, 1.5-3.5 µm in diameter, are branched and hyaline whereas the skeletal hyphae with the diameter of 3- 4 µm, are less branched and have thicker walls. No primordia or fruiting bodies of this species were found in vitro (Petre and Tanase 2013). Basidiospores are smooth, hyaline, thin-walled, and cylindrical (Han and Cui 2015; Han et al. 2016; Kim et al. 2005; Schwarze 1993).

The birch polypore grows mainly as a saprophyte on dead trees and occasionally as a parasite of living trees. It occurs in northern temperate forests and parks in Europe, North America, and Asia. The host range of the fungus is restricted exclusively to birch species, e.g. Betula pendula Roth., B. pubescens Ehrh., B. papyrifera Marsh., and B. obscura Kotula (Schwarze 1993; Žižka et al. 2010).

Wood decay

Wood rotting fungi are traditionally divided into white and brown rot species based on the structure and composition of residual wood. Brown rot fungi extensively degrade the carbohydrate fraction of lignocellulose but, in contrast to white rot fungi, leave lignin, although in a modified form. In these fungi, chemical depolymerization of cellulose, which precedes and supports its enzymatic degradation, is very important. They lack ligninolytic peroxidases and usually some other enzymes such as processive cellobiohydrolases used for degradation of crystalline cellulose, but contain H ₂O ₂-generating oxidases and Fe ³⁺- and quinone-reducing enzymes used for non-enzymatic depolymerization of polysaccharides (Arantes and Goodell 2014; Baldrian and Valášková 2008; Hori et al. 2013). Modern phylogenetic evidence suggest, however, that there is no sharp distinction between the two groups of fungi (Hori et al. 2013; Riley et al. 2014).

Fomitopsis betulina is one of the most common brown rot species but its wood-decaying mechanism has been tested only fragmentarily (Meng et al. 2012) and is still poorly understood. As other fungi of this type, it degrades wood to yield brown, cubical cracks easily broken down. Many factors, including microflora or compounds present in wood, contribute to this complex process (Przybył and Żłobińska-Podejma 2000; Song et al. 2016; Zarzyński 2009). Shang et al. ( 2013) showed that wood samples decayed by F. betulina lost 57% of dry weight (dw) and 74% of holocellulose after 30 days, whereas the fungus growing on wheat straw causes 65% loss of dw within 98 days of culture (Valášková and Baldrian 2006a). A set of enzymes of F. betulina involved in the degradation of lignocellulose was characterized in detail by Valášková and Baldrian ( 2006a, b). The fungus growing on straw produced enzymes with wide substrate specificities: (1→4)-β-endoglucanase, β-glucosidase, (1→4)-β-endoxylanase, (1→4)-β-endomannanase, (1→4)-β-xylosidase, and (1→4)-β-mannosidase. The activities of ligninolytic enzymes and cellobiose dehydrogenase for oxidoreductive cleavage of cellulose were not detected. Similar results were obtained in liquid cultures by Vĕtrovský et al. ( 2013). When F. betulina grew in nature, β-glucosidase and β-mannosidase activity was associated with the fruiting bodies while endopolysaccharidases were detected in colonized wood (Valášková and Baldrian 2006a).

Cultivation

Carpophores of F. betulina from natural habitats or mycelium and culture liquid from submerged cultures were used as raw material to obtain extracts and bioactive substances with medicinal properties (Table 1 ) (Lomberh et al. 2002). Studies concerning the mycelium growth rate in the presence of various substances (metals, dyes) were conducted mainly on agar media or in liquid cultures (Baldrian and Gabriel 2002; Dresch et al. 2015; Hartikainen et al. 2016). The yield of F. betulina mycelium was established in liquid cultures with addition of some agricultural wastes in the studies of Krupodorova and Barshteyn ( 2015). The enzymatic activity of F. betulina was studied in laboratory conditions on agar media (Krupodorova et al. 2014), in liquid cultures (Vĕtrovský et al. 2013), on wheat straw (Valášková and Baldrian 2006a, b), and on Betula sp. wood samples (Reh et al. 1986; Shang et al. 2013).

Table 1

Biological activity

Mechanism of biological activity

Model [method of study]

Extracta

Active compounda

References

Bacillus sp., Rhodococcus equi, S. aureus [zone of inhibition, disk-diffusion method]

Chloroform extracts

Karaman et al. ( 2009)

Bacillus sp., R. equi, S. aureus, E. coli [zone of inhibition, agar well diffusion assay]

Methanol extracts

Karaman et al. ( 2009), Keller et al. ( 2002)

B. subtilis, S. lutea, Brucella sp. [zone of inhibition, agar well diffusion assay]

Ether extracts

Polyporenic acid (suggested)

Kandefer-Szerszeń and Kawecki ( 1974), Utzig and Fertig ( 1957)

B. subtilis, Enterococcus faecalis, E. coli, S. aureus [zone of inhibition, agar well diffusion assay, NCCLS-method]

Piptamine isolated from submerged culture of F. betulina

Schlegel et al. ( 2000)

Candida albicans, Kluyveromyces marxianus, Rhodotorula rubra, Sporobolomyces salmonicolor, Penicillium notatum [zone of inhibition, agar well diffusion assay, NCCLS-method]

Piptamine isolated from submerged culture of F. betulina

Schlegel et al. ( 2000)

Antiviral

Protection of CEF cells from vaccinia virus

Host/target cells: primary culture of chick embryo fibroblast (CEF)

Challenge virus: vaccinia virus

Ethanol extracts

Kandefer-Szerszeń et al. ( 1981)

Ether extracts

polyporenic acid (suggested)

Kandefer-Szerszeń and Kawecki ( 1974)

nucleic acids (RNA and DNA)

Kandefer-Szerszeń et al. ( 1979)

Protection of HAT cells from vaccinia virus by induction of interferon

Host/target cells: human fibroblast culture (HAT)

challenge virus: vaccinia virus

[plaque formation assays]

RNA

Kawecki et al. ( 1978)

Mice protection from lethal infection with TBE

Host/target: Swiss mice

Challenge virus: tick borne encephalitis (TBE) virus

Ethanol extracts

Kandefer-Szerszeń et al. ( 1981)

Ether extracts

Polyporenic acid

Kandefer-Szerszeń and Kawecki ( 1974)

Nucleic acids (RNA and DNA) (suggested)

Kandefer-Szerszeń et al. ( 1979), Kawecki et al. ( 1978)

Mice protection from lethal infection with HSV-2

host/target: Swiss mice

Challenge virus: herpes simplex virus type 2 (HSV-2) [neutralization test]

RNA

Kawecki et al. ( 1978)

Mice protection from ear edema induction by 12- O-tetradecanoylphorbol-13-acetate (TPA)

Mice ear edema model

Polyporenic acid A; polyporenic acid C; (3α,12α,25 S)-3-[(carboxyacetyl)oxy]-12-hydroxy-24-methylene-lanost-8-en-26-oic acid; (3α,12α,25 S)-12-hydroxy-3-[[(3 S)-3-hydroxy-5-methoxy-3-methyl-1,5-dioxopentyl]oxy]-24- methylene-lanost-8-en-26-oic acid; (+)-12α,28-dihydroxy-3α-(30-hydroxy-30-methylglutaryloxy)-24-methyllanosta-8,24(31)-dien-26-oic acid

Kamo et al. ( 2003)

Anticancer

Antimigrative properties

Cancer cell lines: A549, HT-29, T47D, TE671 [wound assay]

Ethanol extracts

Pleszczyńska et al. ( 2016), Zwolińska ( 2004), Żyła et al. ( 2005)

Cancer cell lines: A549, C6, HT-29, T47D [wound assay]

Water extracts

Pleszczyńska et al. ( 2016), Lemieszek et al. ( 2009)

Cell death induction

Cancer cell lines: A549, T47D, TE671 [May Grünwald Giemsa staining]

Ethanol extracts

Żyła et al. ( 2005), Zwolińska ( 2004)

Inhibition of cancer cells proliferation

Cancer cell lines: A549, C6, HEp-2, HT-29, Jurkat E6.1, RPMI 8226, T47D, TE671 [MTT test]

Ethanol extracts

Pleszczyńska et al. ( 2016), Wasyl ( 2006), Żyła et al. ( 2005), Zwolińska ( 2004)

Cancer cell lines: A549, C6, FTC238, HEp-2, HeLa, HT-29, Jurkat E6.1, RPMI 8226, SK-N-AS, T47D, TE671 [MTT test]

Ether extract

Wasyl ( 2006), Kaczor et al. ( 2004), Zwolińska ( 2004)

Cancer cell lines: A549, C6, HT-29, Jurkat E6.1, T47D [MTT test]

Water extracts

Pleszczyńska et al. ( 2016), Lemieszek et al. ( 2009), Zwolińska ( 2004)

Tumor size reduction by induction of cancer cell necrolysis and inhibition of metastases

Female dogs with adenocarcinoma mammae, adenocarcinoma solidum, adenocarcinoma papilliferum

[histopathological examination after Hansen staining]

Water extracts

Pentacyclic triterpenes (suggested)

Wandokanty et al. ( 1954; 1955)

Tumor size reduction and inhibition of bleeding from the genital tract

Female dogs with Sticker's sarcoma

[per vaginal examination]

Ethanol extracts

Pentacyclic triterpenes (suggested)

Utzig and Samborski ( 1957)

There are limited data on small- or large-scale cultivation of this species in which carpophores could be obtained in controlled conditions. The first such report referring to outdoor log cultivation of F. betulina on Betula davurica Pallas originated from Korea (Ka et al. 2008). Logs with a diameter of 8-18 cm and length of 107-135 cm were inoculated and then cultured in natural conditions. The yield obtained was in the range from 212 to 1298 g fresh weight (1-2 mushrooms per log). Development of fruiting bodies took an average of 18 months. The ratio of log yield was estimated at 2.8-6.1%. The only report on indoor production of F. betulina fruiting bodies was given by Pleszczyńska et al. ( 2016). In the study, four strains of F. betulina isolated from natural habitats were applied. Their mycelia were inoculated into birch sawdust supplemented with organic additives. Mature fruiting bodies weighing from 50 to 120 g were obtained from only one strain, after 3-4 months of the cultivation in artificial conditions (Fig. 1 c). The biological efficiency ranged from 12 to 16%. It was shown that extracts isolated from cultivated and naturally grown F. betulina fruiting bodies had comparable biological activity (Table 1 ).

Biotechnological uses

Phytochemistry and pharmacological activity

Comprehensive analyses of the chemical composition of the F. betulina fruiting body carried out under different conditions (Grishin et al. 2016; Hybelbauerová et al. 2008; Reis et al. 2011) revealed the presence of 17 fatty acids, in it 22% saturated and 78% unsaturated (mainly oleic and linoleic acid); sugars (d-arabinitol, d-mannitol and α,α trehalose); biomolecules with antioxidant properties (tocopherols-0.578 mg/100 g dw, mainly β and γ; ascorbic acid-87.5 mg/100 g dw; β-carotene and lycopene). Among other identified compounds were betulinic acid, betulin, lupeol, fomefficinic acid, ergosterol peroxide, and 9,11-dehydroergosterol peroxide (Alresly et al. 2016; Jasicka-Misiak et al. 2010). Total content of phenolics was determined on 14 or 35 mg GAE/g dw whereas phenolic acids were not detected (Reis et al. 2011; Sułkowska-Ziaja et al. 2012). Product of hydrodistillation of F. betulina fruiting bodies contained numerous volatile mono- and sesquiterpenes. Several compounds found, (+)-α-barbatene, (−)-β-barbatene, daucene and isobazzanene, have not been previously reported from other mushrooms. Alcohols, 3-octanol and 1-octen-3-ol, were the main flavour constituents of the fungus (Rapior et al. 1996; Rösecke et al. 2000).

Although some authors considered young specimens of F. betulina edible (Wasson 1969), the fungus value is not the result of nutritional but therapeutic properties. The overview of the available literature concerning medical potential of birch polypore was presented in Table 1 . Referring to the folk uses of the birch polypore, most of the presented research was based on crude extracts, which often have greater bioactivity than isolated constituents at an equivalent dose. This phenomenon is explained by mostly synergistic interactions between compounds present in mixtures. Furthermore, extracts often contain substances that inhibit multi-drug resistance and therefore further increase the effectiveness of the active substances. Particularly noteworthy among the wide variety of biological activities of F. betulina extract, are properties proved in in vivo studies, e.g. the efficacy of water and ethanol extracts in treatment of the genital tract in dogs (Utzig and Samborski 1957; Wandokanty et al. 1954, 1955) or mice protection from lethal infection with the TBE virus by water, ethanol, and ether extracts (Kandefer-Szerszeń et al. 1981; Kandefer-Szerszeń and Kawecki 1974, 1979). The broad spectrum of antiviral and antimicrobial activity of F. betulina extracts proved by a number of research teams in different models based on different techniques deserves special attention as well (see references cited in Table 1 ). Recently, Stamets ( 2011, 2014) has invented formulations prepared from different medicinal mushrooms including F. betulina, which are useful in preventing and treating viral and bacterial diseases, i.e. herpes, influenza, SARS, hepatitis, tuberculosis, and infections with E. coli and S. aureus .

Some pure compounds corresponding to the bioactivity of the birch polypore were also identified (Fig. 2 ). They belong to several chemical classes but the greatest attention was paid to small molecular weight secondary metabolites, especially triterpenoids. Kamo et al. ( 2003) isolated several triterpenoid carboxylic acids with a lanostane skeleton, e.g. polyporenic acids and their derivatives (Table 1 ). In in vivo tests, the substances suppressed TPA-induced mouse ear inflammation up to 49-86% at the dose of 0.4 µM/ear. Alresly et al. ( 2016) purified one previously unknown (identified as 3β-acetoxy-16α hydroxyl-24-oxo-5α-lanosta-8-ene-21-oic acid) and ten known triterpenes from ethyl acetate extract of fruiting bodies of the fungus. The new compound showed anti-gram-positive bacteria activity. The medicinal activity of some triterpenoids tested was examined more accurately. It was shown that polyporenic acid C, just like another compound isolated from F. betulina, i.e. (E)-2-(4-hydroxy-3methyl-2-butenyl)-hydroquinone, had inhibitory activity against some matrix metalloproteinases (MMP), with IC ₅₀ values (concentration causing inhibition by 50% compared to control) in the range from 23 to 128 µM (Kawagishi et al. 2002). Polyporenic acid C and three other F. betulina triterpenoids (Table 1 ) showed anti-inflammatory and antibacterial activity by strong inhibition of 3α-hydroxysteroid dehydrogenase and bacterial hyaluronate lyase activity, respectively (Wangun et al. 2004).

In their search for fungal antimicrobial substances, Schlegel et al. ( 2000) isolated another valuable compound-piptamine, N-benzyl-N-methylpentadecan-1-amine from submerged culture of F. betulina Lu 9-1. It showed activity against gram-positive bacteria (MIC, minimum inhibitory concentration, values in the range from 0.78 to 12.5 µg/ml) and yeasts including Candida albicans (MIC 6.25 µg/ml).

Polysaccharides from higher basidiomycota mushrooms have been usually considered to be the major contributors of their bioactivity. However, birch polypore polysaccharides have not yet been sufficiently explored, in terms of either the structure or pharmacological activity. It is known that the Fomitopsis cell wall contains (1→3)-β-d-glucans in an amount of ca. 52% dw (Jelsma and Kreger 1978; Grün 2003). They are built from β-d-glucopyranose units connected with (1→3)-linkages in the main chain, with (1→3)-β-d linked side branches. However, there are no reports about their biological activities. Another polysaccharide isolated from the birch polypore was water-insoluble, alkali-soluble (1→3)-α-d-glucan. Although α-glucans are believed to be biologically inactive, its carboxymethylated derivative showed moderate cytotoxic effects in vitro (Wiater et al. 2011).

Miscellaneous applications

With the knowledge of the mechanisms of action of brown rot decay, there are possibilities of new applications of these fungi in biotechnology. The enzymatic and non-enzymatic apparatus for lignocellulose degradation can be used for bioprocessing of biomass towards fuels and chemicals (Arantes et al. 2012; Giles and Parrow 2011; Ray et al. 2010). Brown rot fungi, including F. betulina, were tested for bioleaching of heavy metals (Cu, Cr, and As) from wood preservatives due to accumulation of metal-complexing oxalic acid (Sierra Alvarez 2007). Production of biomass degrading enzymes, for instance cellulases, hemicellulases, amylases, etc., was also studied (Krupodorova et al. 2014; Valášková and Baldrian 2006a, b).

The cell wall of F. betulina can be a source of useful polysaccharides, e.g. water-insoluble, alkali-soluble α-glucans (Grün 2003; Jelsma and Kreger 1979). (1→3)-α-d-glucans whose main chain contains 84.6% of (1→3)-linked α-d-glucopyranose in addition to 6% of (1→4)-linked units were purified and characterized by Wiater et al. ( 2011). Another polysaccharide, named piptoporane I, was extracted and purified by Olennikov et al. ( 2012). This α-glucan was built from residues of (1→3)-α-d-glucopyranose with occasional branching by single residues of β-d-glucopyranose at the C ₆ position (17.3%). It has been shown that fungal (1→3)-α-d-glucans, including that from F. betulina, effectively induce the production of microbial (1→3)-α-glucanases (mutanases), i.e. enzymes that have potential in dental caries prevention. (1→3),(1→6)-α-d-Glucans (mutans) synthesized by mutans streptococci are key structural and functional constituents of dental plaque matrix; therefore, they seem to be a good target for enzymatic anti-caries strategy (Pleszczyńska et al. 2015). However, streptococcal glucans are difficult to use as inducers of mutanases because of the low yield and structural variation. Birch polypore α-glucan, whose amount in the cell wall of F. betulina reaches even 44-53% dw (Grün 2003), can be used to replace streptococcal glucans (Wiater et al. 2008).

Conclusions and outlook

The F. betulina fungus has been widely used and appreciated in folk medicine, and modern pharmacological studies have confirmed its potential indicating significant antimicrobial, anticancer, anti-inflammatory, and neuroprotective activities. The possibility of successful cultivation thereof in artificial conditions additionally promotes the applicability of the fungus. However, compared with other polypore fungi, the research on F. betulina is less developed; for instance, little is known about its lifestyle, including the wood degradation strategy. Moreover, most of the bioactivity studies have been performed using crude extracts; hence, only a few of the effects have been associated with the active substances identified, e.g. antibacterial activities with piptamine or polyporenic acids. With a few exceptions, we still do not know the mechanisms underlying the biological activities. Verification of biological activities in in vivo and clinical studies is also required. The further research could contribute to better exploitation of the F. betulina application potential.

Compliance with ethical standards

Competing interests

The authors have no conflict of interest to declare.

References

Dresch P, D'Aguanno MN, Rosam K, Grienke U, Rollinger JM, Peintner U. Fungal strain matters: colony growth and bioactivity of the European medicinal polypores [[Fomes fomentarius, Fomitopsis pinicola and Piptoporus betulinus. AMB Express. 2015;5:4. doi: 10.1186/s13568-014-0093-0. PMC free article] [PubMed] [CrossRef] Google Scholar]

Fungorum I (2016) http://www.indexfungorum.org. Accessed 29 Nov 2016

Giles R, Parrow M (2011) Lignocellulosic treatments and applications thereof. United States Patent Application Publication US 20110008384 A1

Grishin AA, Lutskii VI, Penzina TA, Dudareva LV, Zorina NV, Polyakova MS, Osipenko SN. Composition of the supercritical CO[₂ extract of the fungus Piptoporus betulinus. Chem Nat Compd. 2016;52:436-440. doi: 10.1007/s10600-016-1667-7. [CrossRef] Google Scholar]

Grün CH (2003) Structure and biosynthesis of fungal α-glucans. Dissertation, University of Utrecht

Hibbett DS, Thorn RG. Basidiomycota: homobasidiomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA, editors. Systematics and evolution, the Mycota VII Part B. Berlin Heidelberg: Springer-Verlag; 2001. pp. 121-168. [Google Scholar]

Jelsma J, Kreger DR. Polymorphism in crystalline (1→3)-α-d-glucan from fungal cell-walls. Carbohydr Res. 1979;71:51-64. doi: 10.1016/S0008-6215(00)86060-7. [[PubMed] [CrossRef] Google Scholar]

Lemieszek MK (2008) The estimation of biological activity of water extracts from Piptoporus betulinus and Inonotus obliquus. Dissertation, Maria Curie-Skłodowska University, Lublin, Poland

Lomberh ML, Solomko EF, Buchalo AS, Kirchhoff B (2002) Studies of medicinal mushrooms in submerged cultures. In: Sanchez et al. (eds) Mushroom biology and mushroom products. The 4th international conference on mushroom breeding and mushroom products. pp 367-377

Lucas EH (1960) Folklore and plant drugs. Papers of the Michigan Academy of Science, Arts, and Letters XLV, 127-136

Peintner U, Pöder R. Ethnomycological remarks on the Iceman's fungi. In: Bortenschlager S, Oeggl K, editors. The Iceman and his natural environment. Vienna: Springer; 2000. pp. 143-150. [Google Scholar]

Pleszczyńska M, Wiater A, Janczarek M, Szczodrak J. (1→3)-α-d-Glucan hydrolases in dental biofilm prevention and control: a review. Int J Biol Macromol. 2015;79:761-778. doi: 10.1016/j.ijbiomac.2015.05.052. [[PubMed] [CrossRef] Google Scholar]

Pleszczyńska M, Wiater A, Siwulski M, Lemieszek MK, Kunaszewska J, Kaczor J, Rzeski W, Janusz G, Szczodrak J. Cultivation and utility of [[Piptoporus betulinus fruiting bodies as a source of anticancer agents. World J Microbiol Biotechnol. 2016;32:151. doi: 10.1007/s11274-016-2114-4. PMC free article] [PubMed] [CrossRef] Google Scholar]

Przybył K, Żłobińska-Podejma M. Effects of some bacteria [Pseudomonas spp. and Erwinia herbicola on in vitro growth of Piptoporus betulinus. For Pathol. 2000;30:321-328. doi: 10.1046/j.1439-0329.2000.00215.x. [CrossRef] Google Scholar]

Reh U, Kraepelin G, Lamprecht I. Use of differential scanning calorimetry of structural analysis of fungally degraded wood. Appl Environ Microbiol. 1986;52:1101-1106. [[PMC free article] [PubMed] Google Scholar]

Reis FS, Pereira E, Barros L, Sousa MJ, Martins A, Ferreira IC. Biomolecule profiles in inedible wild mushrooms with antioxidant value. Molecules. 2011;16:4328-4338. doi: 10.3390/molecules16064328. [[PMC free article] [PubMed] [CrossRef] Google Scholar]

Riley R, Salamov AA, Brown DW, et al. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci. 2014;111:9923-9928. doi: 10.1073/pnas.1400592111. [[PMC free article] [PubMed] [CrossRef] Google Scholar]

Semerdžieva M, Veselský J. Léčivé houby dřive a nyni. Praha: Academia Praha; 1986. [Google Scholar]

Song Z, Kennedy PG, Liew FJ, Schilling S. Fungal endophytes as priority colonizers initiating wood decomposition. Funct Ecol. 2016 [Google Scholar]

Stamets PE (2011) Antiviral activity from medicinal mushrooms. United States Patent Application Publication US 20110008384 A1

Stamets PE (2014) Antiviral and antibacterial activity from medicinal mushrooms. United States Patent Application Publication US 201440105928 A2

Valášková V, Baldrian P. Estimation of bound and free fractions of lignocellulose-degrading enzymes of wood-rotting fungi [Pleurotus ostreatus, Trametes versicolor and Piptoporus betulinus. Res Microbiol. 2006;157:119-124. doi: 10.1016/j.resmic.2005.06.004. [PubMed] [CrossRef] Google Scholar]

Wandokanty F, Utzig J, Kotz J. The action of hydrolysates of [Poria obliqua and Polyporus betulinus on malignant neoplastic cells. Med Weter. 1954;10:603-605. Google Scholar]

Wandokanty F, Utzig J, Kotz J. The effect of [Poria obliqua and Polyporus betulinus on spontaneous cancer of the dog with respect to breast cancer in dogs. Med Weter. 1955;3:148-151. Google Scholar]

Wasson RG. Soma: divine mushroom of immortality. New York: Harcourt, Brace & World; 1969. [Google Scholar]

Wasyl A (2006) Evaluation of neurotrophic properties of ethanol and ether extracts from polyporous bracket fungi Piptoporus betulinus (Bull. Ex Fr.) P. Karst in in vitro model. Dissertation, Maria Curie-Skłodowska University, Lublin, Poland

Wiater A, Paduch R, Pleszczyńska M, et al. α-(1→3)-d-Glucans from fruiting bodies of selected macromycetes fungi and the biological activity of their carboxymethylated products. Biotechnol Lett. 2011;33:787-795. doi: 10.1007/s10529-010-0502-7. [[PubMed] [PMC free article] [CrossRef] Google Scholar]

Zwolińska K (2004) Evaluation of anticancer activity of extracts from birch polypore Piptoporus betulinus (Bull. ex Fr.) P. Karst. Dissertation, Maria Curie-Skłodowska University, Lublin, Poland

Żyła M (2005) Comparison of antitumor activity of extracts from Piptoporus betulinus, Fomes fomentarius and Inonotus obliquus. Dissertation, Maria Curie-Skłodowska University, Lublin, Poland

Articles from World Journal of Microbiology & Biotechnology are provided here courtesy of Nature Publishing Group

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Fomitopsis betulina (formerly Piptoporus betulinus): the Iceman's polypore fungus with modern biotechnological potential

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Higher Basidiomycota have been used in natural medicine throughout the world for centuries. One of such fungi is Fomitopsis betulina (formerly Piptoporus betulinus), which causes brown rot of birch wood. Annual white to brownish fruiting bodies of the ...

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The root endophytes Trametes versicolor and Piriformospora indica increase grain yield and P content in wheat

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The root endophytes Trametes versicolor and Piriformospora indica increase grain yield and P content in wheat

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The root endophytes Trametes versicolor and Piriformospora indica increase grain yield and P content in wheat - Plant and Soil

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Background and Aims Soil phosphorus (P) deficiency occurs in many developing and transition countries. One method of resolving soil P deficiency is a strong application of mineral and organic fertilizers in order to saturate the P binding capacity of soil. Another promising method is the implementation of crop-endophyte symbioses in combination with the application of smaller amount of P fertilizer. This study comparatively examined the effect of the fungal endophytes Trametes versicolor and Piriformospora indica in P-deprived and P-rich conditions on P uptake and yield in wheat (Triticum aestivum L., cv. Bobwhite). Methods Three-day-old wheat seedlings were dip-inoculated with mycelia of (a) T. versicolor WC16GW axenically isolated from Galium album, a dicotyledonous plant obtained from grassland in Linden near Giessen, Germany, and (b) axenic cultures of P. indica DSM 11827 freshly re-isolated from surface-sterilized barley roots. Seedlings were subsequently grown in 6 l Mitscherlich pots (eight seedlings per pot) in soil containing mono-calcium phosphate [CP, Ca (H2PO4)2] with 100 mg P kg−1 soil and control (CO) with 6.3 mg CAL-P kg−1 soil P in an open-air pot experiment station for three months. Results Colonization of wheat roots by T. versicolor and P. indica increased plant biomass, yield and P content. T. versicolor-colonized plants exhibited a significant increase in grain yield of 37% (CO treatment) and 8.5% (CP treatment), as well as straw yield of 27% (CO treatment) as compared to non-colonized plants. P. indica-colonized plants showed a significant increase in grain yield of 10% under high P (CP treatment) and straw yield of 22% (CO treatment). Moreover, P. indica improved grain P content by 30% (CO treatment), 16% (CP treatment) and straw P content by 33% (CO treatment), while T. versicolor increased grain P content by 16% (CP treatment) and straw by 35% (CP treatment). Conclusions Both T. versicolor and P. indica improved wheat P uptake in both P-deprived and P-rich conditions. T. versicolor supported a high grain yield under the CO and CP treatments, suggesting this fungus has a promising potential for P management in cereal crops.

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Ecovative unlocks the power of mycelium to grow better materials – and your business.

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Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities

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Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities

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Abstract

Adaptive behaviour of plants, including rapid changes in physiology, gene regulation and defence response, can be altered when linked to neighbouring plants by a mycorrhizal network (MN). Mechanisms underlying the behavioural changes include mycorrhizal fungal colonization by the MN or interplant communication via transfer of nutrients, defence signals or allelochemicals. We focus this review on our new findings in ectomycorrhizal ecosystems, and also review recent advances in arbuscular mycorrhizal systems. We have found that the behavioural changes in ectomycorrhizal plants depend on environmental cues, the identity of the plant neighbour and the characteristics of the MN. The hierarchical integration of this phenomenon with other biological networks at broader scales in forest ecosystems, and the consequences we have observed when it is interrupted, indicate that underground 'tree talk' is a foundational process in the complex adaptive nature of forest ecosystems.

Introduction

A mycorrhiza is typically a mutualistic symbiosis between a fungus and a plant root, where fungal-foraged soil nutrients are exchanged for plant-derived photosynthate ( Smith and Read 2008). The extent of fungal mycelium in the soil is vast and the mutualisms between the fungal species and host plants are usually diffuse, enabling the formation of mycorrhizal networks (MNs). These MNs are composed of continuous fungal mycelia linking two or more plants of the same or different species. The MN can thus integrate multiple plant species and multiple fungal species that interact, provide feedbacks and adapt, which comprise a complex adaptive social network. The MN is considered ecologically and evolutionarily significant because of its positive effects on the fitness of the member plants and fungi. Our understanding of this significance derives from evidence that MNs influence the survival, growth, physiology, health, competitive ability and behaviour of the plants and fungi linked in the network. How the MN affects the member plants and fungi is increasingly understood to involve plant-fungal-plant communication, and may involve biochemical signalling ( Song et al. 2010; Babikova et al. 2013), resource transfers ( Francis and Read 1984; , ; He et al. 2009; Teste et al. 2009) or action-potential-driven electrical signals ( Baluŝka et al. 2006; Kai et al. 2009). The responses of the plants and fungi to this communication are rapid, and thus can be described as behavioural responses, allowing us to refocus our understanding of the significance of MNs through the lens of plant behaviour. Here, we provide insight into the mechanisms and conditions through which MNs may influence plant behaviour, and discuss the potential circumstances and consequences for the ecology of plant communities and the evolution of plant-fungal interactions. We finish with a discussion of how MN influences on plant behaviour are congruent with viewing plant communities as complex adaptive systems. Gaps in our understanding of these patterns and processes are highlighted.

Mycorrhizas

Mycorrhizal associations of plants have large-scale ecosystem-wide consequences ( Averill et al. 2014; Dickie et al. 2014). The magnitude of their importance is likely due to the proclivity of most terrestrial plants to form them ( Smith and Read 2008; Brundrett 2009). The origins of this symbiosis are thought to be ancient and have been proposed as a mechanism for facilitating land colonization by plants 400 Mya ( Redecker et al. 2000; Humphreys et al. 2010). The mycorrhizal symbiosis is a many-to-many relationship: plants tend to form symbioses with a diverse array of fungal species (broad host receptivity) and likewise, fungal species tend to be able to colonize plants of different species (broad host range). While most mycorrhizal fungi are broad host generalists, forming diffuse mutualisms, a few appear to be specialists, occurring exclusively on a single host ( Lang et al. 2011).

Plant species tend to display fidelity to specific classes of mycorrhizal fungi, and entire ecosystems are often dominated by one class or the other. By far the most ubiquitous class is arbuscular mycorrhizal fungi (AMF), obligate biotrophs in the Glomeromycota that form arbuscules and sometimes vesicles within the root cells of hosts ( Smith and Read 2008). Arbuscular mycorrhizal fungal symbioses dominate temperate grasslands, tropical forests and agricultural systems, but also associate with some temperate forest trees, such as members of the Cupressaceae and Aceraceae families ( Brundrett 2009). The AMF are microscopic with few morphological features to distinguish between species, and are classified by spore appearance and molecular markers ( Rosendahl 2008), and continue to stir controversy due to the atypical genetics of these fungi ( Koch et al. 2004).

The other major class of mycorrhizas is the ectomycorrizal fungal (EMF) class. Although fewer plant species have been found to form symbioses with EMF, in comparison to AMF ( Brundrett 2009), the hosts of EMF tend to be widely dispersed, abundant and dominant members of their assemblages. For example, EMF hosts include most coniferous trees (all of the Pinaceae), the majority of woody shrub species in temperate and boreal forests and the Dipterocarpaceae, which results in EMF also being common in tropical forests. Root tips harbouring EMF are distinguishable by macroscopic features ( Peterson et al. 2004) including: (i) the mantle (a fungal sheath that encases a colonized root tip) and (ii) extramatrical mycelium (diffuse hyphae that extend out into the surrounding soil). Some species of EMF form epigeous mushrooms and others form hypogeous truffles, predominantly from the phyla Basidiomycota and Ascomycota. Ectomycorrizal fungi appear to have evolved separately in multiple plant families, with as many as 66 incidences identified thus far from phylogenetic evidence ( Tedersoo et al. 2010). Some exceptional plant families and genera are capable of forming viable symbioses with EMF and AMF simultaneously (e.g. Salicaceae, Eucalyptus). Whether an ecosystem is dominated by AMF or EMF associations has large-scale consequences for resource availability, as AMF systems have been recently demonstrated to have lower soil C : N ratios than those dominated by EMF, indicating fundamentally different nutrient cycling regimes, resulting in more carbon sequestered in EMF forests ( Averill et al. 2014).

Both EMF and AMF fungi have been demonstrated to form networks. Their structure and known associations are noted here to highlight the differences between them, and to point out that despite these differences, they both appear to be able to affect plant behaviour changes through the formation of networks. We do not fully explore the potential mechanisms by which communication is occurring through mycorrhizas, as this topic is reviewed elsewhere ( Barto et al. 2012); rather, we synthesize the evidence for and consider the potential extent and ecosystem consequences of this phenomenon.

Mycorrhizal Networks: Structure and Function

An MN is formed when multiple plants are linked belowground by a continuous AMF ( Kiers et al. 2011) or EMF mycelium ( van der Heijden and Horton 2009; Beiler et al. 2010) (Fig. 1). Networks can be exclusive to a subset of plants able to form mycorrhizas with the same fungi, potentially linking members of a single species [for example Beiler et al. (2010)]. The MN can also be inclusive, as may be the case for AMF systems, where linkages can occur between multiple plant and fungal species ( Molina et al. 1992). Evidence for the occurrence of MNs has been accumulating for half a century ( Björkman 1970; Reid and Woods 1969; Francis and Read 1984; Newman 1988), but their significance for ecosystems has been pursued intensively only in the past two decades (; Fitter et al. 1998). We now know that MNs can influence plant establishment ( Dickie et al. 2002; Nara 2006), survival ( Horton and Bruns 2001; Teste et al. 2009; Bingham and Simard 2011), physiology ( Wu et al. 2001, 2002), growth ( Teste et al. 2010) and defence chemistry ( Song et al. 2010, 2014; Babikova et al. 2013). This influence is thought to occur because the MN serves either as a pathway for interplant exchange of resources and stress molecules or as a source of fungal inoculum (Fig. 1) (see reviews by Simard et al. 2012, 2013, 2015). For instance, anastomosis with existing MNs of established plants is considered the most common mechanism for mycorrhizal fungal colonization of regenerating plants in situ ( van der Heijden and Horton 2009; Kariman et al. 2012). Colonization of establishing seedlings by MNs enables them to acquire sufficient soil nutrients for root and shoot growth and hence survival ( Teste et al. 2009; Kariman et al. 2012).

As with mycorrhizal colonization, interplant resource and signal fluxes through MNs have the potential to alter plant behaviour. These fluxes have been shown to include carbon (, ), water ( Egerton-Warburton et al. 2007; Bingham and Simard 2011), nitrogen ( Teste et al. 2009), phosphorus ( Eason et al. 1991), micronutrients ( Asay 2013), stress chemicals ( Song et al. 2010, 2014; Babikova et al. 2013) and allelochemicals ( Barto et al. 2011), and can occur between plants of the same or different species. Understanding the potential effects of these fluxes on plant behaviour, however, first requires an understanding of transfer processes, and the factors that regulate these processes. For instance, interplant resource exchanges are thought to be regulated by source-sink relationships within the MN, where one plant that is rich in nutrients serves as a source (donor) of compounds for a neighbouring plant that is poor in nutrients, which thus serves as a sink (receiver) ( Simard et al. 2012). The long-distance transport of carbon and/or nutrients appears to occur predominantly by advective mass flow driven by the source-sink gradient generated by these interplant nutrient differences ( Simard et al. 2012). Mass flow can also be generated by fungal mycelium growth, and diffusion or active transport mechanisms may operate during active fungal cell expansion at growing mycelium fronts ( Heaton et al. 2012).

The primary importance of plant-sink strength in governing the magnitude and direction of resource transfer through MNs is illustrated in studies showing transfer of carbon to rapidly growing EMF saplings with high transpiration rates, or to shaded EMF seedlings with high respiration demands for survival and growth ( Read and Bajwa 1985; ; Teste et al. 2009, 2010). Organic compounds are thought to enter the transpirational stream of the receiver plant via the xylem, and then be actively transported to rapidly expanding biosynthetic tissues. Plant source strength also drives transfer under certain conditions. This was demonstrated in the rapid transfer of labile carbon from the roots of injured EMF seedlings to healthy neighbours ( Song et al. 2014), and in the transfer of nitrogen from N ₂-fixing or fertilized source plants to non-N ₂-fixing sink plants ( He et al. 2009). Increasing source strength by CO ₂ fertilization of plants in AMF networks, in contrast, has had no effect on carbon transfer ( Fitter et al. 1998). Although either source or sink strength may dominate under certain circumstances, it is more likely that the simultaneous behaviour of both source and sink plants (and sources and sinks within the mycelium itself) influences carbon and nutrient transfer through MNs. For instance, the direction and magnitude of carbon transfer changed over a growing season due to simultaneous changes in phenology, and hence source and sink strength, of different plants involved in an EMF network in mixed temperate forest ( Philip 2006) and Low Arctic Tundra ( Deslippe and Simard 2011). Carbon and nitrogen are thought to travel through MNs together in simple amino acids ( Simard et al. 2015). These molecules travel through the MN rapidly, moving from donor plants to the fungal mycelium within 1 or 2 days ( Wu et al. 2002; Heaton et al. 2012) and to the shoots of neighbouring plants within 3 days ( Wu et al. 2002).

Using experimental designs that prevent the aboveground transfer of volatile organic compounds (VOCs), as well as controlling for the formation of an MN, stress signals have been shown to transfer from injured to healthy plants through MNs even more rapidly than carbon, nutrients or water. Herbivore- and pathogen-induced stress responses were up-regulated in undamaged neighbours in as little as 6 h following insect or fungal infestation of donor plants linked in AMF MNs ( Song et al. 2010, 2014; Babikova et al. 2013). Song et al. (2014) found up-regulation of four defence-related genes in healthy neighbours 6 h after AMF tomato donors were infested with the leaf-chewing caterpillar Spodoptera litura Fabricius, likely in response to signalling via the jasmonate pathway through the MN. They showed that production of defence enzymes increased receiver resistance to pests, as indicated by lower weight gain and hence lower fitness of the herbivore. In an earlier study, Song et al. (2010) infested AMF tomato plants with the foliar necrotrophic fungus, Alternaria solani, and similarly found that six defence genes encoding for defence enzymes were activated after 65 h in the un-infested neighbours. In this study, the use of mutant controls and the genes that were up-regulated suggested that salicylic acid and jasmonic acid pathways were involved in signalling (or signal detection 'eves-dropping') through the MN. In an MN linking EMF Douglas-fir and ponderosa pine, defoliation of Douglas-fir with the insect Choristoneura occidentalis (western spruce budworm) induced defence enzyme production in neighbouring linked ponderosa pine within 24 h of infestation ( Song et al. 2015). These studies clearly show a rapid physiological response of recipient plants to stress signalling transmitted through MNs, even in plants of a different genus, indicating a shift in plant behaviour to protect fitness.

Plant Behaviour

Plant behaviour is defined as a change in plant morphology or physiology in response to environmental stimuli, including responses to chemicals, light and water, that occurs within a plant's lifetime ( Karban 2008). Phenotypic plasticity, the ability of an individual to alter its traits in response to the environment, is a defining feature of plants. McNickle et al. (2009) define behaviour as the expression of plant plasticity that is like a decision point, where each choice involves trade-offs that will affect fitness. The most studied plant behaviours involve alteration of aboveground morphology to optimize access to sunlight ( Smith 2000; Novoplansky 2009), or of reproductive or defensive traits to deal with environmental heterogeneity ( Karban 2008). Plant behaviour responses can also occur belowground, in foraging for nutrients and water ( Hodge 2004) and in response to root competition ( Cahill et al. 2010). Since all forest plants form obligate symbioses with mycorrhizal fungi, plant behavioural responses must also include any physiological changes due to their mycorrhizal status (e.g. changes in fine root morphology and/or production following fungal colonization). The relative speed of the change, the presence of stimuli and non-permanence of the change (e.g. short-term production of defence chemicals) distinguish plant behaviour from other chemically mediated processes ( Karban 2008).

Mycorrhizal Network Effects on Plant Behaviour

Plants that are connected via an MN can rapidly modify their behaviour in response to fungal colonization and interplant biochemical communication. Plant behavioural responses that have been measured thus far include rapid changes in mycorrhizal colonization, root growth, shoot growth, photosynthetic rate, foliar nutrition, foliar defence chemistry and defence response (Fig. 1, Table 1). For instance, plant hosts have responded to mycorrhizal colonization via MNs by adjusting production of fine roots (e.g. Pickles et al. 2010), probably due to the production of plant auxins, and this has been noted in both EMF ( Frankenberger and Poth 1987; Gay et al. 1994; Karabaghli-Degron et al. 1998; Scagel and Linderman 1998; Felten et al. 2010) and AMF systems ( Hanlon and Coenen 2011). These varied types of plant behavioural responses have occurred in cases where the neighbouring plants linked in the MN (i) are of the same or different species and (ii) are kin (of the same parental lineage) or strangers. These observations raise questions about the evolutionary consequences of MN-related interactions. Plant behavioural changes have qualities and quantities that can substantially alter the community ecology of a site, including intra- and interspecific interactions, species co-existence and biodiversity. Changes to the fitness of connected neighbouring plants and associated organisms can also have ecosystem-wide impacts. In this section, we discuss evidence that MNs can influence plant behaviour, with ripple effects on plant community and ecosystems ecology.

The impacts of MN-mediated resource transfer on plant behaviour are evident in the regeneration success of mono-specific and mixed forests. In the interior Douglas-fir forests of western North America, the transfer of carbon, nitrogen and water from older trees to regenerating seedlings through an MN has been associated with rapid increases in net photosynthetic rates ( Teste et al. 2010), shoot water relations ( Schoonmaker et al. 2007) and shoot and root growth of the young seedlings ( Teste et al. 2009). These responses were linked to improved seedling survival and productivity, and hence regenerative capacity of the forest. Whether they were caused by the observed carbon, nitrogen or water transfer, or by some other facilitative effect of the MN, remains unknown. However, similar shifts in Douglas-fir seedling behaviour in response to MNs have been repeatedly observed in a range of regional climates ( Simard et al. 2012). In a separate study, water transfer from replete to drought-stressed conspecifics through MNs was also associated with increased growth ( Bingham and Simard 2011). Here, the receiver seedlings accessed water through the MN, allowing them to modify root and shoot growth that resulted in increased survival. Under the drought conditions in this study, carbon transfer did not co-occur with water transfer, indicating plasticity in plant behavioural responses to limiting resources.

Thus far, we have presented only one-sided behavioural responses of plants to resource transfers in MNs (i.e. responses of plants that are recipients of resource transfers or stress signals). This is partly an outcome of study objectives, where experiments were designed to test receiver plant behaviour responses, but may also reflect the importance of relative source and sink strengths within an MN. In a study of AMF networks, for example, Walder et al. (2012) demonstrated that flax donated relatively little carbon while receiving 94 % of its nitrogen and phosphorus from the MN, whereas sorghum invested significant amounts of carbon while gaining little, translating into no positive growth effects for sorghum. Interestingly, however, the two plants grown in mixture were more productive relative to when they were grown in monocultures, suggesting unmeasured benefits resulting from linkage to the MN. Likewise, Douglas-fir grew larger when in mixture with linked ponderosa pine, likely due to modified growth behaviour to gain access to excess phosphorus via the MN that would otherwise have been consumed by ponderosa pine as 'luxury consumption' ( Perry et al. 1989). Asymmetrical benefits have also been evident in interspecific carbon transfer from paper birch to Douglas-fir in the summer, with increasing net transfer with shading of Douglas-fir (). Regardless of the net effects of carbon transfer through the MN, both Douglas-fir and paper birch benefitted from growing in mixture versus monoculture through increased productivity ( Sachs 1996), and from increased resistance to Armillaria root disease ( Baleshta et al. 2005), possibly due to a greater population size of the pathogen-antagonistic rhizosphere microbe, Pseudomonas fluorescens ( DeLong et al. 2002). These studies show that plant behavioural responses to resource transfer via MNs are dynamic, asymmetrical at times and dependant on the identity of the plants, the source-sink patterns in the MN and the environmental conditions of the system ( Hynson et al. 2012).

Defence signals travelling through the MN clearly result in rapid behavioural responses of recipient plants, and this is evident in sudden changes in foliar defence chemistry ( Babikova et al. 2013; Song et al. 2015) and pest resistance ( Song et al. 2010, 2014) (see above). For instance, broad beans ( Vicia faba) responded to aphid attack by swiftly transferring defence signals via the MN to neighbouring bean plants, which responded in turn by producing aphid-repellent chemicals and aphid-predator attractants ( Babikova et al. 2013). These higher order interactions represent trophic cascades generated by pest infestation triggering signal propagation through the MN. In a different study, defoliation of Douglas-fir resulted in simultaneous transfer of defence signals and carbon to neighbouring healthy ponderosa pine through MNs, resulting in increased defence enzyme production by ponderosa pine, possibly orchestrated by the networking fungus as a strategy to protect itself against the loss of healthy hosts ( Song et al. 2015). Responses to pest infestations can also lead to larger-scale generational changes in the behaviour of plant-symbiont systems. Shifts in ectomycorrhizal community composition caused by a variety of factors, such as host mortality (e.g. pine beetle outbreaks; Kurz et al. 2008), can result in legacy effects that impact future generations of the host species ( Karst et al. 2015). For example, in areas of western North America dramatically impacted by the mountain pine beetle-induced dieback of lodgepole pine ( Pinus contorta), EMF have declined significantly ( Treu et al. 2014). Seedlings grown in soils from beetle-attacked pine stands expressed both reduced biomass and reduced production of monoterpenes compared with those grown in soil from undisturbed pine stands, revealing a transgenerational cascade mediated by fungal symbionts ( Karst et al. 2015).

In addition to nutrients and defence chemicals, allelochemicals have also been shown to travel between plants through hyphal mycelia ( Barto et al. 2011; Achatz et al. 2014), revealing that not all chemicals moving through the MN benefit the receiving plant. Barto et al. (2011) demonstrated that MNs facilitated the transport of natural allelochemicals, thiophenes, as well as the herbicide, imazamox, resulting in decreased growth in receiver plants. Likewise, tomato plants received more jugalone, an allelochemical, and responded with reduced growth when connected to an MN when compared with control treatments lacking an MN ( Achatz et al. 2014). These examples of amensalism demonstrate that MNs can serve as couriers for biochemical warfare, or negative feedback, from one plant species to another. In previous studies, allelochemicals, demonstrated under laboratory conditions to reduce vigour and growth of recipient plants, were discounted as having meaningful impact in situ due to the assumption that they were transmitted through aerial release ( Duke 2010). In this manner, they would dilute quickly, precluding a targeted attack. The targeted delivery through an MN, however, demonstrates the important role of MNs in isolating plant behavioural responses to allelochemicals. Thus, the ability of the MN to facilitate allelochemical delivery represents a higher order interaction with direct impacts on the behaviour of the sender and receiver plants.

Mechanisms for Adaptive Behaviour

Plant genotypes have shown heritability for mycorrhizal fungal traits (; Temel et al. 2005) and vice versa (), indicating a mechanism by which MNs play a role in host fitness and adaptive behaviour. At the most basic level, the type of association, whether AMF or EMF, depends on the identity of the plant. Further, within those categories, some plants will associate with a subset of fungal species ( Brundrett 2009). The spectrum of symbiotic relationships can range from mutualistic, where both partners benefit, or commensal, where one partner benefits while the other is unaffected, to parasitic where one partner exploits the other ( Egger and Hibbett 2004). These are expressed in plant adaptive behaviours such as survival, longevity, growth, physiology, carbon allocation or reproduction. A fungus can express a mutualism with one plant, while simultaneously exploiting a different plant. Mycoheterotrophic plants are perhaps the most extreme example of this type of exploitation, where a plant acquires all of its carbon by parasitizing fungi through the MN (e.g. Leake 1994; Massicotte et al. 2012). These plants link into the MN of a nearby tree and siphon off photosynthate, enabling them to survive and grow. Importantly this reveals the existence of a mechanism by which plants can acquire nutritional levels of carbon from mycorrhizal fungi. The fitness of all participants in this scenario is increased by the existence of the MN: (i) the mycorrhizal fungus acquires carbon from the tree (or multiple trees) and may use the mycoheterotroph as the staging ground for long-distance exploration and colonization, (ii) the mycoheterotroph acquires carbon from the fungus and (iii) the tree gains access to a wider pool of soil resources, and potentially connection to other trees facilitating the detection of defence signals.

The relatedness of neighbours in mono-specific plant communities can also influence whether MNs will elicit adaptive behavioural changes. For example, foliar nutrition in AMF Ambrosia artisifolia L. improved when it was integrated into an MN with related plants but not conspecific strangers ( File et al. 2012). Likewise, in mono-specific pairs of EMF interior Douglas-fir grown in greenhouse conditions, foliar micronutrients were increased in kin compared with strangers grown with older conspecifics ( Asay 2013). This appears to be linked with mycorrhizal association of this system as mycorrhizal colonization was also elevated in kin seedlings ( File et al. 2012; Asay 2013). These findings reveal that MNs can play an integral role in kin selection, but the exact mechanisms by which they do this are unclear. However, there is strong evidence that biochemical signals derived from mycorrhizas or roots are involved. For example, Semchenko et al. (2014) showed that root exudates carried specific information about the genetic relatedness, population origin and species identity of neighbours, and locally applied exudates triggered different root behaviour responses of neighbours. This included increased root density, achieved through changes in morphology rather than biomass allocation, suggesting the plants limited the energetic cost of their behaviour.

Because the overwhelming majority of plants are predominantly mycorrhizal in situ, any root exudates involved in kin recognition are likely to be filtered through mycorrhizal fungi. In a recent study using stable-isotope probing, we found that MNs transmitted more carbon from older 'donor' Douglas-fir seedlings to the roots of younger kin 'receiver' seedlings than to stranger 'receiver' seedlings, suggesting a fitness advantage to genetically related neighbours (Pickles et al. unpubl.). This may have been facilitated by the greater mycorrhizal colonization of kin than stranger seedlings ( Asay 2013), creating a stronger sink in the MN, an effect also noted in the study by File et al. (2012). The greater colonization of kin seedlings may have arisen from complimentary genetics of the fungal genet and tree genotype (e.g. , ). In order to establish a mutualism, fungi must overcome a tree's pathogen defence system, which involves the activation of genes to express specific enzymes. Recent work has shown that the EMF species Laccaria bicolor secretes an effector protein (MiSSP7) that suppresses host jasmonic acid production, a typical host defence response that interferes with fungal infection, with the effect of enhancing L. bicolor colonization of host roots ( Plett et al. 2014). Furthermore, Populus host plants have been shown to induce the production of MiSSP7 in L. bicolor through flavonoids present in their root exudates ( Plett and Martin 2012). Taken together these findings reveal one mechanism by which plants actively communicate with fungal symbionts to encourage root colonization, with direct consequences for plant behaviour. Thus, related plants may more easily establish mutualisms as a result of the priming effects of root exudates (e.g., Semchenko et al. 2014), which may also lower the resource costs of enzyme production, or promote genotypic complementarity between hosts and co-adapted fungal associates. More research is needed to clarify the role of each player in this system. Nonetheless, kin selection is occurring as evidenced by kin versus stranger behaviour differences, and is connected to the formation of MNs, although the mechanism through which the MN elicits the behaviour response remains to be resolved.

Evolution of MN-Mediated Plant Behaviour

The evolutionary ecology of MNs and the consequences for plant and fungal fitness has been discussed both in terms of individual selection and multi-level or group selection ( Perry 1995; Wilkinson 1998; Babikova et al. 2013; Johnson and Gilbert 2015). In this section, we revisit these discussions with evidence from our own research investigating the MN effects on plant behaviour. The questions, rephrased from Perry (1995), are: Why should a plant support a mycorrhizal fungus that provides carbon (or nutrients or defence signals) to a competing plant? Why would a fungus pass carbon it acquires from one plant to another plant? Upon reviewing the evidence, we agree with Wilkinson (1998) that individual selection appears sufficient to explain evolution within MNs, but we also concur with Perry (1995) and Whitham et al. (2006) that this individual selection can occur within a community context. Several explanations for this are possible, and it is reasonable that a plurality of mechanisms occurs, but the relative contribution of one over the other may vary depending on the conditions of the MN.

Assuming that selection occurs at the individual or gene level, we suggest two possible reasons why a plant would support a fungus that then passes its carbon to another plant. First, if seed dispersal from the parent is limited, as we know is the case in forests ( Perry et al. 2008), then there could be a high degree of relatedness between parent trees and neighbouring seedlings. Given that nearby neighbours are more likely to be relatives, a plant may pass carbon to an MN that then passes it to a relative, resulting in kin selection. This is inclusive fitness, where it is beneficial to a plant to ensure the shared genes of a related neighbour are passed on, provided the cost to the parent individual is not too high. The occurrence of kin selection in conifers, and the involvement of mycorrhizal fungi in the mechanism, has been demonstrated in our studies with Douglas-fir. We found greater mycorrhizal colonization, micronutrient levels ( Asay 2013) and twice as much carbon transferred from established Douglas-fir to nearby kin than stranger neighbours (B. J. Pickles et al. unpubl.). This suggests that Douglas-fir trees connected in a Rhizopogon network in mono-specific stands ( Beiler et al. 2010) may behave much like a clonal plant, shuttling resource across the network to related plants in need, increasing the fitness of the evolving genotype. Congruently, we have also found large amounts of carbon (5 % of total photosynthesis) passed through the MN between Betula nana plants that are clonal in the Low Arctic Tundra. This carbon transfer appears to be supporting the expansion of related clones through the tundra during warmer periods of the growing season ( Deslippe and Simard 2011). But what if the recipient plants are unrelated-that is, they are neither kin seedlings nor ramets? We have found that carbon, albeit in small amounts, can pass from mature Douglas-fir trees through MNs to unrelated Douglas-fir seedlings ( Teste et al. 2009). Could the transfer of carbon to unrelated seedlings simply be a cost of being linked into MN, or do the donor trees have any control over where and how much carbon is transferred? Our studies point to the latter. Teste et al. (2009, 2010) found that Douglas-fir trees transferred more carbon and nitrogen to neighbouring seedlings where the donor tree was larger or the receiver seedlings had a greater demand. Moreover, we have found that Douglas-fir transferred net amounts of carbon to neighbours of a different species, paper birch, which then passed the net amounts of carbon back to Douglas-fir at a different time of year ( Philip 2006) and when it was under increasing shade (). These studies demonstrated that the amount of carbon transferred depended on the strength of the sink and the input of the donor ( Teste et al. 2009, 2010), and thus suggest a degree of control by the donor over the amount of carbon passed to the networking fungi, where the donor may donate excess photosynthate to the MN where it is then shuttled based on strength of the sink ( Simard et al. 2012). From the plant's perspective, the second reason why it would pass carbon to its networking fungus that then passes it to an unrelated plant individual is that there is an evolutionary advantage to the plant through support of the highly diverse and adaptive mycorrhizal symbionts in the MN. The generalist fungal species in the MN can rapidly evolve to the temporally and spatially diverse environment, providing a mechanism for the longer-lived plants and trees to cope with an uncertainty and variability ( Wilkinson 1998).

The second question, why a networking fungus would pass carbon from one plant to another, can also be explained by individual selection. If the networking fungus acquires more carbon from one plant than it requires for its own fitness, it can then supply the excess carbon to other networked plants in need, thus diversifying its carbon portfolio for insurance against potential loss of one of the hosts. This more secure carbon source from multiple plants is important to the fitness of the fungal species in variable environments ( Perry et al. 1989; Wilkinson 1998). From the fungal species perspective, the relatedness of plants involved in the network should be of no consequence, as long as a long-term carbon source is secured. Heil and Karban (2009) similarly suggest that interplant communication via VOC stress signals may be an unavoidable consequence of individual defence strategies or are an extension of within-plant signalling. Interestingly, the greater stability found in mixed species plant communities than monocultures ( Tilman et al. 2001; Perry et al. 2008) suggests that networking and communicating with multiple plant species is a lower risk strategy for the fungus in the MN than networking with only a single plant species. In support of this, we found that ponderosa pine received both carbon and defence signals from damaged neighbouring Douglas-fir through networking mycorrhizal fungi ( Song et al. 2015). Here, the networking fungus may have acted to protect its net carbon source, by allocating carbon and signals to the healthy, more reliable ponderosa pine. In unstable environments, such as ecosystems under stress and experiencing species turnover as a result of climate change, the MN may therefore benefit from transferring carbon and defence signals interspecifically, favouring hosts that can supply more carbon ( Kiers et al. 2011). Babikova et al. (2013) also suggested that allocating stress signals to plants that supply more carbon would benefit the fungus most. It is possible, therefore, that MN-based transfers and signals have evolved through costs and benefits to favour reciprocation, but also remain more generic among multiple plants species in stressful environments for long-term stability. Nothing is known about the specificity of transfer or signalling pathways through MNs ( Johnson and Gilbert 2015), but the differences in specificity of herbivores, and the differences in stability in mixed versus monoculture plant communities, provide fertile grounds for further research.

Group selection is considered to occur where natural selection expresses at the level of the group instead of the individual. It is thought possible where there is an organization of individuals into groups that have a complex social structure that promotes the fitness of group members. When considering that group selection occurs at the level of the species for the formation of groups, it is important to note that there is congruence between individual and group selection theory. Perry (1995) argues that evidence for group selection exists in cooperative guilds, where multiple plants are linked together by MNs for mutual aid. The guilds are then stabilized either through tit-for-tat relationships or reciprocal altruism between the plants and the fungi. It is through these internal relationships and positive feedbacks that the self-organizing behaviour of the guild or group develops. Cooperative guilds exist in communities, especially forests, where species share an ecological commons and experience stochastic disturbance that leads to hiatus in one or more plant species ( Perry 1995). There is evidence for both tit-for-tat and reciprocal altruism in MNs in forests, both which would be resistant to cheaters (i.e. individuals that benefit without reciprocating). Tit-for-tat, distinct from mutualisms, is evident in bidirectional transfer between paper birch and Douglas-fir (, ; Philip et al. 2010) and between unrelated Douglas-fir ( Teste et al. 2010). This cooperative bidirectional exchange occurs over a period of a few days and appears to be related to the behaviour and possibly fitness of the individuals involved in the network. However, reciprocal altruism, or repeated prisoners dilemma, occurs over longer time periods, and this explanation is more congruent with the highly variable disturbances and hiatus in forests. There is some evidence for reciprocal altruism through the switches in the direction of net carbon transfer between paper birch and Douglas-fir ( Philip 2006) or maple and trout lily seedlings ( Lerat et al. 2002) in response to differential changes in plant phenology over a period of several months. The hyperlinking that occurs in Douglas-fir- Rhizopogon networks also illustrates that topology of MNs is designed for such complex reciprocal exchanges between trees. The trees in these and other forests are considered foundational species ( Simard 2009), and the traits of foundational trees have been shown to have heritable effects on the associated networking mycorrhizal fungi (, ), bird and arthropod communities ( Whitham et al. 2006), soil microbes ( Schweitzer et al. 2008), and potentially gene regulation of connected neighbours connected ( Song et al. 2015) and the biochemistry of subsequent generations of seedlings ( Karst et al. 2015), suggestive of group selection. As such, group selection may help explain why forest productivity and tree disease resistance in communities of Douglas-fir, paper birch, their inter-linking mycorrhizal fungi and associative soil microbes are enhanced compared with monocultures of Douglas-fir alone ( Simard et al. 2005). However, studies are needed to test whether groups actually do benefit from MN-driven plant behaviour changes.

Complex Adaptive Systems

Underground 'tree talk' is a foundational process in the complex adaptive nature of forest ecosystems. Since plants form the basis of terrestrial ecosystems, their behavioural interactions, feedbacks and influences are important in generating the emergent properties of ecosystems ( Levin 2005). Given the connectivity inherent in the formation of MNs and the impressive array of plant behavioural interactions that can be mediated through them, plant behaviour and MNs are intricately linked. In the interior Douglas-fir forests of British Columbia, seedlings regenerate within the MN of old conspecific trees. The architecture of the MN is scale-free, where hub trees are highly connected relative to other trees in the forest ( Beiler et al. 2010), and this is characteristic of a complex adaptive system ( Simard et al. 2013; Beiler et al. 2015). The scale of the MN is at least on the order of tens of metres ( Beiler et al. 2010) and potentially much larger, with a single fungus sometimes spanning hundreds of hectares of forest ( Ferguson et al. 2003). Recent work on the diversity of plant-fungal connections in forests revealed multiple levels of nestedness in the associations between host plants and fungal symbionts ( Toju et al. 2014; Beiler et al. 2015). Each individual component (plant or fungus) of the ecosystem-wide network will, therefore, have a different potential to influence the behaviour of every other individual based on the extent, diversity and hierarchical level of its connections. As discussed above, the connections created by mycorrhizal fungi are agents for both positive ( Song et al. 2010) and negative ( Achatz et al. 2014) feedbacks to complex adaptive plant behaviour, which lead to self-organization of ecosystems ( Simard et al. 2013; Beiler et al. 2015). Resilience is an emergent property of the interactions and feedbacks in scale-free networks ( Levin 2005). Targeted loss of hub trees, however, can cross thresholds that destabilize ecosystems. Through the study of MNs, we are beginning to characterize the connections that are important to behaviour of system agents and thus ecosystem stability.

Future Research

With evidence emerging about the potential levels of connectivity in a forest, as well as the extent of the influence that an MN can have, further work to determine the drivers of the senders and receivers, and the nature of the couriers and messages along the mycorrhizal communication highway is all the more relevant. Roots in soil compete ( Cahill et al. 2010), yet neighbouring trees share vital resources under stress ( Philip 2006). The fungi involved may mediate competition between plants and allow for cooperation ( Kiers and van der Heijden 2006). Observing the movement of resources and signalling molecules in field situations will give us a better understanding of how the various components discovered in greenhouse experiments actually manifests to generate the complex ecosystem patterns we observe. Thus the creation of field experiments that examine the scale and diversity of plant communication and behavioural responses taking place exclusively through MN are crucial. Further elucidation of the array of plant signalling molecules that can be transported via the MN will help to establish the full suite of belowground communications that are possible. Finally, experiments are needed to better understand selective mechanisms involved in the evolutionary ecology of MNs.

Sources of Funding

This work is supported by an NSERC CGS-D to M.A.G. and an NSERC Discovery Grant and NSERC CREATE Grant to S.W.S.

Contributions by the Authors

S.W.S. conceived the idea behind the review, M.A.G. and S.W.S. wrote the first draft, and S.W.S., M.A.G., A.K.A. and B.J.P. contributed to subsequent drafts and provided comments.

Conflict of Interest Statement

None declared.

Literature Cited

Author notes

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

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Inter-plant communication through mycorrhizal networks mediates complex adaptive behaviour in plant communities

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Trees can communicate with each other through networks in soil. Much like social networks or neural networks, the fungal mycelia of mycorrhizas allow signa

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Effect of Environmental Conditions on Morphological, Ecological and Geographic Characteristics of Lichens in Coastal Habitats

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Effect of Environmental Conditions on Morphological, Ecological and Geographic Characteristics of Lichens in Coastal Habitats

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Coastal Lichens- Distribution Patterns and Adaptive Strategies

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Coastal Lichens- Distribution Patterns and Adaptive Strategies

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Marine Fungi: Their Ecology and Molecular Diversity

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Marine Fungi: Their Ecology and Molecular Diversity

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Mycorrhizal fungi determine salt-marsh plant zonation depending on nutrient supply

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Mycorrhizal fungi determine salt-marsh plant zonation depending on nutrient supply

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A.B. Frank and mycorrhizae: The challenge to evolutionary and ecologic theory

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A.B. Frank and mycorrhizae: The challenge to evolutionary and ecologic theory

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Data on plant response to mycorrhizal fungi

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Data on plant response to mycorrhizal fungi

MycoDB is a database of 4,010 studies (from 438 unique publications) to aid in multi-factor meta-analyses elucidating the ecological and evolutionary context in which mycorrhizal fungi alter plant productivity. It contains a study how edaphic properties, plant functional groups, and microbial community complexity determine the outcome of mycorrhizal symbioses. Also explores local adaptation among plants, mycorrhizal fungi, and soils as well as how partner identity, colonization levels, and P fertilization impact plant host response to EM associations.

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Wolfram Research, "MycoDB" from the Wolfram Data Repository (2017)   https://doi.org/10.24097/wolfram.79942.data

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Data Resource History

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Data on plant response to mycorrhizal fungi

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Extraction Methods for Medicinal Compounds by David Poplin

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Extraction Methods for Medicinal Compounds by David Poplin

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Extraction Methods for Medicinal Compounds

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North American Mycological Association's past and present webinars!

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North American Mycological Association's past and present webinars!

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A Review of the Fungi That Degrade Plastic

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A Review of the Fungi That Degrade Plastic

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1. Introduction

Plastic is one of the most abundant human-produced, versatile materials on the earth. Its high stability and long durability facilitate its integral role in our day-to-day lives, from the kitchen to an industrial level [ 1, 2]. Plastic is a polymer and consists of the elements carbon, hydrogen, silicon, oxygen, chlorine, and nitrogen [ 1]. Plastic production can be bio-based or synthetic. Bio-based plastics are made from natural compounds such as lignin, cellulose, hemicellulose, terpenes, vegetable oils, carbohydrates, and food waste [ 3, 4, 5]. In contrast, crude oil is the main component of synthetic plastics [ 6, 7], which are generally referred to as non-biodegradable [ 8].

The present study is focused on synthetic plastics. Seven major types of synthetic plastic are used around the world. These are polyethylene terephthalate (PET), high-density polyethylene (HDPE), polyvinyl chloride (PVC), low-density polyethylene (LDPE), polypropylene (PP), polystyrene (PS), and various other plastics that include acrylic, polycarbonates, polylactic acid (PLA), fibers, and nylon [ 3, 9].

Global plastic production is rising year by year. In 2018, the annual global plastic production was 359 million tons, while it was 368 million tons in 2019 [ 10]. China is the world leader in plastic production, accounting for 31% of world plastic production in 2019 [ 10]. Although the production of new plastic increases annually, the rate of plastic waste management and plastic recycling rate has not reached precise levels [ 10]. In Europe, total plastic production in 2018 was 61.8 million tons. However, the amount of plastic post-consumer waste collected in Europe in 2018 was only 9.4 million tons [ 10]. The estimated global total for virgin plastic production was 8300 million tons in 2017 [ 11]. The amount of plastic waste accumulated as of 2015 was 6300 million tons; from that, only 9% were recycled, 12% were incinerated, and 79% were placed in landfills or introduced to the natural environment [ 11]. Every year 25 million tons of synthetic plastics are accumulated along seacoasts and in terrestrial environments [ 12]. In 2019, the amount of plastic waste released into the aquatic environments was 6.1 million tonnes (Mt), and 1.7 Mt flowed into oceans. Currently, there has been a dramatic increase. At least eight million tons of plastic get into oceans, which have the potential of breaking down into tiny microplastics that possibly make their way into our food chains and result in unknown effects [ 13]. Current plastic accumulation in reverse is 109 Mt [ 14]. The build-up of plastics in rivers implies that leakage into the ocean will continue for decades, even if mismanaged plastic waste could be significantly reduced [ 14]. Current estimations reveal that 80% of marine litter accumulation is due to plastic debris [ 4]. This marine plastic waste accumulation in amounts is around 30 Mt. The total amount of plastic waste only in the ocean is expected to grow from 50 million tons in 2015 to 150 million tons by 2025 [ 15]. If current production and waste management trends continue, roughly 12,000 million tons of plastic waste will be in landfills or the natural environment by 2050, with an annual accumulation of ~339 million tons [ 11, 16].

Moreover, when considering the plastic accumulation based on major plastic producing regions globally, in just Europe, 75,000 to 300,000 tons of microplastics accumulate every year [ 4]. In the United States, the landfill rate for discarded plastics exceeds 75% [ 17].

Therefore, these various types of plastics, after being used and then discarded, not only pervade in every nook and cranny of the planet but also cause major negative impacts at the ecosystem level [ 18]. At present, plastic pollution has become one of the major global environmental issues [ 4], and it is the leading cause of biodiversity reduction. Polyethylene causes blockages in the intestines of birds, fish, and marine mammals. Entanglement in or ingesting this waste has endangered hundreds of different species [ 19]. Fragmented plastic debris, referred to as microplastics, were reported entrapping in subtropical gyres that run over a million square kilometers. These microplastics ingested by a wide range of organisms subsequently cause substantial negative impacts on their existence [ 20]. Moreover, plastics can cause health effects; for instance, airborne microplastics can be inhaled, thus representing a direct risk to human health [ 21].

The natural degradation rate of plastic is extremely slow, and that causes plastics wastes to accumulate in all components of the environment [ 22, 23]. The long chain polymer structure, high molecular weight, and hydrophobicity cause plastics to be resistant to biodegradation [ 24]. In fact, some plastics take up to 1000 years to degrade [ 25]. These facts are the reason for the rapid plastic accumulation in natural environments. Hence, developing an efficient process to accelerate the plastic degradation rate is essential to avoid this annual accumulation. Several solutions have been provided in the scientific community and have been experimentally proved to some extent. Those methods include photo-degradation (degraded by light), chemical degradation, thermal degradation (degraded by heat), irradiation using gamma rays, and biodegradation (degraded by biological additives or microorganisms) [ 25, 26, 27]. However, a method with minimum harmful effects to nature but without or at most minimum toxic by-products is required [ 27]. The processes such as photo-degradation, chemical degradation, thermal degradation, and irradiation using gamma rays cause many negative impacts on nature, such as accumulation of heavy metals in ecosystems and disturbance in natural ecosystem functioning. Moreover, those methods require high costs and energy levels to perform. Therefore, scientists across the globe have tended to investigate better biodegradation methods that do not result in harmful effects and represent an eco-friendly approach for managing plastics [ 27]. Furthermore, biodegradation is a proper solution since it is cost-effective and does not require much energy. More than 400 microbes have been recorded to be capable of plastic degradation [ 28]. The present study was focused only on plastic-degrading fungi among plastic-degrading microbes.

Several studies have been carried out on plastic-degrading fungi. For example, Lacerda et al. [ 29] investigated the fungi from the plastisphere within the aquatic environments of the western South Atlantic and Antarctic Peninsula. Microorganisms and enzymes that are able to degrade a variety of generally used synthetic plastics were comprehensively summarized. The microbial metabolic pathways for plastic depolymerization products and the current attempts toward utilization of such products as feedstocks for microbial production of chemicals with high value were highlighted by Ru et al. [ 30]. Sánchez [ 31] described the natural and unique ability of fungi to invade macro- and microplastic substrates by using enzymes that have the capacity to detoxify pollutants. Sáenz et al. [ 32] experimented with biodegradation of low-density polyethylene (LDPE) by Aspergillus niger and A. terreus to increase the degradation rate without any co-substrate or photothermal treatment. Iram et al. [ 33] reviewed some of the most common strategies for the degradation of various types of polymers, along with a list of potential microbes capable of feeding on them. The role of marine fungi was also recently reviewed by Zeghal et al. [ 34]. Microbial degradation of plastics was reviewed by Kale et al. [ 22]. However, a recent complete study on plastic-degrading fungi in all environments, including both aquatic and terrestrial environments, which addresses their detailed phylogenetic relationships, is lacking. As such, the information presented herein reviews plastic-degrading fungi reported thus far and their phylogenetic relationships.

The present study attempted to summarize current plastic production and plastic waste accumulation in natural environments worldwide. Moreover, a list of all taxa of fungi known to be capable of degrading plastic-degrading fungi was developed from the available literature, and notes were compiled on the major fungal groups involved. In addition, the phylogenetic relationships of plastic-degrading fungi were analyzed based on multi-gene analyses (ITS, LSU, SSU, TEF, RPB1, and RPB2). As such, the overall objective of the study was to summarize all currently known basic information on plastic-degrading fungi to influence future research on similar topics.

2. Materials and Methods

2.1. Literature Review

The data presented herein was acquired from several different sources-the published literature, online databases, and personal communication. We selected seven major synthetic plastic types used around the world based on recent literature [ 3, 9] and the species of fungi reported to degrade those plastic types. Plastic-degrading fungal species data were collected primarily from "Google Scholar", "Research Gate", "PubMed", and "Web of Science". The main phrases used in the online literature search for the plastic types mentioned above and the taxa of fungi involved in their biodegradation were "plastic types", "global plastic production", "global plastic waste management", "fungal bio-degradation of plastics", and "bio-degradable plastics". A list of major types of synthetic plastic with their major uses and annual production was prepared ( Table 1). Taxa of fungi reported to degrade plastics are listed in Table 2.

2.2. Phylogenetic Analyses

2.2.1. Taxon Sampling

A data matrix containing 395 taxa, including four out-group taxa (Basidiobolus ranarum AFTOL-ID 301, Basidiobolus ranarum ARSEF 260, Basidiobolus ranarum ATCC 14449, and Olpidium brassicae AFTOL-ID 633) were generated in the present study. ITS, LSU, SSU, TEF, RPB1, and RPB2 sequence data and their GenBank accession numbers are provided in Table S1.

2.2.2. Initial Phylogenetic Analyses

Multiple sequence alignments for each gene (ITS, LSU, SSU, TEF, RPB1, and RPB2) were generated with MAFFT version 7 ( http://mafft.cbrc.jp/alignment/server/, accessed on 22 April 2022). Long alignment gaps were removed using trimAl [ 123] available at Phylemon2 web server [ 124] and manually adjusted in BioEdit v. 7.0.4 [ 125] where necessary. The individual datasets were concatenated into a combined dataset using FaBox (1.41) [ 126]. Ambiguously aligned regions were excluded, and gaps were treated as missing data. Maximum likelihood phylogenetic analyses were performed in the CIPRES web portal [ 127] using RAxML-HPC2 on XSEDE (8.2.12) tool [ 128]. The bootstrap analysis for each ML tree was performed with 1000 thorough bootstrap replicates with the same parameter settings using the GTR+G+I substitution model selected by MrModel Test 2.2 [ 129]. Posterior probabilities (PP) [ 130, 131] were determined by Markov Chain Monte Carlo sampling (MCMC) in MrBayes v. 3.0b4 [ 132]. Four simultaneous Markov chains were run for 20,000,000 generations, and the trees were sampled every 1000th generation. MCMC heated chain was set with a "temperature" value of 0.2. The distribution of loglikelihood scores was examined to determine the stationary phase for each search and to decide if extra runs were required to achieve convergence using the program Tracer 1.5 [ 133]. All sampled topologies beneath the asymptote (40%) were discarded as part of a burn-in procedure, while the remaining trees (12,000) were used for calculating posterior probabilities in the majority rule consensus tree. Bayesian Posterior Probabilities (BYPP) equal to or greater than 0.90 are given below or above each node ( Figure 1). The resulting trees were viewed with FigTree v.1.4.0 [ 134]. The compressed overview of the phylogram resulting from the phylogenetic analysis is presented in Figure 2, where classes including plastic-degrading fungi are colored green.

3. Results

3.1. Phylogenetic Analyses

The present study investigated the phylogenetic relationships of plastic-degrading fungi based on an analysis of ITS, LSU, SSU, TEF, RPB1, and RPB2 sequence data. The alignment of combined genes included 6289 bp (ITS-1-388, LSU-389-1434, SSU-1435-2502, TEF-2503-3382, RPB1-3383-4569, and RPB2-4570-6289). The topology of the tree from maximum likelihood analysis was similar to the tree from Bayesian analysis. The best scoring RAxML tree with a final likelihood value of −275,048.218811 is presented. The matrix had 5830 distinct alignment patterns, with 67.51% undetermined characters or gaps.

The phylogenetic tree ( Figure 1 and Figure 2) representing those taxa of fungi known to be able to degrade fungi comprises three major clades, with these representing the three major phyla Ascomycota, Basidiomycota, and Mucoromycota. The basal clade Mucoromycota includes the class Mucoromycetes. Consequently, these taxa are the basal groups of plastic degraders in the fungi kingdom. The phylum Basidiomycota also can be recognized as a clade, and it is comprised of the Agaricomycetes, Microbotryomycetes, Tremellomycetes, Tritirachiomycetes, and Ustilaginomycetes. For Clade 3, the upper clade is the phylum Ascomycota and includes the Dothideomycetes, Eurotiomycetes, Leotiomycetes, Saccharomycetes, and Sordariomycetes. Based on the phylogeny of the present study, the Eurotiomycetes are the most evolved group of plastic-degrading fungi. The highest numbers of plastic-degrading fungi are included in Clade 3.

3.2. Phylum Ascomycota

3.2.1. Class Dothideomycetes

The Dothideomycetes is the largest class within the phylum Ascomycota. Most of the taxa within this class are recorded as saprobes in various habitats and substrates [ 135]. Our investigations revealed that some members of Dothideomycetes are capable of plastic degradation. Most of the recorded species of the Dothideomycetes belong to the order Pleosporales, but a few taxa are recorded from the Dothideales and Botryosphaeriales ( Table 2, Figure 1 and Figure 2). Plastic degraders in the Dothideomycetes have the ability to degrade LDPE, PUR, PS, PCL, PEA, PPA, PBA, HDPE, PVC, PE, PU, and Sky-Green plastics ( Table 2). Recent studies on plastic-degrading members of the Dothideomycetes are those of Khruengsai et al. [ 64] and Brunner et al. [ 6]. In the phylogenetic tree, the Dothideomycetes formed a well-supported clade sister to the Arthoniomycetes. Most of the plastic-degrading Dothideomycetes were placed in the upper subclade of the main Dothideomycetes clade, and the rest were grouped in a basal subclade ( Figure 1 and Figure 2).

3.2.2. Class Eurotiomycetes

The Eurotiomycetes are extremely common saprobes in diverse habitats and substrates [ 136]. Based on our results, most plastic-degrading fungal records belong to the Eurotiomycetes. Many plastic-degrading members of the Eurotiomycetes are taxonomically placed under the Eurotiales, and the most common plastic-degrading fungal genera are Aspergillus and Penicillium ( Table 2, Figure 1 and Figure 2). The plastic types they are reported to degrade are HDPE, LDPE, PCL, PE, PVC, PS-PUR, PEA, PPA, PBA, PHB, Poly[3HB-co-(10 mol%) 3HV], Sky-Green, PHV, PBS, PLA and PVC ( Table 2). Recent studies on plastic-degrading Eurotiomycetes are those of Rani & Singh [ 12], Ndahebwa Muhonja et al. [ 54], Bermúdez-García et al. [ 57], Laila [ 63], Khruengsai et al. [ 64], Munir et al. [ 65], Alshehrei [ 69], Sangale et al. [ 2], Duan et al. [ 90], El-Morsy et al. [ 92], Brunner et al. [ 6] and Ojha et al. [ 26]. The Eurotiomycetes is the uppermost clade within our phylogram ( Figure 1 and Figure 2). The genera Aspergillus and Penicillium contain a large number of species with a worldwide distribution and a huge range of ecological habitats [ 137]. They are mostly widespread saprobes and can be found in both indoor and outdoor environments, including in both the air and soil. In addition, some species of Aspergillus and Penicillium have the ability to grow under extreme conditions [ 137]. Hence, further research on these genera would provide better solutions for the environmental accumulation of plastics.

3.2.3. Class Leotiomycetes

Most of the Leotiomycetes are saprobes on a wide variety of substrates. However, this class also includes many important plant pathogens [ 138]. Our results showed that the few records of plastic-degrading fungi are phylogenetically related to the Leotiomycetes ( Table 2, Figure 1 and Figure 2). In the phylogenetic tree of this study, the Leotiomycetes formed a well-supported clade sister to the Laboulbeniomycetes ( Figure 1 and Figure 2). However, there is a single record found that clearly belongs to the Leotiomycetes and possibly has the ability of plastic degradation [ 92]. The other records that grouped within Leotiomycetes in our phylogeny were Cephalosporium gramineum, which is currently placed under the Sordariomycetes. Therefore, studies with a wide range of taxon sampling are required to resolve the phylogenetic position of Cephalosporium gramineum. Furthermore, a recent study on the biodegradation of bio-based and biodegradable plastic, polybutylene succinate-co-adipate (PBSA), identified a species (Tetracladium furcatum ) within the Leotiomycetes that has the ability to degrade PBSA [ 139]. However, recent studies on synthetic plastic-degrading members of the Leotiomycetes are very few. As a result, additional studies on the Leotiomycetes are required to assess their ability to degrade plastics.

3.2.4. Class Saccharomycetes

The Saccharomycetes is a small class of yeasts with a single order of about 1000 known species, which are classified under the Ascomycota [ 140]. Most of the Saccharomycetes are saprobes, and few are recorded as human and plant pathogens [ 140]. The present study discovered five records of five members of the Saccharomycetes capable of degrading plastics ( Table 2, Figure 1 and Figure 2). The Saccharomycetes is the second basal clade within the phylum Ascomycota. All Saccharomycetes members that are plastic degraders are grouped in the upper subclade of the main Saccharomycetes clade ( Figure 1 and Figure 2). Arxula, Candida, and Debaryomyces are the genera to which those plastic-degrading members of the Saccharomycetes belong [ 43, 71]. Some members of the Saccharomycetes are widely used in industrial and biotechnological processes. Species such as Saccharomyces cerevisiae are model organisms in many types of research [ 140]. A recent study used Genetic engineering techniques on two strains of Saccharomyces cerevisiae to produce the heterologous protein Polyethylene Terephthalate (PET) hydrolase enzyme, which has been shown to have the capability of degrading PET into its subsequent monomers [ 141]. We believe future research on the Saccharomycetes would find a better solution for plastic accumulation in nature.

3.2.5. Class Sordariomycetes

The Sordariomycetes is the second largest class within the phylum Ascomycota. The majority of the Sordariomycetes are saprobes, but the group also includes some important plant pathogens [ 142]. They have a wide ecological distribution in both terrestrial and aquatic habitats [ 142]. Our research recorded many members of the Sordariomycetes with the ability to degrade plastics ( Table 2, Figure 1 and Figure 2). The plastic types they are reported to degrade are PE, PS, PHB, Poly[3HB-co-(10 mol%) 3HV], PUR, PS-PUR, HDPE, LDPE, PVC, PCL, PEA, PPA, and PBA ( Table 2). Recent studies of plastic-degrading Sordariomycetes are those of Munir et al. [ 65], (Yang et al. [ 93], Brunner et al. [ 6], and Khruengsai et al. [ 64]. The Sordariomycetes formed a middle clade within the main Ascomycota clade that is sister to the Laboulbeniomycetes ( Figure 1 and Figure 2). Many plastic degraders in the Sordariomycetes are classified under the Hypocreales, while others belong to the Amphisphaeriales, Glomerellales, Phyllachorales, and Sordariales. Even though the Eurotiomycetes include the highest number of records of plastic-degrading fungi, the Sordariomycetes contain the highest number of genera with the capability to degrade plastics.

3.3. Phylum Basidiomycota

3.3.1. Class Agaricomycetes

The Agaricomycetes is a morphologically diverse class of macrofungi within the Basidiomycota, containing around 36,000 described species. They are ecologically diverse and include saprobes, mycorrhizal symbionts, and pathogens [ 143]. Moreover, the Agaricomycetes encompasses several important commercially growing edible mushrooms [ 144]. The present study found several records of Agaricomycetes with the ability to degrade plastics ( Table 2, Figure 1 and Figure 2). They are reported to degrade Poly[3HB-co-(7 mol%) 3HV], LDPE, PVC, polyethylene, and PHB ( Table 2). Additionally, da Luz et al. [ 16] performed a study on plastic-degrading Agaricomycetes. They investigated the degradation of oxo-biodegradable plastic bags and green polyethylene by Pleurotus ostreatus. The Agaricomycetes is the upper clade within phylum Basidiomycota, and it is highly statistically supported within the present phylogeny ( Figure 1 and Figure 2). Further studies of edible mushrooms belonging to the Agaricomycetes and their ability to degrade plastics would increase world food production and reduce the plastic accumulation in nature.

3.3.2. Class Microbotryomycetes

The Microbotryomycetes include mainly mycoparasites, saprobic yeasts, and plant pathogens [ 145]. A single record of plastic-degrading fungi was found in the order Sporidiobolales of the Microbotryomycetes in the present study ( Table 2, Figure 1 and Figure 2). In our phylogenetic tree, the Microbotryomycetes formed a well-supported clade sister to Tritirachiomycetes ( Figure 1 and Figure 2).

3.3.3. Class Tremellomycetes

The Tremellomycetes are classified under the Basidiomycota and consist of saprobic yeasts, dimorphic taxa, and species that form hyphae and/or complex fruiting bodies [ 146]. The present study identified a few records from the Tremellomycetes that are capable of degrading plastics ( Table 2, Figure 1 and Figure 2). All the records belong to the genera Cryptococcus and Papiliotrema (Tremellales), andthey are capable of degrading PCL, PBS, and PBSA ( Table 2). The Tremellomycetes formed a well-supported clade sister to Agaricomycetes in the present phylogenetic tree ( Figure 1 and Figure 2). A recent study on synthetic plastic-degrading Tremellomycetes was published by Hung et al. [ 114]. A recent study on biodegradable plastic mulch films (BDMs) and their associated soil microbial communities found that the Tremellomycetes are capable of degrading agriculturally-weathered BDMs [ 147].

3.3.4. Class Tritirachiomycetes

The Tritirachiomycetes is a small class within the Basidiomycota that is made up of filamentous fungi. They are mainly saprobes, but some have been recorded as human pathogens [ 148]. A single record of a fungus from this class that is capable of degrading plastics was found in the present study ( Table 2, Figure 1 and Figure 2). The Tritirachiomycetes formed a well-supported clade sister to the Microbotryomycetes in our phylogenetic tree ( Figure 1 and Figure 2).

3.3.5. Class Ustilaginomycetes

The majority of the Ustilaginomycetes are economically important plant pathogens. They are usually unicellular yeasts (sporidia), but some are simple multicellular forms, such as a pseudomycelium, multicellular cluster, or mycelium [ 149]. Moreover, the Ustilaginomycetes have a comparatively short life cycle, which makes them easy to handle under laboratory conditions. As a result, the Ustilaginomycetes can be considered model organisms for studying fungi [ 149]. The present study found a single record from the Ustilaginomycetes of a fungus capable of degrading plastics ( Table 2, Figure 1 and Figure 2). The Ustilaginomycetes is the basal clade within the main Basidiomycota clade, and it is statistically highly supported ( Figure 1 and Figure 2).

3.4. Phylum Mucoromycota

The Mucoromycetes are a class within the phylum Mucoromycota and consist of mainly filamentous fungi with a saprobic lifestyle. Several species are also life-threatening human pathogens, plant parasites, and food spoilage organisms. Moreover, members of the Mucoromycetes are used as a traditional fermenting agent for Asian and African foods, such as soybean products and several varieties of European cheese. Fungi belonging to the Mucoromycetes are common in the environment and able to colonize all kinds of wet, organic substrates [ 150]. The present study found several Mucoromycetes fungi with the ability to degrade plastics. All the recorded plastic-degrading members of the Mucoromycetes belong to the genera Mucor and Rhizopus. These fungi are capable of degrading PHB, HDPE, LDPE, PVC, PCL, polyalkylene dicarboxylic acids, PPA, and PET copolymers with dicarboxylic acids ( Table 2). A recent study of plastic-degrading Mucoromycetes was that of Pardo-Rodríguez & Zorro-Mateus [ 106]. The Mucoromycota formed the basal clade within our phylogenetic tree ( Figure 1 and Figure 2). However, the phylum presented a polyphyletic nature in the present phylogenetic tree and was separated into two basal clades.

4. Discussion

As global plastic production and plastic waste accumulation increase rapidly, we need to look for a quick and efficient solution to save nature and, indeed, the entire planet [ 4, 7]. The problem becomes even more acute as the natural degradation rate of all types of plastic is very slow [ 23]. Hence, it is essential to look at ways to accelerate plastic degradation methods. Several solutions that have been proposed are photo-degradation (degrade by light), chemical degradation, thermal degradation (degrade by heat), irradiation using gamma rays, and biodegradation (degrade by biological additives or microorganisms) [ 25, 26, 27]. Biodegradation has been suggested as the best solution as it is an eco-friendly approach [ 27]. However, based on the results obtained in previous studies, people select biodegradation since the other options are not cost-effective [ 26]. In this study, we reviewed the literature on plastic-degrading fungi from different sources and summarized a list of records on plastic degraders in the fungi kingdom. Moreover, we analyzed phylogenetic relationships of plastic-degrading fungi based on a combined ITS, LSU, SSU, TEF, RPB1, and RPB2 dataset from 395 strains and provided brief taxonomy at the level of class.

The present study identified more than 200 records of fungi capable of degrading different plastic types under a wide range of conditions. These are listed in Table 2. Most plastic-degrading fungal records are found in the class Eurotiomycetes of the phylum Ascomycota. However, a wide range of generic level diversity in plastic-degrading fungi was found in the class Sordariomycetes of the phylum Ascomycota. Considering phylum level diversity in relation to the ability to degrade plastic, most of the plastic degraders belong to the phylum Ascomycota. The second group with the highest number of recorded plastic degraders was in the phylum Basidiomycota, with a few records also found in the phylum Mucoromycota. However, very few sequences are available directly from the plastic-degrading fungi. Hence, we used sequence data from another strain of the same species, which the species was recorded as a plastic degrader. Furthermore, to establish a detailed and accurate phylogenetic tree for plastic-degrading fungi, sequence data need to be obtained exactly from the strains which were recorded as plastic-degrading fungi. Moreover, future studies on whole-genome sequencing or sequencing of more gene regions and evolutionary relationships analyses of plastic-degrading fungi concerning the specific plastic type the fungi can degrade would be beneficial to develop commercially available plastic degrading fungal strains.

Recent studies have reported some common saprobic fungi and plant pathogenic fungi that can degrade plastic [ 6]. Our study agrees with this statement as we found many plastic degraders that belong to the Eurotiomycetes and Dothideomycetes when most of the saprobic fungi are taxonomically members of the Sordariomycetes, where many important plant pathogens are classified. Moreover, recent research has reported that fungi that can degrade complex C-polymers, such as lignin and protein, can also degrade plastics [ 6]. Therefore, future studies of the Dothideomycetes, Eurotiomycetes, and Sordariomycetes are essential. Since these classes include plant pathogens, saprobes, and degraders of complex C-polymers, it is possible that they can degrade plastics. Moreover, these findings also proved that enzymes produced by common saprobes and plant pathogens can degrade or even transform plastics. Hence further studies on the metabolic pathways of those fungi and the discovery of the essential enzymes involved in plastic degradation can significantly contribute to reducing plastic accumulation in nature.

Plastics accumulating in the marine environment are an increasingly important environmental issue [ 34]. Most of the plastic waste is accumulated in the sea, and there will be more plastics in the sea than fish by 2050. Recently, plastic-fungi interactions in marine environments were reviewed by Zeghal et al. [ 34]. The same study listed more than 60 records of fungi identified to the species level and belonging to the Ascomycota and Basidiomycota as having the ability to degrade plastic debris in marine environments [ 34]. Our study listed plastic-degrading fungi from all environmental conditions on the earth. When comparing the number of records, only about twenty-five percent of records are from marine environments, even though the highest environmental pollution from plastics is recorded from marine environments. This clearly shows the requirement for more research on plastic-degrading fungi in marine environments. Moreover, Zeghal et al. [ 34] concluded that future studies are required to identify species of fungi that can degrade plastics in the marine environment. They also concluded that these studies should address their enzymatic potential, which might then serve biotechnological applications for plastic waste bioremediation [ 34]. Furthermore, the effect of physicochemical parameters in marine environments (such as salinity and pH) on plastic-degrading fungi and the differences between the metabolic pathways of marine plastic degraders from terrestrial plastic degraders need to be focused on in future research fields to save the sea from plastic accumulation.

Plastic use in the agricultural sector is growing rapidly. Some of the main examples of LDPE use are in greenhouse and mulch film as well as in structures to provide crop protection against environmental conditions and insects and pests. HDPE is used in containers for pesticides and pesticides as well as in containers for nurseries or slips for irrigation, and PP is used in containers for nurseries or floating covers and polystyrene in trays for a plant nursery [ 151]. Recent research by Khan & Stevenson [ 151] investigated the plastic-degrading ability of soil fungi and found that Aspergillus tubingensis can successfully colonize plastic surfaces. Additionally, they found that the enzymes this fungus produces can break the chemical bonds between the plastic molecules. Moreover, the genus Aspergillus is very important in plastic degradation. Several species from different habitats have been reported that degrade various plastic types ( Table 2). As such, further research on the members of the genus Aspergillus and their ability to degrade plastics needs more attention. Not only Aspergillus, but many other fungi have also been reported ( Table 2), including the ability to degrade multiple plastic types by the same fungi. Some examples are Chaetomium globosum that can degrade HDPE, LDPE, PVC, PCL, PEA, PPA, and PBA, Fusarium solani that can degrade LDPE, HDPE, PVC, PCL, PS-PUR, PHB, and PET, and Penicillium funiculosum that can degrade PCL, PHB, PHV, Poly[3HB-co-(7, 14%) 4HB], Poly[3HB-co-(7, 27, 45, 71%) 3HV], PEA, PPA, and PBA. Those fungi that can degrade multiple plastics have also been recorded from different habitats. Hence, they are the perfect candidates for strain improvements for commercial applications. Molecular studies of those plastic-degrading fungi, specifically on genes related to the metabolic pathways of those fungi involved in plastic degradation, are critical. Simultaneously, even though there are commercially developed strains for plastic degradation in agricultural lands, there must be experimental confirmation that those fungi do not have pathogenic effects on crop plants and the beneficial flora and fauna associated with the farmlands.

Low-Density Polyethylene (LDPE) is the most common type of plastic, generally known as polythene [ 9, 152]. There are more than 15 species of fungi, including several members of Aspergillus recorded as capable of degrading LDPE (i.e., Aspergillus caespitosus, Aspergillus flavus, Aspergillus fumigatus, Aspergillus nidulans, Aspergillus niger, Aspergillus nomius, Aspergillus ochraceus, Aspergillus oryzae, Aspergillus terreus, Chaetomium globosum, Chrysonilia setophila, Diaporthe italiana, Fusarium solani, Gliocladium virens, Phoma sp., Thyrostroma jaczewskii, Trichoderma hamatum, and Mucor hiemalis) ( Table 2). Therefore, we suggest that the genus Aspergillus would be a perfect fungal genus for developing commercial levels to degrade plastics. For the basement of such a lengthy biotechnological application, comprehensive molecular studies related to the ecology of the genus Aspergillus are very important. Moreover, investigations on enzyme production and metabolic pathways of the genus Aspergillus are helpful research areas.

The slow degradation rate of synthetic plastics and the growing demand for increasingly more limited oil reserves drive the effort to produce bio-based plastics [ 3, 16]. Bio-based plastics originate from renewable resources such as plant and animal waste products from industry [ 3]. However, the global markets for bio-based plastics are still small. The annual global production of bio-based plastics in 2020 was approximately 2 Mt [ 153]. Moreover, bio-based plastics do not represent a better solution for the slow degradation rate of synthetic plastics or plastic accumulation in nature. Recent records indicate that only half of bio-based plastics are biodegradable, while the other half is non-biodegradable [ 3, 4, 5]. Bio-based plastics naturally degrade only to some extent. For the remainder, we once again need to look for suitable microorganisms that are capable of their biodegradation.

Although there are more than 400 records of plastic-degrading microbes, including over 200 records of species of plastic-degrading fungi, many studies have failed to differentiate losses caused by the leaching or degradation of polymers [ 28]. Moreover, many studies have used more highly crystalline polymers with species of fungi under laboratory conditions [ 28]. Hence, even the species of fungi involved provided few clues as to their ability to degrade those crystallized polymers. There was no confirmation of their biodegradation rate in a natural environment where large-sized plastic wastes have accumulated. Herein we propose a more detailed in situ research approach that delivers a clearer picture of plastic-fungi interactions, including changes in the polymer structure, mass loss, and confirmation of fungal strains and their enzymatic activity with related genes to degrade large-sized plastic polymers. Furthermore, genetic and biotechnology research is required to identify enzymes and their related genes for plastic degradation from currently identified plastic-degrading fungi. We expect to continue our following review on enzyme production and metabolic pathways of plastic-degrading fungi and their evolutionary relationships. This information can then be applied to develop more powerful hybrid fungal species to degrade plastics. Moreover, we expect this study to influence the research and applications of plastic-degrading fungi to save Earth's planet.

5. Conclusions

Even though plastic is currently an important material in the global environment, it is becoming a huge threat to nature. Because current global plastic production is increasing rapidly (300 million tons annually) and plastics have a very low natural degradation rate, they accumulate in natural environments and cause considerable damage to biodiversity and natural ecosystems. At present, scientists and researchers are assessing the usefulness of microorganisms in accelerating plastic degradation. In this study, we reviewed plastic degradation using fungi. Herein we list more than 200 records of fungi capable of degrading fungi based on the available literature. Their phylogenetic relationships were analyzed using a combined ITS, LSU, SSU, TEF, RPB1, and RPB2 dataset generated from 395 strains. Our results confirm that plastic-degrading fungi are taxonomically diverse and belong to three major fungal phyla-the Ascomycota, Basidiomycota, and Mucoromycota. The Ascomycota plastic degraders belong to five major classes: Dothideomycetes, Eurotiomycetes, Leotiomycetes, Saccharomycetes, and Sordariomycetes. Plastic-degrading Basidiomycota fall within the Agaricomycetes, Microbotryomycetes, Tremellomycetes, Tritirachiomycetes, and Ustilaginomycetes. Mucoromycota fungi capable of degrading plastics were found under the Mucoromycetes. The Eurotiomycetes include the highest number of recorded plastic degraders in the fungi kingdom. However, a wide range of plastic-degrading fungal genera was found within the class Sordariomycetes. Moreover, there is an acute need for future research on similar topics to resolve the global problem of plastic accumulation in nature.

Supplementary Materials

Author Contributions

Conceptualization, S.C.K. and A.H.E.; methodology, S.C.K. and A.H.E.; formal analysis, A.H.E.; writing-original draft preparation, A.H.E. and S.C.K.; writing-review and editing, A.H.E., S.C.K., S.T., C.D., R.X. and S.L.S.; visualization, D.D., N.S. and S.T.; supervision, S.C.K., D.D., N.S. and S.T.; project administration, S.C.K.; funding acquisition, S.C.K. and D.D. All authors have read and agreed to the published version of the manuscript.

Funding

The research was supported by the National Natural Science Foundation of China (No. NSFC 31760013, 31950410558), High-Level Talent Recruitment Plan of Yunnan Provinces ("Young Talents" Program) and Chiang Mai University.

Institutional Review Board Statement

Informed Consent Statement

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding authors.

Acknowledgments

Qujing Normal University is thanked for the facilities provided for research work.

Conflicts of Interest

Authors declare that they have no competing interest.

References

1. Ogunbayo, A.; Olanipekun, O.; Adamu, I. Preliminary Studies on the Microbial Degradation of Plastic Waste Using Aspergillus niger and Pseudomonas sp. J. Environ. Prot. 2019, 10, 625-631. [Google Scholar] [CrossRef] [Green Version]

2. Baheti, P. How Is Plastic Made? Available online: https://www.bpf.co.uk/plastipedia/how-is-plastic-made.aspx (accessed on 15 September 2021).

3. Plastics Europe. How Plastics Are Made. Available online: https://www.plasticseurope.org/en/about-plastics/what-are-plastics/how-plastics-are-made (accessed on 13 September 2021).

4. Hardin, T. Plastic: It's Not All the Same; The Basics on 7 Common Types of Plastic. Available online: https://plasticoceans.org/7-types-of-plastic (accessed on 4 September 2021).

5. Plastics Europe. Plastics-The Facts 2020, an Analysis of European Plastics Production, Demand and Waste Data. Available online: https://www.plasticseurope.org/en/resources/publications/4312-plastics-facts-2020 (accessed on 18 September 2021).

6. United Nations Environment Programme. Fungi Research Lifts Lid on Shy Organisms That Break down Plastic. Available online: https://www.unep.org/news-and-stories/story/fungi-research-lifts-lid-shy-organisms-break-down-plastic (accessed on 12 September 2021).

7. Organisation for Economic Co-Operation and Development. Plastic Pollution Is Growing Relentlessly as Waste Management and Recycling Fall Short, Says OECD; Organisation for Economic Co-Operation and Development: Paris, France, 2022. [Google Scholar]

8. da Luz, J.M.R.; da Silva, M.d.C.S.; dos Santos, L.F.; Kasuya, M.C.M. Plastics Polymers Degradation by Fungi. In Microorganisms; IntechOpen: Vienna, Austria, 2019. [Google Scholar]

9. Gascueña, D. Nature's Allies Against Plastic: Algae, Bacteria, and Fungi. Available online: https://www.bbvaopenmind.com/en/science/environment/natures-allies-against-plastic-algae-bacteria-and-fungi (accessed on 12 September 2021).

10. Soundararajan, N. Pune Researchers Discover Fungi That Can Break up Polythene. Available online: https://researchmatters.in/news/pune-researchers-discover-fungi-can-break-polythene (accessed on 11 September 2021).

11. Statista. Statista: Global No.1 Business Data Platform. 2022. Available online: https://www.statista.com/ (accessed on 22 April 2022).

12. Alyamaç-Seydibeyoğlu, E. Impact Modified Poly(Ethylene Terephthalate)-Organoclay Nanocomposites. Master's Thesis, Middle East Technical University, Ankara, Turkey, 2004. [Google Scholar]

13. Nakei, M.D. Isolation and Identification of Plastics-Degrading Microorganisms from Soils of Morogoro, Tanzania. Ph.D. Thesis, Sokoine University of Agriculture, Morogoro, Tanzania, 2015. [Google Scholar]

14. Kim, M.-N.; Lee, A.-R.; Yoon, J.-S.; Chin, I.-J. Biodegradation of Poly (3-Hydroxybutyrate), Sky-Green® and Mater-Bi® by Fungi Isolated from Soils. Eur. Polym. J. 2000, 36, 1677-1685. [Google Scholar] [CrossRef]

15. Raaman, N.; Rajitha, N.; Jayshree, A.; Jegadeesh, R. Biodegradation of Plastic by Aspergillus spp. Isolated from Polythene Polluted Sites around Chennai. J. Acad. Indus. Res. 2012, 1, 313-316. [Google Scholar]

16. Esmaeili, A.; Pourbabaee, A.A.; Alikhani, H.A.; Shabani, F.; Esmaeili, E. Biodegradation of Low-Density Polyethylene (LDPE) by Mixed Culture of Lysinibacillus xylanilyticus and Aspergillus niger in Soil. PLoS ONE 2013, 8, e71720. [Google Scholar] [CrossRef] [Green Version]

17. Laila, M.D. The Potential of Fungi Isolated from Pleurotus ostreatus (Oyster Mushroom) Baglog to Degrade Plastics. Ph.D Thesis, Universitas Andalas, Padang, Indonesia, 2021. [Google Scholar]

18. Munir, E.; Harefa, R.; Priyani, N.; Suryanto, D. Plastic Degrading Fungi Trichoderma viride and Aspergillus nomius Isolated from Local Landfill Soil in Medan; IOP Publishing: Bristol, UK, 2018; Volume 126, p. 012145. [Google Scholar]

19. Gonda, K.; Jendrossek, D.; Molitoris, H.-P. Fungal Degradation of the Thermoplastic Polymer Poly-β-Hydroxybutyric Acid (PHB) under Simulated Deep Sea Pressure. In Life at Interfaces and Under Extreme Conditions; Springer: Berlin/Heidelberg, Germany, 2000; pp. 173-183. [Google Scholar]

20. Owen, S.; Otani, T.; Masaoka, S.; Ohe, T. The Biodegradation of Low-Molecular-Weight Urethane Compounds by a Strain of Exophiala jeanselmei. Biosci. Biotechnol. Biochem. 1996, 60, 244-248. [Google Scholar] [CrossRef] [PubMed] [Green Version]

21. Nimchua, T.; Punnapayak, H.; Zimmermann, W. Comparison of the Hydrolysis of Polyethylene Terephthalate Fibers by a Hydrolase from Fusarium oxysporum LCH I and Fusarium solani f. sp. pisi. Biotechnol. J. Healthc. Nutr. Technol. 2007, 2, 361-364. [Google Scholar]

22. Pathirana, R.; Seal, K. Gliocladium Roseum (Bainier), a Potential Biodeteriogen of Polyester Polyurethane Elastomers; John and Wiley and Sons: Hoboken, NJ, USA, 1983. [Google Scholar]

23. Han, J.-S.; Son, Y.-J.; Chang, C.-S.; Kim, M.-N. Purification and Properties of Extracellular Poly (3-Hydroxybutyrate) Depolymerase Produced by Penicillium pinophilum. J. Microbiol. 1998, 36, 67-73. [Google Scholar]

24. Hall, T. BioEdit, Version 7.0.9; Ibis Therapeutics: Carlsbad, CA, USA, 2004. [Google Scholar]

25. Miller, M.A.; Schwartz, T.; Pfeiffer, W. Embedding CIPRES Science Gateway Capabilities in Phylogenetics Software Environments. 2013, p. 1. Available online: https://dl.acm.org/doi/10.1145/2484762.2484806 (accessed on 22 April 2022).

26. Nylander, J. MrModeltest, Version 2; Program Distributed by the Author; Evolutionary Biology Centre, Uppsala University: Uppsala, Sweden, 2004. [Google Scholar]

27. Huelsenbeck, J.; Ronquist, F. MrBayes: Bayesian Inferences of Phylogeny (Software); University of Rochester: Rochester, NY, USA, 2000. [Google Scholar]

28. 135 Rambaut, A.; Drummond, A. Tracer. MCMC Trace Analysis Tool, Version v1.5.0; University of Oxford: Oxford, UK, 2009. [Google Scholar]

29. Rambaut, A. FigTree. Tree Figure Drawing Tool, Version 1.3.1; Institute of Evolutionary Biology, University of Edinburgh: Edinburgh, UK, 2006. [Google Scholar]

30. Geiser, D.M.; LoBuglio, K.F.; Gueidan, C. 5 Pezizomycotina: Eurotiomycetes. In Systematics and Evolution; Springer: Berlin/Heidelberg, Germany, 2015; pp. 121-141. [Google Scholar]

31. Issa, N. Towards the Biological Degradation of Plastics: Genetic Engineering of Saccharomyces cerevisiae to Secrete Ideonella Sakaiensis Derived PETase. Ph.D. Thesis, University of Kent, Canterbury, UK, 2021. [Google Scholar]

32. Khan, S.; Stevenson, A. A Feast of Plastic Chewing through the World's Waste. In Mountain Futures Inspiration and Innovation from the World's Highlands; World Agroforestry Centre: Nairobi, Kenya, 2018; pp. 209-212. ISBN 978-9966-108-05-0. [Google Scholar]

33. Morone, A. Can Tiny Fungi Solve Our Giant Plastic Problem? Available online: https://weather.com/en-IN/india/pollution/news/2019-04-29-can-tiny-fungi-be-a-solution-to-our-giant-plastic-problem (accessed on 10 September 2021).

34. Bioplastics Market Development Update Dynamic Growth: Global Production Capacities of Bioplastics 2020-2025; 2020. Available online: https://docs.european-bioplastics.org/conference/Report_Bioplastics_Market_Data_2020_short_version.pdf (accessed on 10 September 2021).

Figure 1. Phylogenetic relationships of plastic-degrading fungi. Phylogram generated from a maximum likelihood analysis of ITS, LSU, SSU, TEF, RPB1 and RPB2 fungal sequence data. MLBP values ≥ 70% and BYPP ≥ 0.90 values are given as the first and the second set of numbers near the nodes. Strain/culture numbers are given after the taxon names. The tree is rooted with Basidiobolus ranarum AFTOL-ID 301, Basidiobolus ranarum ARSEF 260, Basidiobolus ranarum ATCC 14449, and Olpidium brassicae AFTOL-ID 633. Strains in Red: Strains directly reported as plastic degraders. Green: Other strain of the same species reported as plastic degraders. Blue: Other species in the same genus reported as plastic degraders.

Figure 2. Compressed overview of the phylogram for the phylogenetic relationships of plastic-degrading fungi. Class level taxonomic ranks in Green include fungal species that were reported as plastic degraders.

Polyethylene Terephthalate (PET or PETE) [ 36]

Beverage bottles, Food bottles/jars and polyester clothing or rope

30.5

0

-

High-Density Polyethylene (HDPE)
Milk cartons, detergent bottles, cereal box liners, toys, buckets, park benches, and rigid pipes

66.96

4.3 (0−11)

Other
Eyeglasses, baby and sports bottles, electronics, CD/DVDs, lighting fixtures, and clear plastic cutlery

-

270
(20−1400)

Table 2. Recorded taxa of fungi that are known to degrade plastics.

Ekanayaka AH, Tibpromma S, Dai D, Xu R, Suwannarach N, Stephenson SL, Dao C, Karunarathna SC. A Review of the Fungi That Degrade Plastic. Journal of Fungi. 2022; 8(8):772. https://doi.org/10.3390/jof8080772

Chicago/Turabian Style

Ekanayaka, Anusha H., Saowaluck Tibpromma, Donqin Dai, Ruifang Xu, Nakarin Suwannarach, Steven L. Stephenson, Chengjiao Dao, and Samantha C. Karunarathna. 2022. "A Review of the Fungi That Degrade Plastic" Journal of Fungi 8, no. 8: 772. https://doi.org/10.3390/jof8080772

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A Review of the Fungi That Degrade Plastic

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Plastic has become established over the world as an essential basic need for our daily life. Current global plastic production exceeds 300 million tons annually. Plastics have many characteristics such as low production costs, inertness, relatively low weight, and durability. The primary disadvantage of plastics is their extremely slow natural degradation.

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The Potential Role of Marine Fungi in Plastic Degradation – A Review

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The Potential Role of Marine Fungi in Plastic Degradation – A Review

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The Potential Role of Marine Fungi in Plastic Degradation – A Review

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Plastic debris has been accumulating in the marine realm since the start of plastic mass production in the 1950s. Due to the adverse effects on ocean life, the fate of plastics in the marine environment is an increasingly important environmental issue. Microbial degradation, in addition to weathering, has been identified as a potentially relevant breakdown route for marine plastic debris. Although many studies have focused on microbial colonization and the potential role of microorganisms in breaking down marine plastic debris, little is known about fungi-plastic interactions. Marine fungi are a generally understudied group of microorganisms but the ability of terrestrial and lacustrine fungal taxa to metabolize recalcitrant compounds, pollutants, and some plastic types (e.g., lignin, solvents, pesticides, polyaromatic hydrocarbons, polyurethane, and polyethylene) indicates that marine fungi could be important degraders of complex organic matter in the marine realm, too. Indeed, recent studies demonstrated that some fungal strains from the ocean, such as Zalerion maritimum have the ability to degrade polyethylene. This mini-review summarizes the available information on plastic-fungi interactions in marine environments. We address (i) the currently known diversity of fungi colonizing marine plastic debris and provide (ii) an overview of methods applied to investigate the role of fungi in plastic degradation, highlighting their advantages and drawbacks. We also highlight (i…

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Mycorrhizal mycelium as a global carbon pool

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Mycorrhizal mycelium as a global carbon pool

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The distinct plastisphere microbiome in the terrestrial-marine ecotone is a reservoir for putative degraders of petroleum-based polymers

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The distinct plastisphere microbiome in the terrestrial-marine ecotone is a reservoir for putative degraders of petroleum-based polymers

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aka plastic degrading fungi might be hiding in plain sight

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Globally rare truffle found in Scottish Atlantic rainforest

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Globally rare truffle found in Scottish Atlantic rainforest

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“We’re looking at a globally rare fungal species that exists only with non-native spruce trees that were introduced into a highly valuable native habitat. A key question for us now is how prevalent this fungus is at this site – and perhaps more importantly does it occur elsewhere – and should its presence be taken into consideration when restoring these sites?”

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The Physics of Spore Dispersal with Dr. Marcus Roper

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The Physics of Spore Dispersal with Dr. Marcus Roper

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Fungi use spores to move from one host to the next. Only microns in size, a spore can be carried aloft on even the slightest wind. But to enter the wind, the spore must first cross a boundary layer of nearly still air that clings to the fungus. In the first half of the 20th century, Reginald Buller did pioneering work to show how mushrooms, and fungi more generally, are adapted to give their spores the best chance of reaching dispersive winds. I will talk about recent work done in my laboratory at UCLA, re-exploring some of the adaptations that Buller identified, as well as our discoveries of previously unknown adaptations. The story emerging from our work, and others, is that far from being passive organs for producing spores, fungi are capable of exquisite feats of engineering when building their fruiting bodies.

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Los Angeles Mycological Society General Meeting April 2024

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Fungi’s Lessons for Adapting to Life on a Damaged Planet

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Fungi’s Lessons for Adapting to Life on a Damaged Planet

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Merlin Sheldrake in Conversation with Robert Macfarlane

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Merlin Sheldrake's new book Entangled Life looks at the complex world of fungi, its adaptive ability, and its interconnectedness with all other forms of life. He spoke with Robert Macfarlane, author of Underland, about his relationship to fungi and its strategic lessons on growth in the face of climate crisis.

*

Robert Macfarlane: I want to plunge straight in and ask about the title of your book, Entangled Life. I hear echoes of Darwin's famous "tangled bank" paragraph, closing the later editions of On the Origin of Species, and "entanglement" is one of the favorite tropes of what might be called Anthropocene ecology, conspicuous in the work of Anna Tsing and Donna Haraway, for instance. What do you mean by "entangled" and for that matter, what do you mean by "life"!?

Merlin Sheldrake: Plunge! I think of the word "entangle" as a knotting and re-knotting, a ravelling, an intertwining. The word appears to have some of its roots in Nordic and German words for "seaweed," presumably because they are life forms that knot and clump with themselves-besides oars and fishing nets. According to the Chambers Dictionary of Etymology "entangle" was originally used to describe human involvement in "complex affairs" and only later took on other meanings.

Entangled Life is a book about fungi, most of which live their lives as branching, fusing networks of tubular cells known as mycelium. Mycelium is how fungi feed. Animals tend to find food in the world and put it in their bodies; fungi put their bodies in the food. To do so, they must ceaselessly remodel themselves, weaving their bodies into relation with their surroundings. This entanglement-with themselves, with their physical surroundings, and with other organisms-is their staple mode of existence. On a very literal level, then, I use the word entangle to refer to the ancient growth habit of this little-understood kingdom of life.

But fungi don't keep to themselves. Mycelium is the living seam by which much of life is stitched into relation. Fungi string their way through the soil, through sulphurous sediments on ocean beds, through coral reefs, inside plant leaves, roots and shoots. Bacteria use mycelial networks as highways to navigate the bustling wilderness of the soil. Nutrients circulate through ecosystems through fungal networks. Tug on strand of mycelium and you'll find it hitched to something else. Fungi embody the most basic principle of ecology: that of the relationships between organisms. This is another sense in which I use the word entangled. Fungi form literal connections between organisms and in doing so remind us that all life forms, humans included, are bound up within seething networks of relationships, some visible and some less so.

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This relates to your question about life. Evolution's most well-worn iconography is that of a tree, mirroring the genealogical trees used to portray lines of human descent. Since Darwin, the dominant narrative within evolutionary circles has portrayed lineages as endlessly diverging from each other like the branches of a tree. But over the last several decades, it's become clear that divergence is only part of the story. Some of the most dramatic moments in the history of life occurred when single-celled organisms engulfed unrelated single-celled organisms which continued to live inside them. Within the bodies of these new composite organisms, branches of the tree of life that had been diverging for hundreds of millions of years did something entirely unexpected, and converged.

In light of these discoveries, many biologists have begun to reimagine the tree of life as a reticulate mesh formed as lineages not only branch, but fuse and merge with one another. Strands of the mesh loop in and out of the realm of viruses-entities that many don't consider to be living organisms at all-and make it clear that life shades off into non-life gradually. If anyone wanted a new poster organism for evolution they needn't look far. It is a vision of life that resembles fungal mycelium more than anything else.

Are we in broad agreement, would you say?

RM: Yes, I think so. I remember in reading Deleuze and Guattari in A Thousand Plateaus, where they take aim at the ubiquitous metaphor of the "tree" on basis of its implicitly hierarchical-vertical structure; they propose, as you know, in its place the model of the "rhizome," which weaves and moves by node and network. But I always felt they were a little harsh on trees; for as your research as a plant scientist, and your writing in Entangled Life both reveal, trees are themselves participants in a vast web of mutualisms, wafting aerosol signals between each other above ground, and sharing resources below ground via mycorrhizae...
"There are a number of ways that we might partner with fungi to help us to adapt to life on a damaged planet and we don't know nearly as much as we should."
But enough of that; I want to pick up now on those closing sentences of your answer: we are speaking to each other from our respective lockdowns here in England. The entanglement of the "realm of viruses," as you call it, with the human sphere has rarely-perhaps never-been as visible to us as it is now. It is a reminder firstly that what we call humans are profoundly multi-species beings, seething colonies of fungi, bacteria and viruses; and secondly that not all entanglement is good entanglement, as it were. I can't miss asking you to reflect on the current situation (I think you may just in fact have had Covid-19) and in particular on what might be learned from our predicament.

MS: Well I think I just had it. In the absence of widespread testing it's hard to know. In any case, my experience was mercifully short. I woke up feeling like I had aged 80 years overnight and after a miserable day in bed I was more or less back to normal. What can we learn from our predicament? I think it depends on how much we're willing to learn. In 2016 the UK underwent an exercise to simulate the effect of a viral pandemic on the country's systems and infrastructure. It revealed terrible shortcomings, yet insufficient action was taken because those in power were unwilling to learn. Right now we can see a wide range of governmental responses to a common threat, from competence to tragic confusion. I expect that we'll see a similarly wide range of willingness to learn. Perhaps it will become clear-to those who remain unpersuaded-that a stubborn refusal to change our habits is fatal.

The planet is made up of reverberating dynamic systems in which small causes can ripple into large effects. An invisibly small entity can cause human societies to grind to a halt. Are we as in control as we think? Clearly not. This isn't news. Invisibly small organisms have been shaping life on the planet for as long as there has been life. Nonetheless, for our lack of control to be revealed in such vivid and painful detail does help dispel some of our delusions and challenge us to find comfort in-or just endure-uncertainty. It's been astonishing to watch many of our social, political, and economic certainties unclamp themselves so readily. Knowing that this is possible gives me hope. When the tight grip of our dogmas and expectations are loosened we're better able to imagine, perceive, and learn. The categories and assumptions that we use to organize our lives can become questions rather than answers known in advance.

Viruses are prodigious catalysts of evolution. By shuttling genetic material between organisms they generate evolutionary novelty and have even made possible some of our deepest intimacies: as placental mammals we depend on genes acquired from viruses to develop within our mothers. Viruses enter their hosts and must suspend their immune systems; developing mammals are faced with a similar challenge. In the absence of these viral genes, it wouldn't be possible for embryos to share bodily space with their mother without being rejected as an other, a non-self. I can't stop thinking about this. Our parental care, our social bonding, our need for closeness-all have their roots in a viral infection. I hope that the current period of cultural evolution catalyzed by a virus can draw us towards a state of greater care, bondedness, and consideration-both towards other humans, and towards the more-than-humans with whom we share the planet. Of course, it could do quite the opposite.

RM: Fascinating. I have certainly been skeptical of the early wave of what might be called "pandemic utopianism"; an undetailed belief that societies will emerge from the chrysalis-phase of this crisis profoundly transformed for the (progressive) good. There is a strong counter-narrative in terms of historical precedent which finds that power consolidates power after pandemics (especially with regard to marginalized or vulnerable groups). I'm thinking particularly here of the catastrophic consequences of disease for indigenous communities in the North and South Americas, introduced by colonizers. My strong sense is that there are abundant changes for the good which might occur, but each will need to be fought for-by tired citizens, emerging from a bruising period of existence-to prevent a relapse to the status quo or worse.

Watching Milan re-imagine its urban-planning away from the current priority for choking motor-vehicles, and towards cycling and pedestrianism-in large part given the increasingly clear co-morbidity between air pollution and COVID-19-is one example of a positive change that could have taken decades now taking months. Turning back to Entangled Life, then-can I ask you to tell us a little about your own life's entanglement with fungi. How did your fascination with this world-shaping, vision-changing kingdom of life begin, and what shaped its growth?
"Ongoing environmental devastation has brought about renewed interest in the fungal world, and radical mycological possibilities abound."
MS: There are many strands. I've always been fascinated by the way that things transform. Why do things change? And how do they change? My curiosity has led me back again and again to the organisms that deftly arrange and rearrange the world. As a child I used to make piles of leaves and lie inside them to try and catch them in the process of rotting; I cultivated plants and mushrooms and watched them grow; I took up brewing. Fungi are among the most gifted of life's decomposers-and composers-and it's been hard to stay away. Of course, human lives have pivoted around the metabolic ingenuity of fungi for a long time-bread, alcohol, cheese, soya sauce, psychedelic compounds, penicillin, cancer treatments, organ transplants... it's a huge list. Fungi are often described as a hidden kingdom of life, which may be so. But many hide in plain sight and it's hard to unsee them once you've noticed they're there.

Symbiosis was another gateway concept for me. The more I learned about biology, the more I became interested in the often astonishing ways that organisms had evolved to collaborate with each other. Fungi are key players in some of the most blockbuster symbioses in Earth's history, and it was my interest in these relationships that led me to study mycorrhizal fungi and their underground networks of influence-a tangled enquiry from which I'm yet to emerge.

And then there's the urgency. There are a number of ways that we might partner with fungi to help us to adapt to life on a damaged planet and we don't know nearly as much as we should. Ongoing environmental devastation has brought about renewed interest in the fungal world, and radical mycological possibilities abound: some fungi produce powerful antiviral compounds which reduce colony collapse disorder in honeybees; in the process of mycoremediation, fungi can be harnessed to break down toxic pollutants; in mycofiltration, contaminated water can be passed through fungal mycelium which filters out pathogens and heavy metals; in mycofabrication, fungi are used to produce sustainable materials, from bricks to "leather." Not to mention the many ways that fungi change the way we think, feel, and imagine. I anticipate that my fungal fascinations will only increase as the global crisis worsens, and I suspect that I'm not alone.

RM: As someone who has also-especially in my two most recent books, Ness and Underland- tried to write about entanglement, I'd be interested to hear how you approached your task from a literary (as well as a philosophical and scientific) perspectives. This is your first book-and a wildly, wondrously ambitious first book at that. Can you tell us how you found both the work and the craft of writing at this length for the first time, on this subject?

MS: It was an adventure. Early on I decided to produce a first draft by writing very quickly and scrappily. Somewhere in this puddle of text, I hoped, I might find a book. The momentum of this approach helped prevent paralysis. It also allowed me to see more clearly the themes emerge. Reworking this formless mass became a process of trying to understand mycelium, which is conceptually and intuitively slippery: Mycelial coordination takes place both everywhere at once, and nowhere in particular; a fragment of mycelium can regenerate an entire network, meaning that a single mycelial individual-if you're brave enough to use that word-is potentially immortal; mycelial networks are indeterminate shape-shifters, living maybes that fuse and branch, decanting themselves into their surroundings.

Mycelium used to feel like a kōan, unintelligible to my mammalian mind. But I've come to think of our minds as the most mycelial parts of ourselves. Mycelium is a living, growing, opportunistic investigation-speculation in bodily form. A portrait of someone's mind might look something like a mycelial network; mind maps certainly do. It soon became clear that mycelium would be a foundational metaphor for the book whether I liked it or not. There were other guiding figures. Knots helped me a lot. Since I was a child I've loved tying and untying knots and the way it makes me think, and I often found myself imagining the book's themes and stories as cords that I could splice, braid, and weave. Music was another, in particular musical polyphony, which involves voicing more than one part or telling more than one story at the same time. In polyphonic music, melodies intertwine without ceasing to be many. Voices flow around other voices, twisting into and beside one another.

And yet, when listening to polyphonic music several streams of consciousness commingle in the mind and a multitude of parts can coalesce into a single piece of music that doesn't exist in any one of the parts alone. It was this type of listening that helped me to feel my way through the writing process. I came to think of fungal mycelium-which is both a multitude of growing tips and a single interconnected entity-as polyphony in bodily form. Mycelium is what happens when elongating fungal cells, which are streams of embodiment rather than streams of consciousness, commingle.

All the while I did my best to maintain as much contact with the fungal world as possible. I drank large pots of tea made from chaga and reishi mushrooms, for example, and tried to eat mushrooms for at least one meal a day. I still do.

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Entangled Life by Merlin Sheldrake is available via Random House.

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Fungi's Lessons for Adapting to Life on a Damaged Planet

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Merlin Sheldrake's new book Entangled Life looks at the complex world of fungi, its adaptive ability, and its interconnectedness with all other forms of life. He spoke with Robert Macfarlane,...

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Merlin Sheldrake on Embodied Entanglements- For The Wild 

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Merlin Sheldrake on Embodied Entanglements- For The Wild 

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Winding through questions of philosophy, science, and meaning making, this week's episode brings together vital thoughts on what it means to live an embodied life in an entangled world. Guest Merlin Sheldrake shares the motivations that drew him to study fungi and the complex ways this study has shaped his life and thought.

As Merlin shares, "an account of life that doesn't include fungi is an account of life that doesn't exist." Our relationship with fungi is non-negotiable. Merlin invites listeners to pay attention to what this relationship means and how it shapes not only our lives, but the entanglement of life across the world. With this, Merlin also shares the ways fungal life offers a diversity of expressions and possibilities - offering up the perspective that the diversity and complexity of relationship and expression is what makes life fertile.

Across the episode, Merlin and Ayana contemplate the history and meaning of science, and come to see life as a process and a relationship, for "being is always being with and becoming is always becoming with." The meaning we make does not come out of a vacuum, but rather out of relationship. The ways that we process information and create metaphors show us who we are as a culture. Life itself, in its many forms, is improvisational. Understanding this, we are left with the provocation: How might we speak to the world, rather than about it?

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MERLIN SHELDRAKE on Embodied Entanglements /365 - FOR THE WILD

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Merlin and Ayana contemplate the history and meaning of science, and come to see life as a process and a relationship, for "being is always being with and becoming is always becoming with." The meaning we make does not come out of a vacuum, but rather out of relationship.

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Dr. Patricia Kaishian on Queer Mycology- For The Wild

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Dr. Patricia Kaishian on Queer Mycology- For The Wild

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How might a mushroom challenge global control? In this episode, Dr. Patricia Kaishian encourages us to think of mycology as a revolutionary and political practice. Diving into queer mycology, we see the ways that fungi challenge binaries of gender, family structure, and even traditional biological classification. Queer theory teaches us that difference is necessary and fluidity is vital. Queer mycology shows us this applies to the more-than-human. Fungi do not make easy subjects of capitalism. In the tradition of queer theory, how might we learn from fungi rather than being threatened by their binary and definition-defying presence?

Thinking on the urgency of climate change and its affects on our ecologies, knowledge about fungi is vital for the earth's survival and our own spiritual survival. Dr. Kaishian, then, guides us to challenge science to maintain its integrity in the face of capitalistic incentives, and through this guidance brings us to a better understanding of the need for an ethical science that addresses the vital concerns of a changing climate. In this vein, Dr. Kaishian shares her experience in the Armenian diaspora and the need for explicitly political science and mycology in the wake of settler colonialism and genocide.

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Dr. PATRICIA KAISHIAN on Queer Mycology /262 - FOR THE WILD

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Dr. Patricia Kaishian encourages us to think of mycology as a revolutionary and political practice. Diving into queer mycology, we see the ways that fungi challenge binaries of gender, family structure, and even traditional biological classification. Queer theory teaches us that difference is necess

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Patricia Ononiwu Kaishian: Queer Mycology

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Patricia Ononiwu Kaishian: Queer Mycology

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Mycological Association of Washington DC

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Patricia Ononiwu Kaishian: Queer Mycology (MAWDC 6/4/23)

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The Science Underground: Mycology as a Queer Discipline

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The Science Underground: Mycology as a Queer Discipline

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This article explores the science of mycology through a queer theory framework

with the intention of situating the state of the field in a historical and social context. With the understanding that everything is in community with fungi, we look to the biology and ecology of these organisms for transformative inspiration and a deep-time sense of belonging. Our scientific understanding of mushrooms and other fungi has been shaped and indeed impeded by mycophobia, a condition of fear and revulsion that we compare here to queerphobia. In this work, we argue that mycology relies upon queer methodologies for knowledge acquisition given both the nonbinary, cryptic, and subversive biological nature of fungi as well as a hegemonic, Western, cultural rendering of fungi as perverse and unworthy of formal investigation. We further argue that the queer methodologies of mycology that developed in response to these conditions have enhanced rather than hindered our knowledge of fungi. Because our ultimate quest as scientists is the pursuit of truth, as best as we can determine, we suggest that scientists would do well to meaningfully reconcile with the inescapable and oftentimes queer reality of bias and subjectivity.

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The International Congress of Armenian Mycologists (ICAM)

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The International Congress of Armenian Mycologists (ICAM)

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The International Congress of Armenian Mycologists (ICAM) is a network of research scientists of Armenian ethnicity. Our diverse research backgrounds on various aspects of fungal biology are allied in the mission of biological, ecological, and social welfare of all Armenian life forms. As an organization we strive to conduct critical scientific research on the understudied fungal kingdom in the both ancient yet contemporary civilization of Armenia.

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Exploring fungal diversity through DNA barcoding and sequencing services. Also facilitates awesome country-wide Mycoblitz's!

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North American Mycological Association Affiliated Mycology Clubs 

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North American Mycological Association Affiliated Mycology Clubs 

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A pretty broad list of Mycoology clubs around North America!

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Clubs - North American Mycological Association

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NAMA Clubs OUR CLUBS NAMA Affiliated Clubs Use our map to find a club near you!

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The Fungi Foundation is a global organization that explores Fungi to increase knowledge of their diversity, promote innovative solutions to contingent problems, educate about their existence and applications, as well as recommending public policy for their conservation.

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Rewilding Mycology aims to promote the value of of fungal biodiversity in nature conservation projects

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We use the Green Bottle Method to to visually explain what real sliding scale means, that we must think about income level, class background, and costs. (In other words, which 'bottle' best represents your current financial situation?)

There's a lot of trust here. Sliding scales require truthfulness and transparency that can feel jarring since prices and costs are usually fixed.

If you are able to pay more or full price for the service of organizing this gathering, please know that you are actively ensuring that people who may be facing financial barriers can still receive vital community care + education, teachers and presenters can be given even more fair exchange for their contribution and we are able to serve the land, people and ecology of the New Moon Mycology Summit better.

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New Moon Mycology Summit - The Mycelium Underground

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We use the Green Bottle Method to to visually explain what real sliding scale means, that we must think about income level, class background, and costs. (In other words, which 'bottle' best represents your current financial situation?) There's a lot of trust here.

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Guidelines for a Successful Mushroom Fair - North American Mycological Association

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Guidelines for a Successful Mushroom Fair​ Our publications hail from the inception of the organization in 1967. NAMA's founder, Henry Knighton, produced the first Mycophile newsletter in 1960. The Mcilvainea Read more

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Academic Mycology Certificate- Evergreen State College 

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Academic Mycology Certificate- Evergreen State College 

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This 24-credit certificate program is designed for students and professionals seeking a foundation of knowledge and skills in mycology. This includes mycology training for natural resource managers, farmers, environmental scientists, restoration ecologists, and clinical social workers, health professionals, educators, and entrepreneurs.

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What You'll Learn

This 24-credit certificate program is designed for students and professionals seeking a foundation of knowledge and skills in mycology. This includes mycology training for natural resource managers, farmers, environmental scientists, restoration ecologists, and clinical social workers, health professionals, educators, and entrepreneurs.

Interest in fungi for human health and the environment has exploded in the last decade. The value of specialty mushroom sales in the US exceeded $1 billion in 2021 and the psychedelic medicine industry has been projected to reach close to $7 billion by 2027. There is a need for individuals qualified to grow and evaluate the safety and effectiveness of medicinal and nutritional mushroom products, as well as their potential in biotechnology, psychotherapy, and bioremediation. These career paths require knowledge of fungal biology along with chemistry, skills in the cultivation, identification and culturing of fungi, and training in community-based, sustainable, and ethical business practices.

Certificate Prerequisites

Students need at least 8 credits of college-level biology before taking the core courses: Medicinal Fungi and Environmental Applications of Fungi. Topics covered in previous biology courses should have included cell and molecular biology, diversity of life, ecology and evolution.

Email certificates@evergreen.edu if you have questions about these prerequisites.

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This 24-credit certificate program is designed for students and professionals seeking a foundation of knowledge and skills in mycology. This includes mycology training for natural resource managers, farmers, environmental scientists, restoration ecologists, and clinical social workers, health professionals, educators, and entrepreneurs. Interest in fungi for human health and the environment has exploded in the last decade.

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Certified Mycology Diploma Course- Centre of Excellence 

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Certified Mycology Diploma Course- Centre of Excellence 

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The Mycology Diploma Course provides a comprehensive introduction to the study of fungi – their biology, biochemical properties and genetics, as well as their interactions with human beings and the ways in which they can contribute to our health and produce diseases.

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Mycology Diploma Course - Centre of Excellence

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A comprehensive introduction to the study of fungi - their biology, biochemical properties, genetics, and interactions with human beings.

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MycoCreation Course- an 8 Module Online Mycology Course 

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MycoCreation Course- an 8 Module Online Mycology Course 

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The live version of this course is finished, but you can now purchase the recordings and associated materials to learn at your convenience!

($150)

The MycoCreation Course is an immersive, deep-dive into the vast world of fungi, which ranges a multitude of topics.

Each purchase will come with the recording of the class or classes, the associated presentation slides, resources to further your learning, access to the course padlet and more!

If you have particular fields of interest, you can sign up for classes individually (see each class and description below).

Fungal biology & ecology

the KINdom of fungi, from micro to macro

taxonomy & phylogeny

nutritional modes & anatomy

asexual & sexual life cycles

Evolutionary biology through the fungal lens

Mycorrhizal fungi & mycoheterotrophy

Nutrient cycling & ecosystem dynamics

Fungal interactions: plants, animals, bacteria & beyond

A review of basic fungal biology & ecology aimed at deepening our relationships while in the field

How to seek fungi ecologically & successfully

Anatomy, morphology, & identification

Edibles, medicinals, poisonous/deadly & "look-alikes"

Honorable & regenerative foraging practices

Tools & safety

Cultivation: past to present

An overview of fungal biology and the fungal life cycle for cultivation purposes

Techniques & ideologies

Indoor/Outdoor

laboratory skills & design

substrates, media, preparations & fruiting

Synergizing practices: Mushroom seeking meets cultivation

Cultivation as applied mycology: mycoremediation, mycofabrication, entomopathogenic fungi (biocides)

Part One:

Review of mushroom biology & ecology through the medicinal lens

Medicinal Ethnomycology

Fungal constituents: how the medicine fungi make for themselves is also medicine for us

Grounding sensational claims in actual research: discussing in vitro, in vivo, human clinical trials

Navigating the flood of medicinal mushroom products

Medicine making techniques:

Part Two:

Bioremediation

The connections between remediation, regeneration & our internal-external landscapes

Mycoremediation in water and land:

how does it work?

the connections between lignin, petrochemicals & fungal enzymes

organic & non-organic pollutants

facilitated adaptation (not "training")

in situ, DIY, low-tech & low cost remediation

remediation in fire ecologies

Case studies: Bay Area Applied Mycology (BAAM) & CoRenewal (formerly Amazon Mycorenewal Project)

Other noteworthy projects & grassroots efforts

Taye Bright is a mycologist, naturalist and all-around biophile passionate about fungal ecology, plant-fungal symbioses, bioremediation, ethnomycology, community science and conservation.

Taye is a post-fire bioremediation researcher for the Fire Ecology Network in X-Site Study (FENiXS), a climate adaptation study investigating the effects of microbial and fungal inocula on community resilience and ecosystem recovery. She is also a field mycologist for the CA Fungal Diversity Survey project and co-coordinator for the West Coast Rare Fungi challenge. She leads classes, courses, workshops and walks around California and beyond focusing on increasing accessibility of mycological and ecological education outside of conventional academia. Taye is the Education and Outreach coordinator for CoRenewal, on the Conservation and Stewardship committee for the North American Mycological Association, and sits on the board for the Sonoma County Mycological Association and Bay Area Applied Mycology.

With a reverence for all things weird & wild, Taye is a devotee to the Kindom Fungi and the holistic regeneration of our living Earth. She strives to illuminate the importance of inter-species kinship and to help deepen peoples' sense of place and purpose as an integral part of Earth's unfolding story.

Ryath Fujita Beauchene is a mushroom seeker & cultivator, horticulturalist & ecologist who works as a mycological educator, outdoor mushroom farmer & estate manager in Sonoma County, CA.

Ryath studied ecology and environmental education at Sonoma State University where he received an interdisciplinary BA engaging the cross-sections of outdoor leadership and ecological translation.

Ryath is curious and enchanted by the world and its myriad expressions, hooked on life through the lenses of nutrition, ecology, fungi, plants, soil, endosymbiosis, herbalism, photography, cooking, and the maintenance of human-made thingamajigs.

Ryath's has great hope that someday we will realize that separateness and isolation are human-constructed illusions, the interconnected reality of every process we call a thing is literally immeasurable, and that love will live forever in the infinite universe. (And then we will all sing with Beautiful Chorus.)

We want to share our passion with the world and incite curiosity for everyone. We have thus attempted to price our courses at a relatively accessible level and are pouring all of our fungal and planetary love into our work. We hope to make our sharing way more than worth the "ticket" value.

Yet, we acknowledge: what is modest to one is outrageous to another. If our courses feel financially inaccessible to you and you feel you would benefit greatly from attending, please reach out below to let us know. We will consider partial or full scholarships for those in need.

"This course was amazing. It is a deep dive into the delightful and diverse world of fungi. From cultivation to folklore, I couldn't even choose which part was my favorite; the multi-faceted approach truly does fungi justice (although...Amanita! You deserve all the attention you get, you beautiful creature!). Taye and Ryath's knowledge and enthusiasm for the subject infuses their teaching, making the time fly by and leaving your mind buzzing and hungry for more."

- L

"I came across this course a couple days before it began back in 2022 and I am so glad I enrolled. It was such an enjoyable experience! Very comprehensive, yet easy to understand as a beginner and opened the door to many new mycological interests that I have gone on to continue studying and working with. Taylor & Ryath are intelligent & passionate teachers, I highly recommend this course."

- Sabrina

"This course is richly packed with information conveyed with creative enthusiasm by experts with direct hands-on knowledge of their domain. Detailed, generous, engaging and interactive, endlessly fascinating. This course is an extraordinary resource and incredible value with so many wonderful takeaways across a sweeping survey of all things mycological. I'm so very grateful to Taye and Ryath for sharing their knowledge, experience, and so much heart put into crafting and curating this course. Thank you so very much!"

- Mark S.

"Learning alongside Taye and Ryath in this course was incredibly delightful. Their knowledge is grounded in love and shares a rhizome with their deeply rooted values of reciprocity, curiosity, right relationship, and justice. There was more inspiration packed into each week than I could possibly digest--I will be revisiting this course for the rest of my life!"

- Anna

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The live version of this course is finished, but you can now purchase the recordings and associated materials to learn at your convenience! Each purchase will come with the recording of the class or classes, the associated presentation slides, resources to further your learning, access to the course padlet and more!

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Common Mycorrhizae Network: A Review of the Theories and Mechanisms Behind Underground Interactions

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Common Mycorrhizae Network: A Review of the Theories and Mechanisms Behind Underground Interactions

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Institute of Soil Science, Leibniz Universität Hannover, Hannover, Germany

Most terrestrial plants establish symbiotic associations with mycorrhizal fungi for accessing essential plant nutrients. Mycorrhizal fungi have been frequently reported to interconnect plants via a common mycelial network (CMN), in which nutrients and signaling compounds can be exchanged between the connected plants. Several studies have been performed to demonstrate the potential effects of the CMN mediating resource transfer and its importance for plant fitness. Due to several contrasting results, different theories have been developed to predict benefits or disadvantages for host plants involved in the network and how it might affect plant communities. However, the importance of the mycelium connections for resources translocation compared to other indirect pathways, such as leakage of fungi hyphae and subsequent uptake by neighboring plant roots, is hard to distinguish and quantify. If resources can be translocated via mycelial connections in significant amounts that could affect plant fitness, it would represent an important tactic for plants co-existence and it could shape community composition and dynamics. Here, we report and critically discuss the most recent findings on studies aiming to evaluate and quantify resources translocation between plants sharing a CMN and predict the pattern that drives the movement of such resources into the CMN. We aim to point gaps and define open questions to guide upcoming studies in the area for a prospect better understanding of possible plant-to-plant interactions via CMN and its effect in shaping plants communities. We also propose new experiment set-ups and technologies that could be used to improve previous experiments. For example, the use of mutant lines plants with manipulation of genes involved in the symbiotic associations, coupled with labeling techniques to track resources translocation between connected plants, could provide a more accurate idea about resource allocation and plant physiological responses that are truly accountable to CMN.

Mycorrhiza Network: Theoretical Background

Mutualistic associations between mycorrhizal fungi and plants are well-known. Within the diverse mycorrihza types, the arbuscular mycorrhizae (AM), from the phylum Glomeromycota, is one of the most common, ancient and widespread, associating with around 80% of all land plant species ( Schüßler and Walker, 2011). This fungi type is more predominant in warm climates and species rich ecosystems, such as tropical forests. The second most common fungi type in nature is the ectomycorrhizal (EM) fungi. Although a lower number of plant species have been found to form symbiosis with EM, in comparison to AM, the hosts of EM tend to be widely dispersed, abundant and dominant members of their groups ( Brundrett, 2009; Teste et al., 2020). Different from AM, EM fungi are mainly found in colder regions and ecosystems, where less host species are present, e.g., temperate and boreal forests ( Brundrett, 2009; Gorzelak et al., 2015). AM and EM networks are assumed to differ in their structure, but both affect plant responses, such as growth, photosynthesis rate, nutrition, survival, and others ( Gorzelak et al., 2015). Besides, AM and EM fungi species are frequently found co-existing in the same ecosystem. Some exceptional plants are even able to host both types of fungi in its roots, although the proportion of the association with each may differ along plant's life ( Gorzelak et al., 2015).

Mycorrhizae fungi are widely recognized to improve plant nutrition by being able to access soil spaces and nutrient sources inaccessible for roots ( Smith and Read, 2010, Wipf et al., 2019; Andrino et al., 2021). The great majority of mycorrhizae fungi are not host specific, being that a single mycorrhizae fungi specie is able to colonize a wide range of plant species. Once a fungi colonize the host plant, its mycelium is able to grow over large distances in the soil and may reach and colonize the roots of multiple neighboring plants, from the same or different species ( Van Der Heijden and Horton, 2009). Therefore, plants sharing the same host fungi are reported to become interconnected by the so-called common mycorrhiza network (CMN) ( Heaton et al., 2012; Rhodes, 2017; Wipf et al., 2019). Connectivity are therefore likely to occur between plants able to associate with the same fungi species.

As ecosystems are usually dominated by mycorrhizal plants, including most temperate and tropical grasslands as well as boreal, temperate and tropical forests ( Read, 1991; Van Der Heijden, 2016), abundant and extensive mycorrhizal fungal networks are formed ( Wipf et al., 2019). It is believed that plant species can interact and communicate via these CMNs ( Gorzelak et al., 2015; Pickles et al., 2017; He et al., 2019). This may affect survival and behavior of connected plants as well as competitive and cooperative patterns, consequently influencing plant diversity at local and regional scales ( Deslippe and Simard, 2011; Simard et al., 2012; Bücking et al., 2016). Among the reported effects of such connectivity are the improvement of seedling establishment ( Bingham and Simard, 2011; Seiwa et al., 2020), impact on plant and microorganism community compositions ( Meng et al., 2015; Teste et al., 2015; Kadowaki et al., 2018), induction of plant defense responses ( Babikova et al., 2013; Song et al., 2014), plant communication through a variety of phytohormones such as jasmonic acid, methyl jasmonate and zeatin riboside ( Song et al., 2010), and nutrient exchange, which may play a pivotal role for interplant nutrition ( Bücking et al., 2016; He et al., 2019; Fang et al., 2021).

In the review made by Van Der Heijden and Horton (2009) it is stated that CMN can be compared either to "socialist" or "capitalist" systems, or even to a "superorganism." For the "socialist" behavior, individuals are able to have equal opportunities and resources are distributed more evenly providing benefits for all connected plants. For the "capitalist" network, mycorrhizal would be privately controlled for the profit of certain group of plants, increasing therefore competition between connected plants. If network behaves as a "superorganism," fungal species in the network are considered redundant physical extensions of the roots, which might translocate nutrients freely between plants. Therefore, the mode of interplant connection might have evolutionary consequences of CMN by substantially defining the community ecology of a site, leading to ecosystem-wide impacts ( Gorzelak et al., 2015). This depends largely on which of these responses are predominant ("socialist," "capitalist," or simple physical extensions) in the moment plants are connected; together with the question whether these responses may change if plants from the same or from different species are connected.

In face of all the possible effects of CMN on plant interactions, many different theories have been raised with the intention to predict how mutual association and co-existence of species in the system is stabilized. By one hand, we have the biological market theory, for example, which is based on the assumption that fungi might recognized the best plant partner and re-allocate nutrient accordingly to its carbon (C) gain. On the other hand, we have the source-sink theory in which resource would move in a concentration gradient. This could lead resources to be distributed more equally among partner involved in the network, which is the opposite of what is expected if the biological market is driven resource allocations. Both theories will be more detailed discussed in the following sections. Nevertheless, benefits and disadvantages from the interactions between connected plants are hard to distinguish in nature, once most of the plants are colonized simultaneously by multiple fungal species, each one with its own cost-benefit. In addition, in natural ecosystems, not only mutualistic interaction between connected mycorrhizal plants takes place, but networks may also include commensalistic and even antagonistic interactions ( Toju et al., 2013). Therefore, some plant species might benefit from CMN more than others, depending on the fungi and plants involved in the association. It is important to note that, even if plants would be connected mainly by a single mycorrhiza type, i.e., AM fungi, variations in the functional properties and temporal patterns of different strains can also be observed ( Kiers et al., 2011). This adds further complexity to the potential mechanisms by which such network would determine plant community composition and productivity through their facilitative and antagonistic effects on plants ( Wagg et al., 2015). Therefore, predicting ecosystem dynamics of connected plants is still a huge challenge.

Due to the high complexity to discriminate effects of CMN in natural ecosystem, the majority of studies aimed to evaluate the influence of CMN for connected plants were mainly performed with few species of plants growing in pairs in microcosms and under controlled environmental conditions. Even under such controlled situation, the outcomes may still vary significantly, once benefits of connected plants may change according to host's physiological status, plants and fungal species involved, environment conditions, nutrient availability, etc. ( Wagg et al., 2011). With this in mind, it is necessary to assess the most recent findings in literature and define still open questions, in order to guide upcoming studies in the area aimed to have a better understanding of possible plant-to-plant interactions via CMN and its effect shaping plants community. The present paper therefore evaluates results and theories of the functionality of CMN for plant-to-plant communication, especially, for resource exchange. Here, we also point the gaps of such studies in order to highlight especial points that need to be address in further studies.

Source Sink Theory

In the source-sink model, the source is defined as the entity that can produce more of a given resource than it uses and the sink as the entity that has the potential/necessity to use more of a given resource than it produces ( Heaton et al., 2012). The primary importance of plant-sink strength in governing the magnitude and direction of resource transfer through CMNs is illustrated in studies showing transfer of C to rapidly growing young EM trees with high transpiration rates, or to shaded seedlings with high respiration demands, increasing its survival and growth ( Lekberg et al., 2010; Philip et al., 2010). Similarly, transfer of other resources, such as nitrogen (N), were also reported following a source-sink pattern ( Montesinos-Navarro et al., 2017; Muneer et al., 2020). This mechanism has been proposed to increase the regenerative capacity of forest ecosystems ( Teste et al., 2009, 2010). However, there are also reports of reduced transfer of C within a CMN to sink (shaded, defoliated, seedling) plants ( Kytöviita et al., 2003; Walder et al., 2012), and even C transfer from sink (shaded) plants to source plants ( Deslippe and Simard, 2011). Thus, a better understanding of the forces driving such interactions is required, since it has profound implications for our understanding of plant communities and competition. Depending on the species involved in the CMN and the possible effects for its fitness, it will drive forest community composition and dynamics ( Beiler et al., 2010; Simard et al., 2015).

Biological Market Theory

Asymmetry on resource allocation has been also demonstrated to increase competition between connected species ( Merrild et al., 2013; Weremijewicz et al., 2016). Merrild et al. (2013) found that the growth suppression of small neighboring plants was diminished by clipping the shoots of large plants, which also increased the P uptake by interconnected small neighbors 6.5-fold. In order to exclude that suppression was caused by a general negative growth response, treatments including solitary vs. networked seedling was performed. In the referred study, suppression occurs only when seedlings were linked to the extraradical mycelium (ERM) of the large plant. Therefore, the authors concluded that the observed effects could solely be attributable to the CMN effect. However, such results has to be interpreted carefully, since inherent characteristics of plant species involved, such as growth rate, size, and root:shoot ratio, are likely to influence observed nutrient uptake.

Nevertheless, based on the observed results, an alternative theory has been proposed to elucidate such effects, the biological market theory. This theory is based on the assumption that both, plant and fungi, are able to detect variation in quality and amount of the resource supplied by their partner, allowing them to adjust their own resource allocation according to its gains ( Kiers et al., 2011; Walder and van der Heijden, 2015; Werner and Kiers, 2015; Wang et al., 2019). Kiers et al. (2011) used molecular markers and stable isotope probing to track C flow from Medicago truncatula hosts into fungal RNA of roots colonized by mixed AM fungal communities with different cooperative behavior to the host plant. The authors found greater C enrichment in the most beneficial fungal species, suggesting a preferential allocation of C by the host, operating in a small spatial scale. The opposite flux was also observed, in which the fungi delivered more P for the host, which provided more C to fungi. Fellbaum et al. (2014) also evidenced fungal discrimination by greater N allocation to the host under elevated C allocation. If "rewards" indeed are reciprocal between mycorrhizal fungi and host plants, larger plants are supposed to obtain larger amounts of limiting nutrients by the fungal networks once they can produce and allocate much more C to the fungal partner. Increasing competition and suppressing growth of smaller individuals thus makes CMN a stronghold to avoid outcompeting its own kind.

It is important to note that the market theory proposed by some authors goes in an opposite direction to what was stated in the "source-sink" theory presented above. Neither theory should be defined as an universal framework to explain resource exchange in the mycorrhizal association nor predict plant interactions within a CMN, since the outcome of such interactions may vary with environmental conditions, functional diversity, competition for surplus resources, reciprocity and sink strength. Therefore, the effect of each variable should be tested separately and considered into the proposed models in order to define a more universal framework.

Underground Connectivity

Both the source-sink theory and the market theory relies on the prerequisite of an underground connectivity of plants via CMN. In general, ecologists agree on the definition of CMN as a physical linkage among plants via the mycelia of the mycorrhiza fungi and that this linkage is common in nature ( Simard and Durall, 2004; Simard et al., 2012; Hoeksema, 2015). However, this premise comes from observations that species of AM fungi are often compatible with multiple host plant species. In addition, Giovannetti et al. (2001) have demonstrated the ability of genetically compatible hyphae to anastomose (fusion), with disappearance of hyphal walls and exchange of cytoplasm and nuclei ( Barreto de Novais et al., 2017). Both findings suggesting that CMNs are probably ubiquitous, although confirmation of such assumption still requires direct evidence for these linkages in the field. In this context, plants of same and different species have been reported sharing same fungi species or even same genet in several ecosystems ( Simard et al., 2012; Beiler et al., 2015). Some authors have estimated the potential of plants to become interconnected by evaluating the similarity between mycorrhizal community composition, assuming a greater similarity when plants are connected through a CMN ( Beiler et al., 2010; Diédhiou et al., 2010). ( Beiler et al., 2010), for example, evaluated the distribution of genets of two species of ECM fungi ( Rhizopogon vesiculosus and R. vinicolor) among roots of individual trees of Interior Douglas-fir ( Pseudotsuga menziesii) as a network link. The authors proposed a model where trees of different ages were connected in a scale-free architecture and the larger trees served as hubs of nutrition, favoring understory regeneration, and functional continuity in the stand.

These achievements were of great importance to demonstrate the complexity of the CMN and the number and diversity of individuals that are potentially linked, resulting in a multitude of interactions involving multiple generations. However, sharing compatible species or even the same genets, does not necessarily indicate a direct connection among the host plants. Collembolas, for example, are known to feed on fungal hyphae. Such as AM fungi, they are widespread and abundant in the soil ( Ekblad et al., 2013; Ngosong et al., 2014). By grazing the hyphae of a genet connecting two or more plants, this genet can still be identified in the roots of those plants although they would no longer be connected ( Rotheray et al., 2008; Beiler et al., 2010). This is one of the examples of CMN disruption that could occur in the soil, and would be hard to identify ( Wu et al., 2005; Beiler et al., 2015). Consequently, technical difficulties in proving hyphal connections between plants are the main obstacle when identifying whether any observed effect is really an intrinsic property of a CMN.

Therefore, it is also important to prove the extent and continuity of the mycelial network, together with mechanisms driving such connections and its consequences for plant fitness. In this context, there are few non-destructive methods for mycelium network observation, especially for AM fungi, mostly by the use of root observation chambers ( Mikkelsen et al., 2008; Gyuricza et al., 2010) and in vitro dual systems ( Kiers et al., 2011; Van't Padje et al., 2021). Such studies have nicely demonstrated the architecture of the extraradical mycelium of the fungi connecting two neighboring plants, but yet the relative importance of such network under realistic conditions is frequently under debate. For experiments developed in the forest, many interferences are found and the effects and mechanisms involved in the CMN cannot be excluded from other effects, such as positive and negative plant-soil feedback due to modulation of soil microbiota and biogeochemical cycles or even by production of roots exudates that might affect growth of nearby plants ( Hu et al., 2018). Therefore, mycorrhizae studies still face challenges, raising questions if the data represents a natural situation, since there are no guarantees that evaluated effects are caused by mycorrhizae network.

Mechanisms Involved for Plant Interaction VIA CMN

Currently, the mechanisms that drive benefits and competitive interactions between plants involved into a CMN has been under debate (e.g., Fellbaum et al., 2012; Bücking et al., 2016), raising diverse theories about the mechanism in these associations. The first one is based on the assumption that established mycorrhizal plants would facilitate mycorrhization of neighboring seedlings, acting as an inoculum and C source. In this case, seedlings would be able to join a CMN, which were already stablished and supported, in terms of translocation of reduced C by the older plants. Thus, seedling would be able to get access to limiting nutrients provided by the fungi without contributing with C supply to maintain the network. The second mechanism is based on the idea that CMN will act as conduits for interplant nutrient transfer ( Gilbert and Johnson, 2017; Wipf et al., 2019). In this context, depending on how resources are distributed between connected plants, plants may either benefit by a more equilibrate distribution of resources or by increasing discrepancies of resources. In the first case, plants with higher nutritional conditions may donate excess of their resources to the receiver plants by a direct transfer. In the second case, resources might be distributed unequally favoring a certain group of individuals increasing therefore competitive interactions.

Inoculum Source and Carbon Provision

Firstly, CMN may provide an inoculum source. Association with hyphae from the CMN can be much faster in comparison to soil spore bank, by the provision of an already established fungal inoculum source by the mature tree, permitting seedlings to quickly tap into a large soil resource pool that they could not access by their own ( Bingham and Simard, 2012). Thus, this faster access to mycorrhizal services in the early plant stage, where mortality is high due to drought and biotic interactions, may be of critical importance, especially under harsh environmental conditions ( Simard et al., 2012; Teste et al., 2015). In the experiment developed by Varga and Kytöviita (2016), the proportion of colonized seedlings by three different AM fungi was strongly related to the fungal species as well as to the source of inoculum. Seedlings inoculate much faster from nearby mycorrhized plants than from spores, despite a high spore density. This premise is also supported by some field experiments showing a positive relationship between the survival rate of seedling and its distance from the mature tree ( McGuire, 2007; Grove et al., 2019). In addition, experiments involving barriers (e.g., mesh bags) or soil disturbance to manipulated seedling contact with CMN have shown higher seedling mortality when seedling are impeded to join the network ( Nara, 2006; Pec et al., 2020).

Secondly, seedling may benefit from sharing a CMN with adult established tree since adult trees might provide much more C to sustain the network while seedling invest very little C and still obtain nutrients provided by the fungi. The maintenance of fungal symbiosis can be costly, resulting in a high C demand by the fungi for its development and activity ( Smith and Read, 2010; Keymer et al., 2017; Rezáčová et al., 2017). In this context, sugars and lipids are the main C source derived from host plants transported to the fungal symbiont. Those C derived components will provide the fungi with the energy necessary for nutrient acquisition and the C skeleton for mycorrhizal growth ( Bravo et al., 2017; Bezrutczyk et al., 2018). A benefit for seedlings would arise if larger trees pay the C cost required for the growth and maintenance of the CMN, so seedlings could potentially become mycorrhized and receive the benefits of this association without expending their own C for this ( Diédhiou et al., 2010; Walder et al., 2012; Weremijewicz et al., 2016). In the study made by Högberg et al. (1999), for example, EM fungi connecting overstory pine trees with understory plants of different ages received 87-100% of their C from overstory trees and very little from understory trees. Walder et al. (2012) have shown a similar asymmetric pattern by using ¹³C of natural abundances between C ₃ and C ₄ plants without disturbing the system. The authors found that the C ₄ plant, which had the higher biomass, was invested more C to both fungal partner than the C ₃ plant but did not have a higher nutritional benefit. In this context, nutritional benefit strongly depended on the fungus involved in the CMN, in which Rhizophagus irregularis allocated nutrients preferentially to the C ₃ host plant while the CMN formed by Glomus mosseae were more balanced with respect to the nutrient allocation to both, C ₃ and C ₄, host plants. This demonstrate that C investment and nutritional benefit are not necessarily tightly linked and that some plant species can receive disproportional benefits from CMN. It is important to note that these experiments indicate that disproportional C investment by one plant does not necessarily mean a disadvantage for the other plant, especially when the cost of C is negligible for the main C donor.

Mycorrhiza Network as Conduits for Interplant Resources Transfer

The premise of a possible nutrient transfer through a physical connection established by CMN may be of great importance in agricultural, where redistribution of symbiotic costs and benefits between individuals of the same or different plant species could increase growth of connected plants and therefore reduce amounts of chemical fertilizer input ( Pena et al., 2013; Jansa et al., 2019). However, if a direct transfer of photoassimilates and nutrients between plants occurs via CMN is particularly controversially discussed ( Bever et al., 2010; Courty et al., 2010). Such transfers have been frequently reported in field and laboratory experiments using labeling compounds to trace the fate of nutrients in plants connect by a CMN, trying to demonstrate belowground resource transfer between plants of same and different species is facilitated by mycorrhizal fungi ( Teste et al., 2009; Deslippe and Simard, 2011; He et al., 2019; Fernandez et al., 2020).

In earlier studies, this mechanism was mainly observed in mycoheterotrophic plants, which are partly or entirely non-photosynthetic and indirectly parasitize green plants via CMN. These non-photosynthetic plants, also called epiparasites, associate with AM fungi emanating from the roots of surrounding green plants, therefore having access to C provided by those plants, together with other resources ( Bidartondo et al., 2002; Girlanda et al., 2006; Selosse and Roy, 2009). In addition to mycoheterotrophic plants, some green orchids or small green perennial shrubs from the Ericaceae family have also been shown to receive considerable amounts of C from their mycorrhizal fungi ( Selosse and Roy, 2009; Selosse et al., 2016). Those studies have raised the attention for the existence of a network where unrelated plants are able to transfer elemental compounds via shared fungal symbionts.

The mycorrhizal fungi which associates with mycoheterotrophic plants and green orchids usually belong to a diverse fungal taxa that also form mycorrhizae association with phototrophic tree roots ( Zimmer et al., 2008; Waterman et al., 2013; Brundrett and Tedersoo, 2018). Since C transfer were observed between mycoheterotrophic and green plants and the same fungi species connecting those plants can also colonize several phototrophic trees, theories were raised regarding the possible C allocation between phototrophic trees as well. If such networks could act as a direct pathway of C and nutrients between green plants, this could play an important role for plant to plant interactions ( Selosse and Roy, 2009; Smith and Read, 2010). Once C is an important resource for fungi growth, C allocation between plants would go to an opposite direction of the natural C flux commonly accepted in the symbiosis, which is from plant to fungi. In this case, one of the host plants would provide fungi with C and the fungi would not incorporate but channel this C through a neighboring plant. Some researchers believe that it might happen when networking fungus can acquire more C than it is required for its own fitness, therefore it may supply the excess to other plants in need ( Gorzelak et al., 2015; Prescott et al., 2020). This has been suggested as a mechanism from the fungi to ensure survival of its host plants and therefore its access to multiple C supply, in case of a potential loss of one of the hosts ( Gorzelak et al., 2015; Bücking et al., 2016). Some authors raised this theorem by using experiments involving high and low quality plants connected into a CMN ( Kiers et al., 2011; Fellbaum et al., 2014; Bücking et al., 2016). In this context, the quality of a host is determined by its C investment into the mycorrhiza, in which low quality hosts have a reduced investment while high quality host can produce and allocate higher amounts of C to fungi partner. In previous studies, shading have been frequently used to reduce the plant's ability to produce C compounds to be exchanged by limiting nutrients. In such experiments, although a discrimination between plants was observed leading to higher resources (such as N and P) allocation to high quality host of the network, the fungi also transferred nutrients for the low quality host and maintained a high colonization rate in these plants ( Kiers et al., 2011; Fellbaum et al., 2014; Bücking et al., 2016). Those mechanisms shows a possible strategy from the fungi in maintaining both high and low quality host into the network, to ensure that the possible loss of a high quality host is not harmful for its survival. This might be an important mechanism for fungi survival, especially under variable environments, as suggested first by Perry et al. (1989) and Wilkinson (1998).

In this context, Simard et al. (1997a) was one of the first to demonstrate a bi-directional flux of C between two autotrophic plants, Douglas-fir ( P. menziesii) and paper birch ( Betula papyrifera) species, sharing an EM network. Here, a great amount of C was observed to be exchanged between the plant species, with no net gain for any one of them in the end. However, in the second year of study, Simard et al. (1997b) observed a net gain of C by one of the species independently of full, partial or deep shade light intensity. However, some methodological issues regarding the experimental design of this study was unraveled later by Robinson and Fitter (1999), raising doubts regarding the ecological relevance of CMN-facilitated resource transfer. Simard et al. (1997b) used a double labeling technique ( ¹⁴C and ¹³ C) to track C exchange between plants connected by an EM network in the field and calculate proportions of C received by each individual. However, not only EM connected plants received the applied C, but AM surrounding plants not connected to the network had access to labeled C too. That demonstrate that the movement of C between plants were not necessarily exclusively by mycorrhizal links, but could have reached neighboring plant by different pathways. This is especially likely to occur when no physical barriers are used in the experiments.

Robinson and Fitter (1999) also suggested that C transferred from neighboring photosynthetic active plant to hyphae within the roots of C-stressed plants is probably a strategy of the fungi for its own growth and survival, with minor consequences for plant communities. Teste et al. (2010) using a different experimental design also showed a low net C transfer between Douglas-fir seedlings in the field relative to total C uptake by photosynthesis. The significance of the amounts transferred have been repeatedly questioned in other works ( Teste et al., 2009; Philip et al., 2010; Pickles et al., 2017), raising a center debate on whether the extent of net transfer from one plant to another is sufficiently large to affect significantly plant fitness and predict communities' dynamics. In addition, there are also reports about the accumulation of C partially or entirely in mycorrhizal roots of receiver plants, probably in fungal tissues, and not detected on shoots even under situations where root to shoot C flow is encouraged by clipping or shadding ( Robinson and Fitter, 1999; Pfeffer et al., 2004; Lekberg et al., 2010). However, some authors argue that the movement of C to receiver plant, even without transfer into plant tissues, is still an important subsidy to meet the nutrient requirements of the plant, especially under stress conditions ( Bever et al., 2010; Teste et al., 2015).

Mycorrhizal networks have also been frequently reported to play an important role for belowground transfer of N among plants, but as for C different studies lead to contradicting results. Patterns of N transfer have been studied using natural abundance (δ ¹⁵N) or ¹⁵N-enriched techniques. For the ¹⁵N-enriched techniques, fertilizer is applied directly to the growth media of the N donor root or directly to the N donor plant by exposure to ¹⁵N ₂ (in case of experiments using N-fixing bacteria as an additional symbiont to host plant) or foliar spray or petiole injection of labeled ¹⁵N (, , or urea). In early studies of several intercropping systems, a substantial one-way N transfer was demonstrated via a source-sink gradient from N ₂ fixing plants to non-N ₂ fixing plants, within a range of 20-50% ( He et al., 2009). However, when a bi-directional flux was considered it was possible to note a greater flux of N from non-fixing plants to N-fixing plants, contradicting the source-sink theory initially proposed by this system ( He et al., 2005, 2009; Pirhofer-Walzl et al., 2012).

Moreover, a transfer between N ₂ non-fixing donors and receiver plants of varying amount of N has also been observed. The transfer of N usually was reported to be lower than 5 % of N added by pulse labeling, while the direction of transport was largely found to be correlated with plant size ( Teste et al., 2009, 2015; He et al., 2019) or plant physiology ( Meding and Zasoski, 2008; Weremijewicz et al., 2018). Teste et al. (2009) also suggested that C and N move together in form of amino acids, once the stoichiometry of the relative amounts of C and N transferred was similar of this compound, but they were never identified ( Simard et al., 2015).

Interestingly, the idea of plant-to-plant transfer implies that N may flow in the "opposite" direction of what is widely known to occur. In the context of nutrient uptake, the current model suggests that P and N acquired from surrounding soil by the ERM of the fungi are transferred to the intraradical mycelium (IRM) as polyphosphate (polyP) and arginine, respectively, stored later on in vacuoles ( Hijikata et al., 2010; Bücking and Kafle, 2015). Once in the IRM, polyp, and arginine are catabolized and Pi and ammonium are released and transported to the plants through transporters present in the periarbuscular membrane ( Breuillin-Sessoms et al., 2015; Wang et al., 2017; Figure 1). Therefore, for plant-to-plant transfer, N should be transferred in the opposite direction: from plant to the IRM via transporters in the periarbuscular membrane, from IRM transferred to the ERM of the fungi and then again to the IRM of the receiver plant to be assimilated. Although many studies have been made in order to prove such transfer via connected hyphae (please check Supplementary Table 1 for some of those studies), such fluxes were never described anywhere. In the studies presented in Supplementary Table 1, it is also possible to observe that amount of N transferred via CMN is quite variable, probably due to differences in the experimental design and the choice of plant and fungi combination. In addition, transfer exclusively via mycelium connection in comparison to other possible are not distinguishable, especially in those studies in which a mesh barrier is not used to prevent roots intermingle and flow of soil solution.

Figure 1. Mycorrhizal pathways for Pi and N in AM Symbiosis. In the mycorrhizal pathway, Pi is assimilated directly via phosphate importers while ammonium () and/or nitrate () are assimilated into glutamine (Gln) and then into arginine (Arg). Assimilation will generate excess H⁺ or OH − with and , respectively. Phosphate is mainly transported in the form of polyphosphate (Poly-P) granules, which is negatively charged, making possible it association with arginine and metal ions for further transportation to the IRM. Phosphate (Pi) and transporters from the intraradical mycelium (IRM) to the interfacial apoplast are still unknown and therefore marked with a "?," requiring further study (modified from Wang et al., 2017).

Direct Vs. Indirect Transfer

Mechanistically, AM fungi can facilitate the transfer of N between plants by creating direct mycelial connections between donors and receivers ( Høgh-Jensen, 2006; Meng et al., 2015; He et al., 2019). When it comes to resource allocation through CMN, it is easy to notice a disagreement regarding its concept within published papers, even most recent ones. On the one hand some authors report a transport of nutrients via CMN exclusively via connected hyphae, thus describing hyphae as "pipelines" for resources ( Klein et al., 2016; Van Der Heijden, 2016). On the other hand, other authors describe nutrient transfer to occur at least additionally via an indirect pathway. In such pathway, compounds are exuded or leaked into the soil pool by the roots or associated hyphae of one plant and then picked up by the roots or associated hyphae of a neighboring plant or even by other microorganisms present in the soil ( Jansa et al., 2019; Fernandez et al., 2020; Fang et al., 2021). In this context, it is frequently stated in studies that CMN simply facilitate transfers between plants without further specification of the mode of transport, although this transport may occur by several pathways simultaneously between a single pair of plants ( Wang et al., 2016; Fang et al., 2021).

For these indirect pathways, resources are vulnerable for potential disruptions, such as adsorption of nutrients to soil particles, immobilization and mineralization by surrounding microorganisms, biochemical transformation, and others ( Philip et al., 2010; Simard et al., 2012). Thus, a direct pathway genuinely utilizing mycorrhizal hyphae would represent a potential conduit of resource sharing, in which resources would be free of disruption by leakage and re-assimilation by other microorganisms.

In field and laboratory studies, split root designs and root restrictive screening techniques have been used to determine the different pathways in interplant transfers ( Xiao et al., 2004; He et al., 2005; Meng et al., 2015; Muneer et al., 2020). These designs can effectively prevent contact between individual host plant root systems, but they do not entirely prevent bulk flow or diffusive chemical movement in the soil water. Therefore, some experimental designs rely on air gaps to avoid diffusion over the soil solution flow while allowing the ingrowth of hyphae but not roots. This assures that all labeled compounds found in the receiver plant using in this system can be attributed to the mycorrhizal transport ( Zhang et al., 2020; Andrino et al., 2021; Fang et al., 2021). However, these measures still do not exclude a transfer over indirect pathways, once transported resources by fungi mycelium can be released on neighboring plant compartment, leading the receiver plant to have access to resources without being connected ( Figure 2). Moreover, connections among plants can hardly be directly visualized in soils of traditional pot experiments or even under field conditions.

Figure 2. Possible movement of resources between networked plants, even when mesh barriers are used to avoid roots intermingle and flow of soil solution between connected plants. (A) Represents disrupted hyphal connections between two mycorrhizal (M+) plants and (B) possible transfer from a mycorrhized (M+) plant to a non-mycorrhized (M−) neighbor plant.

Therefore, due to the technical difficulties to distinguish between transport pathways, it still remains unknown whether transfer occurs preferentially via direct hyphae connections or through indirect pathways. Creation of new experiment set-ups using new technologies to improve previous experiments should be developed for a more accurate idea about resource allocation and plant physiological responses that are truly accountable to CMN. Manipulation of the genes involved in setting up symbiotic associations between plant and fungi partner may help to differentiate the fungal effect in such networks ( Merrild et al., 2013; Song et al., 2014). Mutant lines where the development of arbuscules is impaired and not functional are a promising starting point, and at least for M. truncatula such a mutant line is already known. Arbuscules are recognized as the main site of exchange, and comparing networks formed by wild type and mutant lines might lead to e better understanding of the effects of arbuscular network on the development of donor and receiver. Unfortunately, to our knowledge there are no such impaired mutant lines for EM fungi, therefore such studies are only possible for AM networks. In addition, some plant genera such Acacia, Alnus, Eucalyptus, Fraxinus, Populus, Salix, Shorea, and Uapaca are recognized to associate with both AM and EM fungi simultaneously ( Teste et al., 2020), although frequency of each fungi type might differ along plant life. Much less research have been made in dual-mycorrhizae plants, and how AM and EM networks may affect connected plants differently. Altogether, such experiments could be helpful in order to achieve deeper understanding of mechanisms and processes behind CMN and its impact on plant community.

Nevertheless, it is important to keep in mind that, even if resources exchanges between plants takes place mainly via indirect pathways, receiver plants can still be favored by a facilitation of its access to resource coming from neighboring plants, which may anyway play a role in plant-to-plant interaction ( Høgh-Jensen, 2006; Alaux et al., 2021).

Role of Transfer for Plant Fitness

The simple movement of elements from one plant to another does not by itself indicate a net transfer able to represent an ecological advantage on plant fitness ( Kytöviita et al., 2003; Bücking et al., 2016). Quantifying the contribution of each pathway to plant fitness is likewise a matter of discussion in most studies on CMN. However, quantification of nutrient and C fluxes exclusive to the fungal hyphae is difficult. To the best of our knowledge, there are only few quantitative information on the magnitude of C fluxes between plants sharing a CMN. In general, C transfer through CMN is not frequently considered a significant pathway for mobile C transfer among plants, although some authors suggest that even small amounts may be of great importance for receiver plant survival and development ( Wu et al., 2001; Deslippe and Simard, 2011; Klein et al., 2016). This can be especially true if the receiver plants are seedlings ( Nara, 2006; Booth and Hoeksema, 2010; Burke et al., 2018; Liang et al., 2021). Reported amounts of C vary from 0 up to 10% in literature ( Teste et al., 2010; Lin et al., 2020). Simard et al. (1997b) was the first attempting to quantify a bidirectional flux of C between plants connected via EM network, in order to evaluate its ecology significance. The authors concluded that there was no net transfer between the species. However, the study raised debate in the literature due to its difficulty in extrapolating the data from young seedlings to mature tree and the use of relevant controls ( Robinson and Fitter, 1999; Simard et al., 2012; Tedersoo et al., 2020). In addition, Simard et al. (1997b) concluded that it was not possible to distinguish whether the translocation occurred through interconnecting hyphae, soil pathways, or even both simultaneously, and, hence, did not really demonstrate the contribution of the CMN for C transfer.

A more recent approach was developed by Klein et al. (2016), attempting to evaluate C transfer between trees in a mature forest. They continuously labeled five 40-m-tall Norway spruce trees ( Picea abies) as part of a 5-year free-air CO ₂ enrichment experiment (FACE) with ¹³C-depleted CO ₂. Despite the low difference in the δ ¹³C ratios of canopy twigs, stems, and fine roots between labeled and unlabeled control (max. 2.6‰), the isotopic signal of neighboring trees belonging to same or different taxa ( Fagus sylvatica, Pinus sylvestris, and Larix decidua) were than measured to evaluate C allocation. The authors claimed to find evidences that reciprocal C transfer indeed occurred between trees, as δ ¹³C of fine roots of neighboring plants followed the same signal from the donor Picea. Most of the label was found in the fine roots, which was concluded to prove the participation of the mycorrhizae in the transfer. It was estimated that C derived from transfer represents 4% of net primary productivity.

Another point usually under discussion regarding C transfer is whether transferred C is taken up by the receiver plant for its own growth or, contrastingly, whether the C is mainly kept in the roots, probably incorporated into fungal structures, therefore not representing a meaningful advantage for the receiver plant. This was evaluated, for example, by Waters and Borowicz (1994) and Fitter et al. (1998). They assumed that by clipping the aboveground parts of living plants, additional C would be required and translocated from the roots to the re-growing clipped shoots. However, in neither of the experiments labeled C was found in the re-growing shoots of the receiver plants. Thus, the authors concluded that the transferred C remained in fungal structures. The opposite was found by Song et al. (2015) who reported labeled ¹³C in the shoots of the receiver plant. Another difference in the mentioned studies is that, in the experiment developed by Song et al. (2015), C transfer from donor to receiver plant increased by increasing defoliation of donor plant. This has been suggested as an effect of the sink-source strength of the connected plants. The authors concluded authors that defoliation could have stimulated interior Douglas-fir donor to rapidly export labile C from enriched roots to the CMN, while the rapid growth rate of ponderosa pine would created a large sink. Nevertheless, even if it is assumed that mycorrhizae might be able to transfer C from one plant to its neighbors, it remains unclear if the amounts of the transferred elements are of any significance to the receiver plant. If this amount is viable for the receiver plant, a process understanding of the switch between fungal storage and delivery to the plant is still required.

Equally contradictory is the magnitude of N transfer reported in the literature. In grassland ecosystems, N transfer was reported to vary from 0 to 72% under field conditions, while it is less variable in agroforestry ecosystems, ranging from 0 up to 16%, depending of the conditions under which the experiments were performed (e.g., in pots, field, etc.; Marty et al., 2009; Chapagain and Riseman, 2014; Meng et al., 2015; Zhang et al., 2020). In general, the high variability in the literature may reflect many different factors that might interfere in plant-to-plant interaction, such as differences in environmental conditions, in the different experimental setups, or plant and fungi combinations, soil nutrient supply, additional stress conditions added (e.g., nutrients deficiency, drought, shading, etc.), and the general experimental design (e.g., field, pot or microcosmos experiments). In addition, like for C, quantification of N transfer via interconnecting hyphae is not distinguishable from other pathways ( Montesinos-Navarro et al., 2016; Fang et al., 2021). The distinction and relative importance of the different pathways determines the strength, direction, and outcome of interactions among plants and soil organisms, requiring new technologies and ideas to address such issues. Nevertheless, the many researches made on this topic so far developed different hypotheses that could give us some hints on how CMN would affect plant-plant interaction.

Conclusions

Despite of the great progress in understanding the effect of mycorrhiza network for plant-to-plant interactions, and how this might affect mycorrhizal communities, there are still important questions to be answered in future researches. Resource allocation between connected plants thereby drew the largest attention of the scientific community. Many possible effects of such transfers of resources have been described, but contrasting results were frequently found. Labeled experiments using C and N isotopes have revealed that under certain conditions a movement of such resources between donor and receiver plants seem to happen, but none of them could demonstrate unequivocally that the transfer occurred preferentially through the direct mycorrhizal pathway and not over the soil solution or simply over exudates. Moreover, quantification of this transfer demonstrated to be an even bigger challenge. Therefore, the real effect of the CMN in shaping plant communities is still not clear. Further research involving new experiment set-ups and new technologies to improve previous experiments should be developed for a more accurate idea about resource allocation and plant physiological responses that are truly accountable to CMN. The use of mutant lines with manipulation of the genes involved in setting up symbiotic associations between plant and fungi partner together with labeling techniques to track resources translocation between connected plants can be used to differentiate the fungal effect in such networks. Effects exclusively to CMN for plant interactions may help us to understand plant community and ecosystem functioning.

Author Contributions

AF, JB, and GG conceived the idea about the topic reviewed in this manuscript. AF wrote the manuscript. JB and GG contributed with corrections and comments and approved the submitted version. All authors contributed to the article and approved the submitted version.

Funding

We want to thank the German Research Foundation (Deutsche Forschungsgemeinschaft) for the funding of this project in the framework of the DFG-GRK 1798 Signaling at the Plant-Soil Interface. The publication of this article was funded by the Open Access fund of Leibniz Universität Hannover.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/ffunb.2021.735299/full#supplementary-material

References

He, X., Critchley, C., Ng, H., and Bledsoe, C. (2005). Nodulated N2-fixing Casuarina cunninghamiana is the sink for net N transfer from non-N2-fixing Eucalyptus maculata via an ectomycorrhizal fungus Pisolithus sp. using 15NH4+ or 15NO3- supplied as ammonium nitrate. New Phytol. 167, 897-912. doi: 10.1111/j.1469-8137.2005.01437.x

Simard, S. W., Jones, M. D., Durall, D. M., Perry, D. A., Myrold, D. D., and Molina, R. (1997a). Reciprocal transfer of carbon isotopes between ectomycorrhizal Betula papyrifera and Pseudotsuga menziesii. New Phytol. 137, 529-542. doi: 10.1046/j.1469-8137.1997.00834.x

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Common Mycorrhizae Network: A Review of the Theories and Mechanisms Behind Underground Interactions

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Most terrestrial plants establish symbiotic associations with mycorrhizal fungi for accessing essential plant nutrients. Mycorrhizal fungi have been frequently reported to interconnect plants via a common mycelial network (CMN), in which nutrients and signaling compounds can be exchanged between the connected plants.

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Mycorrhizal ecology and evolution: the past, the present, and the future

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Mycorrhizal ecology and evolution: the past, the present, and the future

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Global biogeography of marine fungi is shaped by the environment

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Global biogeography of marine fungi is shaped by the environment

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Fungi in the Marine Environment: Open Questions and Unsolved Problems

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Fungi in the Marine Environment: Open Questions and Unsolved Problems

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Targeted ITS1 sequencing unravels the mycodiversity of deep-sea sediments from the Gulf of Mexico

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Targeted ITS1 sequencing unravels the mycodiversity of deep-sea sediments from the Gulf of Mexico

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We study the taxonomy and ecology of marine fungi & fungi associated with coastal and marine plants in the Department of Biology at Acadia University. Research in our lab includes field collecting in coastal habitats (saltmarsh, intertidal, seagrass, Acadian forest) as well as agroecosystems, and traditional culture-based and microscopic identification of fungi. This is combined with modern molecular systematic and phylogenetics, DNA community fingerprinting, ITSbarcoding, quantitative-PCR, genomics & metagenomics. Recent collaborative projects have discovered a new obligate marine fungus Lulworthia fundyensis and explored fungal interactions with microarthropods in salt marshes.

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COASTAL AND MARINE MYCOLOGY TAUGHT BY DR. CHRIS SMYTH FROM SUNY BINGHAMTON UNIVERISTY

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This course will explore the diversity, ecology and evolution of coastal and marine fungal species. Marine fungi are an understudied and underappreciated group of organisms. Like many microorganisms, marine fungi play integral roles in ecology and biogeochemistry in coastal and ocean ecosystems. These fungi can be found anywhere from beach sand to marine sponges. Through this course, students will gain an understanding and appreciation for the diversity of fungi thriving in the maritime forests, estuaries, salt marshes, eelgrass beds and the coastal waters of Virginia's Eastern Shore.

The focus of this class is to survey the fungal diversity of the near-pristine coastal and marine ecosystems of the Chincoteague National Wildlife Refuge, Wallops Island National Wildlife Refuge, and the Assateague Island National Seashore. There is very little known about fungal diversity in these areas. As a class, we will work to create species lists with real-world implications in the discovery, documentation and conservation of fungi.

Field trips will include hikes, kayaking, and boat trips. Marketable Skills Gained from This Course:

Collection and preservation of fungal specimens in the field and lab

Field data collection and analyses

Fungal biodiversity survey techniques

Mushroom Identification

Microscopic Identification of Marine Fungi

Microbiological Culturing Techniques

Dissecting & Light Microscopy

Critical evaluation of peer-reviewed literature

Science Communication

Students will visit a number of ecosystems to observe and collect fungi, including:
Approximate Amount of Course Time Spent in Field:
50%

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An epic compilation of mushroom cultivation resources by the North American Mycological Society

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Mushroom Cultivation Links - North American Mycological Association

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Mushroom Cultivation References Home Cultivation Supplies: kits, spawn, books etc. Fungi PerfectiPaul Stamets, leader in the home cultivation field - supplies, books, kits, everything a mushroom cultivator needs. Field and Read more

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Maintaining California Lichen Diversity in an Era of Global Change: Dr. Jesse Miller

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Maintaining California Lichen Diversity in an Era of Global Change: Dr. Jesse Miller

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Lichens surround us and though they are rarely noticed, they are sensitive environmental indicators and play critical ecological roles. California is a continental hotspot for lichen diversity, but its lichen communities are among the most threatened in North America. In this talk, Jesse Miller will discuss his research on the effects of altered wildfire regimes on California lichen communities, with case studies from low- to mid-elevation conifer forest in the Sierra Nevada and old-growth chaparral in the Coast Range of Napa County. He will also present recent research conducted with an undergraduate class that uses lichens to monitor air pollution in the vicinity of the Stanford campus. Jesse Miller has spent many years working as a botanist and lichenologist across California and the Pacific Northwest. He is currently a lecturer at Stanford, where he teaches several ecology classes. Jesse’s research interests include the effects of global change factors such as altered fire regimes on lichen and plant communities.

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Maintaining California Lichen Diversity in an Era of Global Change: Dr. Jesse Miller

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CATALOG OF LICHENS, LICHENICOLES AND ALLIED FUNGI IN CALIFORNIA (second revision)

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CATALOG OF LICHENS, LICHENICOLES AND ALLIED FUNGI IN CALIFORNIA (second revision)

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This second revision of the California lichen catalog reports 1,869 taxa at species level and below (of which 58 are recognized at the level of variety, subspecies, or forma) for the state, an increase of about 295 taxa since 2006, and 565 taxa since the 1979 catalog. The number of genera is 340, an increase of 43 since 2006. The lichen flora of California includes about 35% of the 5,246 species and 52% of the 646 genera reported for the continental United States and Canada.

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CATALOG OF LICHENS, LICHENICOLES AND ALLIED FUNGI IN CALIFORNIA (second revision)

Shirley C. Tucker
Cheadle Center for Biodiversity, Department of Ecology, Evolution & Marine Biology, University of California, Santa Barbara, CA 93106-9610 USA;
Santa Barbara Botanic Garden, Santa Barbara, CA; and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803
tucker@lifesci.ucsb.edu

Type all or part of a lichen name into the search box.

ABSTRACT
This second revision of the California lichen catalog reports 1,869 taxa at species level and below (of which 58 are recognized at the level of variety, subspecies, or forma) for the state, an increase of about 295 taxa since 2006, and 565 taxa since the 1979 catalog. The number of genera is 340, an increase of 43 since 2006. The lichen flora of California includes about 35% of the 5,246 species and 52% of the 646 genera reported for the continental United States and Canada. All known references are given that cite each species as occurring in California. Synonyms are cross-referenced to the current names. Accepted names are listed first, followed by names of taxa that are either excluded or not confirmed. The bibliography includes 1158 publications pertaining to California lichens (citations through 2011, and some from 2012).
Key words: California; Flora; Lichens; Lichenicoles

The 34 years since publication of the first catalog of California lichens (Tucker & Jordan 1979) have seen enormous changes in accepted names of lichens, particularly an increase in generic names. The Tucker & Jordan catalog was originally based on literature records assembled by William A. Weber that were contributed to the cryptogamic herbarium at the University of California, Berkeley, CA, where they are deposited. Since then, California lichen material has been examined critically in many genera, resulting in recognition of many new taxa and necessitating many name changes. The need for a revised lichen checklist for California became markedly apparent, particularly because of an increased interest in lichen collecting in California. An online revised catalog was published in 2006 in Constancea. Now, seven years later, so many changes have occurred that it is considered best to publish the entire revised catalog. The catalog is intended to provide a current, comprehensive picture of the species known to occur in California. I consider it a working document that is subject to change. Although a catalog is never complete, the current version should be made easily available to lichenologists and collectors in California and elsewhere. The great geographic diversity in the state of California is responsible for the relatively large number of lichens found here.

The state includes 158,297 square miles (409,990 km ²) and extends from 32°32' to 42° north latitude. Climates vary greatly according to elevation and other factors. Yearly precipitation ranges from under 2 inches (5 cm) in the deserts to over 65 inches (165 cm) in the north coastal counties. Elevations range from 282 feet (86m) below sea level in Death Valley to 14,494 ft. (4,419 m) at the summit of Mt. Whitney. The state includes a wide range of habitats for lichens: deserts, sand dunes, mountain ranges, rain forests, montane forests, oak savanna, chaparral, and seacoast. The Mojave, Colorado, and Sonoran deserts are represented in the southern part. Mountain ranges include the Sierra Nevada along most of the eastern boundary, the coast ranges, and desert ranges. In the south, the San Gabriel, Santa Monica, Santa Ynez, Tehachapi, and other ranges have been explored for lichens since the 1870's. Yosemite National Park, in the central part of the Sierra Nevada, was one of the earliest sites collected by Bolander and others. Records from Tucker & Jordan (1979) are included for completeness for accepted names, and in some cases for synonyms or lists of references where useful.

The continuing literature search for state reports since 1979 was begun independently by the author and B.D. Ryan, and was eventually combined. Publications (1158) include monographs, lichen floras, field trip reports, and other articles, plus some unpublished theses and government reports. References from the 1979 publication are included that reported the species under its present name or some additional synonyms, or that represent scarce reports for a species. The references to specific collections include initials of the herbaria (Holmgren et al. 1990) where they are housed. If no herbarium is indicated, the collections are presumed to be held by the collector. Unfortunately, most large holdings of California lichen collections are located in institutions out of the state. A study of literature citations for the state shows how frequently a species has been collected, and thereby suggests the level of abundance or rarity.

The literature citations also provide a means of locating particular lichen collections for comparison, and for determining geographic locations where a species has been found. While distributions in California are not included in the catalog, some information on distribution can be gleaned from a review of the authors of papers cited.

Central and northern California collections have been reported by Baltzo, Bourell, Doell, Cooke, Hammer, Herre, Jordan, Jovan, Lindsay, Malachowski, McGee, E. Peterson, Pinelli, Robertson, Shevock, Sigal, D. Smith, Sweet, Tavares, Thiers, Toren, and Wright. Authors who collected primarily in southern California (or reported on southern collections, including the CA Channel Is.) include Bowler, Bratt, Eckfeldt, Hasse, Howe, Hue, Knudsen, McClatchie, Merrill, Moxley, Nash, Orcutt, Parish, and Zahlbruckner. Collectors who have collected and reported from throughout California include Arup, Bolander, Hale, Magney, Printzen, Riefner, Ryan, Sanders, Thomson, Timdal, Tucker, Weber, and Wetmore.

The total number of lichen taxa reported here for California is 1,868, compared to 999 (1060 including subspecific taxa) in the first catalog (Tucker & Jordan 1979) and 1,575 species in the 2006 version. The species number known has more than doubled since 1945, when Herre (1945) reported 794 species and varieties known in California. The lichen flora of California includes about 35% of the 5246 spp. in 646 genera in the Esslinger list, (version 17) species reported for the continental United States and Canada by Esslinger (2011). The number of genera represented in California has increased from 170 in 1979, to 339 in 2012, about 52% of the genera found in the United States and Canada.

I follow approximately the format used in the Esslinger list. Taxa are arranged alphabetically, with accepted taxa first (in boldface), followed by names in italics that are either synonyms, possible misidentifications, or names of taxa erroneously attributed to the state. Generic names are in caps the first time they occur. Some generic synonyms are included, if they have been cited for California. Synonymy is not intended to be comprehensive, but includes those names under which the taxa have been reported for California. The source for synonyms, if not given in the text, is usually Esslinger and Egan (1995) or Esslinger's online list (2011). For full citations of older names, Tucker & Jordan (1979) should be consulted. Names have been checked against the Esslinger (#17, posted 6 May 2011) online updated checklist for the continental United States and Canada (URL is given in References). [Authorities follow those in Esslinger (2011) except where discrepancies with Index Fungorum or Zahlbruckner's Catalogus Lichenum Universalis could not be resolved in Esslinger's favor.] For species having few or no published reports in California, collection data of verified representative collections from California are included.

Where a choice of several collections was available, I selected records that show the broadest geographic range within the state, or that have not been published previously. In some cases, I cite the opinions of experts about problematical reports of species. Some entries are reported based only on a report from a secondary source, such as Fink (1935), Tucker & Jordan (1979), Hale & Cole (1988), or Brodo et al. (2001). Because Tucker & Jordan is cited so frequently, it is referred to as "TJ" in the text.

Knowledge concerning lichenicolous fungi has increased greatly since the first lichen catalog for California was published. These are fungi that are either gall-forming or commensals, and live on other lichens (Hawksworth et al. 1995). 212 of the accepted taxa in this list are lichenicolous, saprophytic, or related fungi of uncertain status.

The identifications by specialists such as P. Diederich, D. Triebel, J. Kocourková, and K. Knudsen are responsible for 200 species in 82 genera reported in the current work, compared to seven species in five genera in 1979. Many more lichenicoles are likely to be found and identified for the state, as collectors become familiar with them. Much of California remains to be explored lichenologically. Most collectors have concentrated on coastal areas and around major centers of population. The profound influence of individual collectors can be seen in the work of two early collectors, Hermann E. Hasse (Los Angeles area, published 1895-1915), and Albert W. C. T. Herre (around Santa Cruz, published 1906-1963).

Of the lichens in early reports for California (primarily by Hasse or Herre), 86 species have not been collected for 100 years, since 1913; another 15 species have not been re-collected for over 75 years (since 1935); and another 27 have not been collected for over 60 years (since 1950). Encouraging evidence of renewed enthusiasm for collecting shows that 42 species have recently been re-collected by Kocourková & Knudsen that had not been collected for at least 50 years. 111 species of lichens currently appear to be endemic to California and are so labeled in the text. An additional 47 species are endemic to California plus Baja California, Mexico. Status as an endemic can change with an altered concept of a particular species or by discovery of the species outside the known geographic range. Some putative endemics await a detailed study of their genus; for example seven species of Arthonia are considered endemics, but their status may change when the genus undergoes a monographic study. Recently named taxa may appear endemic due to a lack of recognition by collectors as distinct species; an example is in the eight CA endemics in the genus Lecania, most described as new by Ryan & van den Boom (2004). Publications with descriptions of newly recognized species generally stimulate extension of the known range of such species. Many that were once considered endemic, such as Dirina catalinariae Hasse, Lecanora phryganitis Tuck., and Schizopelte californica Th. Fr., have been found in either Arizona or Mexico, due to the diligent collecting and systematic work of the Sonoran Desert Project headed by T. H. Nash (Nash, Ryan et al. 2002, 2004; Nash, Gries & Bungartz 2008). The lichens of California still present numerous problems in identification of numerous species, so that future changes are to be expected in the status of many taxa.

ACKNOWLEDGMENTS.
Eighteen years of work have gone into preparation of this catalog. Starting in 1995 when I moved back to California after my retirement, Bruce Ryan and I combined our individual lichen catalogs, and worked to update the earlier catalog by Tucker and Jordan (1979). The devastating death of Bruce Ryan on 23 January 2004 cut short the many years of collegial sharing of his first-hand knowledge of the California lichen flora. Since then, I have continued work on the catalogue, with the help of numerous friends. I want to thank several colleagues especially for their contributions. Bruce Ryan's discerning eyes and multitudinous collections were responsible for a major improvement in our understanding of the California lichen flora. Tom Nash at Arizona State University has been a major knowledgeable collector and student of the California flora. Not only has he collected in many parts of CA, but his many publications are major contributions to the state flora. His comprehensive project on the Sonoran Desert lichen flora has funded visits to CA and Arizona by numerous lichen specialists, and has resulted in publication of the results in three volumes of a major compendium on lichens of the Sonoran region including southern California (Vol. 1), edited by Nash, Ryan, Gries & Bungartz, 2002;
Vol. 2, edited by Nash, Ryan, Diederich, Gries & Bungartz, 2004;
Vol. 3, edited by T. H. Nash III, C. Gries & F. Bungartz, 2008.
Isabelle Tavares, outstanding mycologist and lichenologist at the University of California, Berkeley, is also especially commended for her contributions. Isabelle served as reviewer for the catalog after it was submitted to Constancea. She was a meticulous and severe critic, but the catalog would have far more errors had it not been for her sharp eyes reviewing every word. She spent most of a year on the review, sacrificing time she would prefer to have spent on her own research. Her dedication and high standards for the journal Constancea are a model to be admired. Unfortunately, Isabelle died recently, after a long illness that prevented her from completing some favorite longterm projects. The author also is grateful to Richard L. Moe, editor of Constancea, who has spent countless hours on the two versions of the online catalog. With his computer expertise, he has made it easy to use and vastly reduced the number of errors. His endless patience and tolerance have made the transition to electronic publication relatively painless, and a much appreciated learning experience for this author. The catalog has benefited from the cooperation of many individuals in preparation of this catalog. Specialists who have provided identifications and other expertise include
T. Ahti, A. Aptroot, D. Baltzo, O. Breuss, I. Brodo, W. Buck, B. Büdel, F. Bungartz, T. Carlberg, M. Cole, B. Coppins, P. Diederich, J. Doell, Egea & Torrente, S. Ekman, T. Esslinger, T. Feuerer, A. Fryday, S. Hammer, R. C. Harris, D. Hawksworth, S. Heidhmarsson, P. M. Jørgensen, K. Kalb, K. Knudsen, I. M. Lamb, J. Lendemer, L. Lindblom, T. Lumbsch, B. McCune, R. Moberg, T. Nash, E. Peterson, C. Printzen, R. Riefner, J. & R. Robertson, R. Rosentreter, B. Ryan, W. Sanders, R. Santesson M. Schultz, J. Sheard, L. Sparrius, B. Staiger, L. St. Clair, I. Tavares, J. W. Thomson, L. Tibell, E. Timdal, T. Tønsberg, D. Toren, D. Triebel, P. van den Boom, A. Vĕzda, W. Weber, C. Wetmore, and D. Wright. A major source of lichenological discovery in southern California has been Kerry Knudsen. He has re-collected mountain ranges and canyons in Hasse's footsteps, clarifying many of the Hasse reports from around 1900, as well as publishing over 100 publications on California lichens in the ten years since 2003.
I thank the following for assistance in arranging loans:
M. Bourell (CAS); P. Bowler (UCI); O. Breuss; D. Desjardin (SFSU); P. Diederich; D. Ferguson (LSU); L. Janeway (CSU Chico); P. M. Jørgensen; D. Keil (OBI); L. Lindblom; T. Lumbsch and R. Lücking (FM); B. McCune; R. Muller (SBBG), T. Nash and S. Standley (ASU); C. Printzen; M. Schultz; J. Sheard; S. Sillett; and M. Vincent (MU).

Abbreviations and symbols:
"TJ" =previously reported by references in the California lichen catalog by Tucker & Jordan (1979);
* =lichenicolous fungi;
† =saprophytes related to lichens or to lichenicolous fungi;
# =various related fungi of uncertain status.
Use of the latter three symbols follows usage in Esslinger & Egan (1995). Symbols for herbaria follow usage in Holmgren et al. (1990).
Other abbreviations include:
CA, California;
Cpgd, Campground;
Co., County;
Cyn, Canyon;
Hwy, Highway;
Isl., isls., Island(s);
mi., miles;
Mtn, Mts, mountain(s);
Nat., National;
N. F., National Forest;
N. P., National Park;
pr. p., pro parte;
Rd, Road;
S. P., State Park;
Syn., Synonym[s];
Univ., university;
also months and directions of the compass are abbreviated.

NOTES ON THE ELECTRONIC VERSION. Accepted names and synonyms are mutually linked. References pertinent to an entry may be retrieved by clicking on the folder icon ( ). Most names are linked to Index Fungorum ( ), where additional information about nomenclature and taxonomy may be found..

ACAROCONIUM Kocourk. & D. Hawksw.

ACOLIUM (Ach.) Gray

AHTIANA Goward

ALECTORIA Ach.
(Brodo & Hawksworth 1977; TJ; Brodo et al. 2001 [p. 152, with color photograph]; Carlberg 2003; McCune & Geiser 2009; Weber 1981 [Univ. Colo. Lich. Exs. 417])

(Howe 1911; Fink 1935; Herre 1945; Ahti & Henssen 1965; Lindsay 1973; Tucker 1973; Malachowski 1975; Brodo & Hawksworth 1977; Pinelli & Jordan 1978; TJ; McCune & Geiser 2009)

(Brodo & Hawksworth 1977; TJ; Goward 1999; Brodo et al. 2001 [p. 154]; Jovan & McCune 2004; Williams & Sillett 2007; McCune & Geiser 2009)

=Bryoria implexa (Motyka 1964; Jordan 1968)
Note: Baltzo (2002) suggested that Jordan's material might rather have been Bryoria capillaris, based on the reported C- chemical reaction and the absence of B. implexa from further south than Idaho in western U. S.; no correctly identified specimens of this species from CA are known to us.

(Malachowski 1975; Robertson 2002a; herbarium name for A. imshaugii, fide I. Brodo [personal communication])

(Hasse 1913b; Fink 1935)
Note: CA reports are based on misidentifications, although the species occurs in Oregon.

ALLARTHONIA (Nyl.) Zahlbr. =ARTHONIA
(Hasse 1913b) misidentifications for unidentified non-lichenized species of Arthonia

AMANDINEA M. Choisy ex Scheid. & H. Mayrhofer

ANAPTYCHIA Körb.
(Robertson & Robertson 2002 [based on J. & R. Robertson 5702, rocky headlands along Hwy 1, Mt. Tamalpais S. P., Marin Co., ! T. Esslinger])

(Knudsen & Kocourková 2012c; K. Knudsen s.n., San Jacinto Mts, Riverside Co., UCR)

(Herre 1910; Thomson & Ketchledge 1958; TJ; misidentifications for CA)

ANEMA Nyl. ex Forss.

ANISOMERIDIUM (Müll. Arg.) M. Choisy
(R. Harris 1975; TJ; von Reis 1991; Kocourková 2000; Aptroot 2002; Baltzo 2002; Tucker et al. 2004; Knudsen & Kocourková 2010a, citing Hasse collections)
Synonyms: Arthopyrenia biformis,A. parvula,Leiophloea parvula
Misapplied names: Arthopyrenia conformis (Herre 1910; Fink 1935),Trimmatothele umbellulariae (fide Lendemer & Knudsen [2007])
Note: A. biforme was considered synonymous with A. polypori by some authors (Hawksworth 1985, p. 157; Kocourková 2000, p. 142) but more recently they are considered distinct entities (Kocourková et al. 2008; Smith et al. 2009).

(Aptroot 2002; S. Tucker 34375 pr. p., Montecito, Santa Barbara Co., SBBG, det. A. Aptroot)

(von Reis 1991; misidentification for CA, fide Tucker [1999])

ANTHRACOTHECIUM Hampe ex A. Massal.

ARTHONIA Ach.
(Sundin 1999; Grube 2008; Knudsen & Kocourková 2010a, citing Hasse collections; Tucker 2010; S. Tucker 39051, Santa Barbara Co.;C. Bratt 12087, NE of Escondido, San Diego Co., SBBG)
Synonyms: A. crozalsiana,A. stictella
Misapplied names: Arthothelium anastomosans

(Sundin 1999; Grube 2008; Knudsen & Kocourková 2009b; Tucker 2010; Knudsen & Kocourková 2012a; S. Tucker 35661B, Santa Cruz Isl., Santa Barbara Co., SBBG)
Misapplied names: Arthonia orbillifera,A. pruinascens,A. taediosa,Arthothelium subcyrtodes,A. taediosum

(TJ; Brodo et al. 2001 [p. 164, with color photograph]; Tucker et al. 2004; Grube 2008 for northern central CA; Stone & Villella 2010)
Synonyms: A. gregaria,A. tumidula

(Diederich 2003 [as "s. str.", citing K. Knudsen 13706, Joshua Tree N. P. on Rhizoplaca chrysoleuca]; Grube 2008 [cites for Arizona and New Mexico on same]; Kocourková et al. 2012)

(Lendemer, Knudsen, & Coppins 2009; Knudsen & Kocourková 2010f, 2012a; Kocourková et al. 2012; Anacapa Isl., Ventura Co. on Diploicia canescens)

(Kocourková et al. 2009; Kocourková et al. 2012; on Physcia spp., esp. P. adscendens, San Diego Co.)

(Jordan 1968; TJ; Baltzo 2002)

(Diederich 2003; Grube 2008; Kocourková et al. 2012; S. Tucker 36515, 36516, San Simeon S. P., San Luis Obispo Co., on soralia of Ramalina, SBBG, det. P. Diederich)

(Grube 2008, from Santa Rosa Isl.; Knudsen & Kocourková 2012a)

(Sundin 1999; Grube 2008; Knudsen & Kocourková 2010a, citing Hasse collections)
Misapplied names: Arthonia epipastoides,A. leucopellaea,A. galactitella [possibly also A. galactites, similar but a European species],A. punctiformis.

(Tuckerman 1872, 1888; Willey 1873a, 1890; Orcutt 1903 [as "A. globosa"]; Zahlbruckner 1903-1907, p. 90; Orcutt 1907; Fink 1935; TJ; Grube 2008; Knudsen & Kocourková 2012a)

(Sundin 1999; Grube 2008; Knudsen & Kocourková 2010a, citing H. Hasse s.n., Santa Monica Mts, Los Angeles Co., on willow, ASU)

(Grube 2008, for Humboldt and Monterey counties; Williams & Sillett 2007; Tucker 2009a; S. Tucker 35259, Caspar Point, S of Fort Bragg;S. Tucker 35278, Pygmy Forest off Mitchell Creek Drive, 1.6 mi. S of Simpson Lane, near Fort Bragg, Mendocino Co., SBBG, ! B. Ryan)
Misapplied names: A. caudata,A. complanata,A. quintaria

(Egea & Torrente 1995b; Grube 2008, citing a Monterey Co. report; Knudsen & Kocourková 2009b, 2012a; Kocourková et al. 2012 [as juvenile parasite on Lecanographa];K. Knudsen 11207, Santa Monica Mts, Los Angeles Co., UCR; also known from Santa Rosa Isl.; CA endemic)

(Kocourková et al. 2008; K. Knudsen 9960, Limekiln S. P., Santa Lucia Mts, Monterey Co., UCR)

(Egea & Torrente 1995b; Grube 2008; Knudsen & Kocourková 2012a; K. Knudsen 11397, Santa Rosa Isl., Santa Barbara Co., UCR; CA endemic)

(Cole & Hawksworth 2001 [p. 312], based in part on C. Bratt 7864, on Caloplaca luteominia, San Nicolas Isl., Ventura Co., SBBG, det. M. Cole; Grube 2008, for San Nicolas Isl.; Knudsen & Kocourková 2012a; Kocourková et al. 2012;K. Knudsen 11708, San Jacinto Mts, Riverside Co.; also onXanthoria elegans and various Caloplaca species)

(Villella & Carlberg 2012, foliicolous on Sitka spruce & Evergreen huckleberry Vaccinium ovatum; also reported from Oregon and British Columbia.)

(Hafellner et al. 2002; on Phaeophyscia spp.; Knudsen & Kocourková 2012a, on Santa Cruz Isl.; Kocourková et al. 2012)

(Grube 2008; S. Tucker 38638, Pinnacles Nat. Monument, San Benito Co., SBBG [=type]; CA endemic)

(Grube 2008; Knudsen & Kocourková 2010a, citing Hasse collections; H. Hasse Exs. 51, Santa Monica Mts, Los Angeles Co., ASU; CA endemic)
Synonyms: Arthothelium pruinascens
Note: The type locality for this species is in the Santa Monica Range.

(Grube 2008; Tucker 2009a; Knudsen & Kocourková 2010a, citing Hasse collections; Knudsen & Kocourková 2010f; Stone & Villella 2010; Tucker 2010; Knudsen & Kocourková 2012a)
Synonyms: A. chiodectella,A. impolita,A. impolita var. chiodectonoides,A. impolita var. subfusca,A. pruinata,A. pruinosa
Misapplied names: A. gyalectoides,A. ochrolutea

(Zahlbruckner 1902; Hasse 1903b, 1903f, 1913b; Merrill 1923; Fink 1935; TJ; Sundin 1999; Grube 2008; Knudsen & Kocourková 2010a, citing Hasse collections; Tucker 2010; H. Hasse 27, Santa Monica Mts, Los Angeles Co., ASU, SBBG; CA endemic)
Synonyms: A. microspermella, fide Sundin (1999)

(Hasse 1897, 1913b; Fink 1935; TJ; Sundin 1999; Grube 2008, for S CA [Santa Monica]; Knudsen & Kocourková 2009b, 2012a; not endemic, also in Baja California)

(Sundin 1999; Grube 2008, for S CA)

(Hasse 1913b; Merrill 1923; Fink 1935; TJ; Bourell 2000; Sundin 1999; Grube 2008, for coastal southern and central CA and Baja California; Knudsen & Kocourková 2009b; Tucker 2009a, 2010)
Synonyms: A. dispersa var. tetramera,A. radiata f. angustata

(Kocourková 2009; Knudsen & Kocourková 2009b; Kocourková et al. 2012; J. Kocourková s.n., Santa Monica Mts, Los Angeles Co., on Xanthoparmelia mexicana, UCR)

(Williams & Sillett 2007, det. L. Sparrius in 2002, but keys to A. pinastri in Grube [2008] key for S. CA)

(Brodo et al. 2001 [p. 164, with color photograph and map which showed it around Los Angeles. A search for a specimen has not been successful]; Tucker 2002, repeated the Brodo et al. report)

(Herre 1944b)
Synonyms: A. obscura (synonymy fide Clauzade et al. [1981])
Note: According to Grube (2008), A. complanata is a tropical species that is similar to A. ilicina, although he noted differences. A. complanata, as reported by Herre and by Lindsay, was probably misapplied to A. ilicina in northern CA.

(Fink 1935; TJ)
Synonyms: A. dispersa var. cytisi (Hasse 1896, 1898a, 1903b; Orcutt 1903, 1907)
Note: This species was rejected by Grube (2008) for the Sonoran area on the basis that Hasse did not retain it in his 1913b flora. Grube (2008) discusses A. cytisii under A. subdispuncta.

(Willey 1890, p. 36; Hasse 1898a, 1913a; TJ; H. Hasse 852, on Malvastrum thurberi [=Malacothamnus fasciculatus], Santa Monica Range, Los Angeles Co., 1900, MIN)
Note: Grube (2008) indicates that identifications of A. diffusa from S CA are incorrect.

(Lindsay 1973)
Note: This is probably a misidentification.

(Hasse 1895; McClatchie 1897; Hasse 1898a, 1903b; Orcutt 1903, 1907; TJ; Bourell 2000 [as "cf."])
Note: Grube (2008) omitted this species from the Sonoran area, perhaps because Hasse did not retain it in his 1913b Flora.

(Orcutt 1885, 1903, 1907; TJ)
Note: This name is not in Zahlbruckner (1934) or Esslinger (2011). The taxon to which it refers is uncertain.

(Willey 1890; Hasse 1906, 1913b; Fink 1935; TJ) is a name misapplied to Arthonia glaucella, fide Grube 2008.

(Hasse 1898a; TJ)
Note: This name was rejected by Grube (2008) for Sonoran area on the basis that Hasse did not retain this species in his 1913b flora.

(Hasse 1903f, 1913b; Merrill 1923; Fink 1935; TJ; Bourell 2000; H. Hasse (! S. Tucker) on Heteromeles arbutifolia, Catalina Isl., 1902, Lichenes Exsiccati, Sullivant Moss Soc. 2470, MIN;B. Ryan 31270, Santa Rosa Isl., Santa Barbara Co., ASU;T. Tønsberg TT14742, Del Norte Co., BG, det. R. Sundin)
=A. pruinata, fide Grube 2008

(Tuckerman 1872; Willey 1873a, 1890; Hasse 1903f, 1913b; Merrill 1923; Fink 1935; Herre 1942c; Lindsay 1973; TJ; Doell 2002; Tucker et al. 2004; W. Weber, Univ. Colo. Lich. Exs. 192, Santa Catalina Isl. 477, Marin Co.)
=A. pruinata

(Williams & Sillett 2007, det. L. Sparrius in 2002, but keys to A. glaucella Nyl. in Grube [2008] key for S CA.)

(Hasse 1903f, 1913b; Fink 1935; TJ; Tucker et al. 2004) possibly =A. rhoidis

(Hasse 1896; McClatchie 1897; Hasse 1898a, 1903b; Orcutt 1903 [as "A. orbolifera"], 1907)
=name misapplied to Arthonia beccariana

Arthonia patellulata var. caesiocarpa Zahlbr.

(H. Hasse on Chrysoma pinifolia [=Ericameria pinifolia], near Playa del Rey, Los Angeles Co., 1900, Lichenes Exsiccati, Sullivant Moss Soc. 2071, MIN)
=name misapplied to Arthonia pinastri in depauperate condition, fide Grube 2008
Synonyms: Allarthonia patellulata var. caesiocarpa

(Hasse 1906; Fink 1935; TJ)
Note: Grube (2008) omitted this species from the Sonoran area, perhaps because Hasse did not retain it in his 1913b Flora.

(H. Hasse 700 on Tilia americana, Soldiers' Home, Los Angeles Co., 1899, MIN)
Synonyms: A. lurida (McClatchie 1897; Hasse 1898a; Fink 1935; TJ)
Note: This was rejected by Grube (2008) for the Sonoran area on the basis that Hasse did not retain this species in his 1913b flora.

(Hasse 1898a)
=name probably misapplied to Arthonia sanguinea

(Williams & Sillett 2007, det. L. Sparrius in 2002, but keys to A. pyrrhuliza in Grube [2008] key for S CA.)

(Hasse 1903f)
Synonyms: Arthothelium taediosum
=name misapplied to Arthonia beccariana, which has smaller spores than A. taediosa, fide Grube (2008)

(H. Thiers 23222, San Francisco watershed, San Mateo Co.;H. Thiers 32400, Santa Cruz Peninsula, Santa Cruz Co., SFSU;H. Thiers 1208, Bolinas Lagoon, Marin Co., SFSU)
=A. cinnabarina (synonymy fide Esslinger 2011)

ARTHOPYRENIA A. Massal.
(Herre 1910; Fink 1935; TJ; Aptroot 2002 [reported only collections from CA Channel Is.]; Tucker 2010)
Synonyms: A. fallax,Pyrenula fallax,Verrucaria epidermidis var. analepta,V. fallax
Note: Most early reports for N. Amer. were misidentifications for A. punctiformis, fide R. C. Harris (personal communication).

(Aptroot 2002; Tucker 1997, 1999; Tucker et al. 2004; Knudsen & Kocourková 2009a; Tucker 2010; Knudsen & Kocourková 2012a; S. Tucker 34374, Montecito, Santa Barbara Co., SBBG;S. Tucker 35974, Santa Cruz, Santa Cruz Co., SBBG)

(R. Harris 1975; TJ; Aptroot 2002; Knudsen & Kocourková 2009a, 2010a [citing a Hasse collection], 2012a)
Synonyms: Porina plumbaria,Verrucaria carpinea var. plumbaria,V. plumbaria
Misapplied names: A. cinereopruinosa (Herre 1910; Fink 1935; R. Harris 1975; TJ),Pyrenula herrei (Fink 1935; Herre 1942b)

(Herre 1910; Fink 1935)
=misidentifications for CA

(Herre 1910; Fink 1935; R. Harris 1975; TJ)
=misidentifications, probably of A. plumbaria for early CA reports

(Herre 1910; Fink 1935)
=misidentifications of Anisomeridium polypori for N. Amer.

(Herre 1942c; TJ)
=misidentifications, possibly of Collemopsidium sublitorale

(Herre 1912b; Hasse 1915a; Merrill 1923; Fink 1935; TJ)
=Acrocordia gemmata, but misidentifications for CA

ARTHRORHAPHIS Th. Fr.
(Kocourková et al. 2008; Knudsen & Kocourková 2012a; Kocourková et al. 2012; J. Kocourková s.n., Santa Rosa Isl., Santa Barbara Co., on Cladonia species, UCR)

ASPICILIA A. Massal.
(Owe-Larsson et al. (2008); B. Ryan 26279, Eagles Roost, San Gabriel Mts, Los Angeles Co., ASU; also San Bernardino and San Diego counties; CA endemic)

(Ryan & Nash 1991; Owe-Larsson et al. 2008; B. Ryan 12615a, Eastern Brook Lakes, Inyo Co., ASU)

(Rosentreter et al. 2007)

(Owe-Larsson et al. 2008 from LA, San Diego, Riverside Co.; K. Knudsen 385, Wildomar, Menifee Hills, Riverside Co., ASU)

(Owe-Larsson et al. 2008 [from Riverside, San Diego, Tulare, Tuolumne counties]; B. Owe-Larsson 9147, North Fork of San Jacinto River, San Jacinto Mts, Riverside Co., ASU)

(Rosentreter 1998; Sanders 1999b; Riefner & Rosentreter 2004; Benson 2005; Owe-Larsson et al. 2008; CA endemic)
Synonyms: Aspicilia sp. (Weber 1967a;W. Weber, Univ. Colo. Lich. Exs. 178, S of Ione, Amador Co., SBBG)
Note: A. tuckerae is an herbarium name applied to some herbarium specimens of this species by Ryan.

(Knudsen 2006c [host for lichenicole Lichenochora verrucicola]; Owe-Larsson et al. 2008; Knudsen et al. 2009; Rajakaruna et al. 2012, on serpentine, San Benito Co.; Weber 1989a [Univ. Colo. Lich. Exs.689, San Joaquin Experimental Range, Madera Co., ASU, as A. cf. epiglypta, re-identified as A. cuprea by Owe-Larsson])
Note: This species is common in the interior valleys and SW mountains, fide Owe-Larsson et al. 2008.

(Owe-Larsson et al. 2008; Knudsen et al. 2009; Stone & Villella 2010; CA endemic)
Note: This species has been found in Los Angeles, Riverside, San Diego, Santa Barbara and Tulare counties, according to Owe-Larsson et al. 2008.

(Owe-Larsson et al. 2008 reporting it from Kern, Riverside, and San Diego counties; Tucker 2010; CA endemic)

(Owe-Larsson et al. 2008; CA endemic)

(Owe-Larsson et al. 2008 reporting it from El Dorado, Inyo, Los Angeles, and Mono counties; Rajakaruna et al. 2012, on serpentine, San Benito Co.)

(Owe-Larsson et al. 2008 reporting it as common along the coast southward from San Francisco and Solano counties; Knudsen & Kocourková 2009c, 2010f; Benson & Hillyard 2012 [as "cf."]; Knudsen & Kocourková 2012a; CA endemic)

(Owe-Larsson et al. 2008 reports it as common in central and S CA; Knudsen et al. 2009; Knudsen & Kocourková 2009a, 2009c; Tucker 2010; Glacy et al. 2011; Knudsen & Kocourková 2012a; CA endemic)

(Rosentreter et al. 2007 [from extreme NE corner of CA])

(Owe-Larsson et al. 2008; B. Owe-Larsson 9100a, Sandstone Peak, Santa Monica Mts, Ventura Co., ASU; CA endemic)

(Owe-Larsson et al. 2008; Ryan & Nash 1991; B. Ryan 26602b, San Gabriel Wilderness, Los Angeles Co., ASU, SBBG;B. Ryan 25382b, Marble Mtn Wilderness, Siskiyou Co., ASU;T. Nash 23548b from El Dorado Co. bore this name misapplied to Pertusaria excludens, fide A. Fryday)
Misapplied names: A. mastrucata

(Owe-Larsson et al. 2008, citing collections from Riverside and San Benito counties)

(Owe-Larsson et al. 2008; B. Owe-Larsson 9167a, St. Rosa Mtn, Pinyon Flats, Riverside Co., ASU)

(Owe-Larsson et al. 2008, citing only Siskiyou Co. collection; B. Ryan 25388, trail through Big Meadows, edge of Marble Mtn Wilderness, Siskiyou Co., ASU)

(Hale & Cole 1988; Sigal 1989; Ryan & Nash 1991; Tucker & Bratt 1995; Hill 1997; Thomson 1997; McGee 1998 [as A. cf. caesiocinerea]; Bratt 1999; Baltzo 2002 [asA. cf. caesiocinerea ]; Robertson 2003b; Benson 2005; Owe-Larsson et al. 2008; Stone & Villella 2010; Tucker 2010)
=Circinaria caesiocinerea (Nordin et al. 2010)

(Baltzo 1989; von Reis 1991; Wright 1997)
Synonyms: Lecanora cinerea var. gibbosa,L. gibbosa (Hasse 1898a, 1908a; Herre 1910; Hasse 1913b; Fink 1935; Herre 1950a; TJ),L. gibbosula (Thomson & Ketchledge 1958 [as "cf.A. gibbosula"]; Baltzo 1970, as "synonymous withL. gibbosa Ach. sensu Herre"; TJ; Baltzo 1989),L. lusca f. lignicola
Note: This name has been misapplied to Aspicilia confusa and perhaps other species.

ATHELIA Pers.
(Knudsen & Kocourková 2010a; Kocourková et al. 2012; K. Knudsen 11821, Santa Monica Mts, Los Angeles Co., UCR, on Candelaria pacifica)
Note: This species is also found on Lepraria santamonicae.

BACIDIA De Not.
(Ekman 1996 [cited collections from Marin Co. and Humboldt counties])

(Herre 1944b; TJ; Ekman 1996 [cited collections from Humboldt, San Mateo, and Mendocino counties])

(Knudsen & Kocourková 2008b, based on K. Knudsen 7574, Santa Rosa Isl., UCR)

(Wetmore 1985 [based on C. Wetmore 50703, Sequoia N. P., junction of Crystal Cave Rd and General's Highway, Tulare Co., CA 11 May 1984, MIN])

(Ekman 1996 [cited collection from Trinity Co., CA])

(Ekman 1996, 2004; Tucker et al. 2004; Knudsen & Kramer 2007; Knudsen & Kocourková 2009a; Tucker 2010; Benson et al. 2012)
Note: This species occurs in coastal CA and Arizona.

(Knudsen & Kocourková 2012a; K. Knudsen 8878, Santa Rosa Isl., Santa Barbara Co., UCR;K. Knudsen collection, Joshua Tree N. P., Riverside Co., UCR)

(Ekman 1996; Baltzo 2002; Ekman 2004; Tucker et al. 2004; Robertson 2005b; Williams & Sillett 2007; Benson et al. 2012; Knudsen & Kocourková 2010a citing Hasse collections; Tucker 2010; Glacy et al. 2011; Knudsen & Kocourková 2012a; S. Tucker 37767, 37768 pr. p., Sugarloaf Ridge S. P., Sonoma Co., SBBG)

(Ekman 1996, 2004; S. Ekman L-620, Santa Ynez Mts, Santa Barbara Co., ASU; rare)

(Ekman 2004; Knudsen & Kocourková 2011; H. Hasse s.n., low elevation cyns, Santa Monica Mts, Los Angeles Co., ASU; CA endemic)

(Ekman 1996 [collection from Tulare Co.])

(Herre 1944b [based on C. L. Brown 2951, 1/2 mi. W of Larkspur, Marin Co., F]; TJ)
=misidentification of Cresponea chloroconia, fide S. Tucker

(Herre 1910; TJ)
=Lecanactis sp. (Ekman 1996)
Note: Herre made this combination slightly before Fink, who is usually credited with the name (fide I. Tavares, personal communication). Ekman (1996) said this is a corticolous species of Lecanactis, but did not indicate the species.

(Hasse 1913b; Thomson & Ketchledge 1958; Weber 1967a; W. Weber, Univ. Colo. Lich. Exs. 182, Big Sur, Monterey Co., SBBG; TJ)
=misidentification of Bacidina californica for CA reports

(Hasse 1908b; Fink 1935; Lindsay 1973; TJ)
=misidentifications for CA

(Hasse 1913a, 1913b; Merrill 1923)
=B. laurocerasi, but Hasse records (repeated by Merrill) are misidentifications of Bacidia coruscans fide S. Ekman (personal communication)

(Hasse 1913b; Herre 1944b; TJ)
=misidentifications for CA

Synonyms: Bilimbia granosa (Fink 1935),Lecidea granosa (Herre 1907)
Note: Ekman (1996, p. 130) denied that the species occurs in CA. The disposition of the collections reported by Herre and Fink is uncertain.

(Herre 1944b; TJ)
Note: According to Ekman (1996, p. 130) this is a misidentification; the species is European.

(Ekman 1996)
=misidentifications for CA, fide Ekman 2004

(Stone & Villella 2010)
=misidentifications for CA
Synonyms: B. atrogrisea Delise ex Hepp,Biatora atrogrisea
Misapplied names: B. endoleuca auct. (TJ; Baltzo 2002)
Note: According to Ekman (1996), B. laurocerasi is not in CA, and is likely to be confused with B. heterochroa, which does occur in CA. The reports by Baltzo and others should be checked.

(Herre 1944b; TJ)
=misidentifications for CA fide Ekman 1996

(Hasse 1913b; TJ)
=misidentifications for CA, fide Ekman 1996

(Brodo et al. 2001 [p. 172 with color photograph as "Bacidia" sabuletorum]; Tucker 2002 [repeated the Brodo citation])
=Bilimbia sabuletorum (synonymy fide Esslinger & Tucker 2009)

Bacidia schweinitzii (Fr. ex E. Michener) A. Schneid.

(TJ)
=misidentifications for CA fide Ekman 1996

BACIDINA Vĕzda
(Ekman 1996; Magney 1999; Baltzo 2002; Ekman 2004 [pp. 29-30]; Knudsen 2009; Tucker 2010; Knudsen & Kocourková 2012a; S. Tucker 37768, Sugarloaf Ridge S. P., Sonoma Co., SBBG; CA endemic)
Note: According to Ekman (1996), reports of Bacidia albescens (e.g., Weber 1967a; Ekman 1996, p. 127;W. Weber, Univ. Colo. Lich. Exs. 182) and B. phacodes (Ekman 1996, p. 133) in CA may refer to Bacidina californica.

(Ekman 2004)

(Ekman 2004 [based on a single collection from downtown San Diego])
Note: This species is common on bark in urban situations in Europe.

(Ekman 1996, 2004; S. Tucker 37843, Half Moon Bay, San Mateo Co., SBBG; Knudsen & Kocourková 2010a citing Hasse collections; Knudsen 2009; Stone & Villella 2010; Tucker 2010; Benson et al. 2012;S. Tucker 35778, Santa Cruz Isl., Santa Barbara Co., SBBG)

BACTROSPORA A. Massal.
(Egea et al. 2004; Knudsen & Kocourková 2012a)

(Egea et al. 2004; Knudsen & Kocourková 2012a; T. Nash 32436, Santa Cruz Isl., Santa Barbara Co., ASU)

(Egea et al. 2004; Knudsen & Kocourková 2012a; T. Nash 33095, 33097, 33110, Santa Rosa Isl., Santa Barbara Co., ASU; det. Egea & Torrente)

(Egea et al. 2004; Knudsen & Kocourková 2012a; S. Tucker 35777, Santa Cruz Isl., Santa Barbara Co., SBBG;B. Ryan 31147, Santa Rosa Isl., Santa Barbara Co., ASU, SBBG)

BAEOMYCES Pers.
(Thomson 1967; Sigal & Toren 1974; Tucker & Kowalski 1975; TJ; Thomson 1984; Hale & Cole 1988; Goward 1999; Brodo et al. 2001 [p. 174, with color photograph]; Hinds & Hinds 2007 [p. 128, color photograph only]; McCune & Geiser 2009; Glacy et al. 2011)

BAGLIETTOA A. Massal.

BIATORA Fr.
(Printzen 1995 [description but citations only from Europe]; Williams & Sillett 2007; T. Tønsberg TT28922, Mendocino Co., BG)

(Herre 1910; Fink 1935; TJ; Williams & Sillett 2007; Hertel et al. 2008; Benson et al. 2012; C. Printzen s.n., W of Whisky Ridge, Sierra N. F., Madera Co., ASU)
Synonyms: Biatora sylvana,Catillaria globulosa,Lecidea sylvana
Note: Printzen (2004) reported this species only from Arizona, but his collection from CA suggests presence in CA also.

(Printzen & Tønsberg 1999)

(T. Tønsberg TT28922 pr. p., Mendocino Co., BG)

(Tuckerman 1888; Hasse 1896; McClatchie 1897; Orcutt 1903, 1907; TJ; B. Ryan 24978, 20 Aug., 1989, Gold Flat SW of Scott's Bar, Klamath N. F., Siskiyou Co., ASU,B. Ryan 27080, Monterey Co., ASU)
Synonyms: Lecidea turgidula
Note: Early reports through those of Hasse are probably based on misidentifications.

(Tuckerman 1888)
=Lecanactis sp.
Note: Ekman (1996) said this is a corticolous species of Lecanactis, but did not indicate the species.

(Tuckerman 1888)
=misidentifications for CA

Synonyms: Lecidea meiocarpa (Stizenberger 1895; Hasse 1915a)
Note: This is an accepted species, known from high elevations in Arizona (Printzen 2004), but the old reports from CA are unlikely.

(Hasse 1906)
=Micarea punctella (Norman) Hedlund (synonymy fide Printzen 1995)
Note: This report is a probable misidentification by Hasse, because he did not repeat the name in his 1913b compilation.

(Brodo et al. 2001 [p. 176, with color photograph])
Synonyms: Lecidea vernalis,B. conglomerata
Note: According to C. Printzen (personal communication), this taxon is unlikely to occur in CA.

(Hasse 1903e [as "xanthococci"])
=Lecidea xanthococcoides
Note: Hasse 1903e referred to "xanthococci A. Zahlbr." and cited Zahlbruckner 1900, the place of publication of Lecidea xanthococcoides.

BIATORELLA De Not.
(Magnusson 1935a)
Note: This is a European species, not otherwise reported for N. Amer., so the report should be checked.

(Herre 1910; Hasse 1913b; Merrill 1923)
=Polysporina simplex
Note: Herre evidently grouped material of Sarcogyne spp. with reddish apothecia under this name; Hasse's (1913b) material isSarcogyne californica, at least in part, fide Magnusson (1935a).

BIATOROPSIS Räsänen
(Diederich 2003; Kocourková et al. 2012; S. Tucker 31755D, Armstrong Redwoods S. P., Sonoma Co., on Usnea pendulina, SBBG, det. P. Diederich;S. Tucker 31865B, Indian Valley Cpgd 10.7 mi. W of Downieville, Sierra Co., on Usnea cf. silesiaca, SBBG, det. P. Diederich)

BLASTENIA A. Massal. =CALOPLACA
(Hasse 1913b; Fink 1935)
=Caloplaca luteominia var. luteominia (synonymyfide Esslinger & Tucker 2009)

(Hasse 1913b) probably
=Caloplaca luteominia var. luteominia, fide Wetmore (2006)

BOTRYDINA Bréb. =LICHENOMPHALIA

BOTRYOLEPRARIA Canals, Her.-Mar., Gómez-Bolea & Llimona
(Kocourková et al. 2008)

BRYORIA Brodo & D. Hawksw.
(Brodo & Hawksworth 1977; TJ; Thomson 1984; Hale & Cole 1988; von Reis 1991; Wright 1997; Goward 1999; Brodo et al. 2001 [pp. 179-180, with color photograph]; Jovan & McCune 2004; Hinds & Hinds 2007 [p. 133, color photograph only]; McCune & Geiser 2009)

(Brodo & Hawksworth 1977; Pinelli & Jordan 1978; TJ; Sigal & Nash 1983; Tucker & Bratt 1995; Wright 1997; Goward 1999; Brodo et al. 2001 [p. 180, with color photograph]; Ryan 2002; Jovan & McCune 2004; Williams & Sillett 2007; Knudsen et al. 2009 [as "cf.", citing Segal & Nash (1983) and suggesting the species may be extinct in the Cuyamaca Mts of San Diego Co.]; McCune & Geiser 2009)
Synonyms: Alectoria fremontii,A. tortuosa,B. tortuosa

(Brodo & Hawksworth 1977; TJ; Smith 1980; Thomson 1984; Goward 1999; Brodo et al. 2001 [p. 181, with color photograph]; Ryan 2002; Blauman 2004a; Jovan & McCune 2004; Hinds & Hinds 2007 [p. 135, color photograph only]; Williams & Sillett 2007)

(Brodo & Hawksworth 1977; TJ; Sweet 1983; Thomson 1984; Hale & Cole 1988; Goward 1999; Brodo et al. 2001 [p. 182, with color photograph]; Ryan 2002; McCune & Geiser 2009)

(Brodo & Hawksworth 1977; TJ; Hale & Cole 1988; Riefner, Bowler, & Ryan 1995; Magney 1999; Baltzo 2002; Glavich 2003; Spribille & Hauck 2003; Geiser et al. 2004; Glavich et al. 2005a, 2005b; Glavich 2008a)

(Goward 1999; Jovan & McCune 2004; McCune & Geiser 2009)

(Brodo & Hawksworth 1977; TJ; Hale & Cole 1988; Riefner, Bowler, & Ryan 1995; Wright 1998; Magney 1999; Glavich 2003; Spribille & Hauck 2003; Geiser et al. 2004; Glavich et al. 2005a, 2005b; Glavich 2008b; McCune & Geiser 2009)

(Brodo & Hawksworth 1977; TJ; Goward 1999; Williams & Sillett 2007; McCune & Geiser 2009, in which range is S to Santa Cruz)

Synonyms: Alectoria bicolor (Hale 1969 [map])
Note: Hale's assertion that this species is in CA is incorrect; it occurs on the West Coast from Vancouver Isl. N to Alaska,fide Brodo & Hawksworth 1977.

BUELLIELLA Fink
(Esslinger & Egan 1995 [under Appendix, New records for N. Amer., p. 539, based on H. Hasse, Topanga Cyn, Santa Monica Mts, Los Angeles Co., UPS]; Alstrup & Cole 1998; Diederich 2003; Hafellner 2004; Knudsen & Kramer 2007; Tucker 2010; Kocourková et al. 2012;Rundel 3214, Hastings Natural History Reserve, Monterey Co., UPS;T. Nash 32836, Santa Rosa Isl., Santa Barbara Co., ASU; onPhaeophyscia spp.)

BYSSOLOMA Trevis.
(Tucker 2009a; Villella & Carlberg 2012, mentioned from Oregon, not from CA; S. Tucker 35280, Pygmy Forest, Mitchell Creek Drive near Fort Bragg, Mendocino Co., SBBG)

(Williams & Sillett 2007, foliicolous on redwood; Villella & Carlberg 2012)

(Villella & Carlberg 2012, mentioned from Oregon, not from CA)

CAERULEUM K. Knudsen & L. Arcadia (Arcadia & Knudsen 2012)
(Arcadia & Knudsen 2012)
Synonyms: Acarospora aeruginosa (synonymy fide Thomson 1997, p. 27),A. heppii,Myriospora heppii
Note: Range includes Los Angeles, Riverside, San Bernardino, and Santa Barbara counties.

CALICIUM Pers.
(Pinelli & Jordan 1978; TJ; Goward 1999; Rikkinen 2003; B. Ryan 24443, 5 km SW of Fraser Flat, Tuolumne Co., ASU)

(Goward 1999; Peterson & Rikkinen 1999; Rikkinen 2003; Peterson 2006 [known from only one location in CA, in Del Norte Co.])

(Pinelli & Jordan 1978; TJ; Tucker 1997; Wright 1998; Goward 1999; Bourell 2000; Rikkinen 2003; Tibell & Ryan 2004 [for S CA]; Williams & Sillett 2007; Knudsen & Kocourková 2012a)
Note: Collections are known from El Dorado, Marin, Riverside, San Luis Obispo, Santa Barbara, Sierra, Trinity counties, ASU, SBBG, UCR.

(Goward 1999; Robertson 2002a; Rikkinen 2003; Williams & Sillett 2007)

(Williams & Sillett 2007 [as "cf. lutescens"])

(Rikkinen 2003)

(Williams & Tibell 2008; Villella 2012)

CALVITIMELA Hafellner
(J. & R. Robertson 6886, on serpentine outcrop, Bolinas Fairfax Rd 0.3 mi. W of golf course, Mt. Tamalpais S. P., Marin Co., UC1975524)

Synonyms: Tephromela armeniaca (Ryan & Nash [1991], but report was based on a misdetermination)
Note: According to Brodo et al. (2001) and Hafellner et al. (2004), this species does not occur in CA.

CANDELARIA A. Massal.
(Westberg & Nash 2002 [as Candelaria "pacifica"]; Tucker et al. 2006; Knudsen 2007b; Knudsen & Kocourková 2009c; Tucker 2009a; Tucker 2010; Knudsen & Kocourková 2012a;C. Wetmore 73411, Santa Catalina Isl., Los Angeles Co., ASU;T. Nash 18927, E side of Pinnacles Nat. Monument, San Benito Co., ASU;S. Tucker 34684, Santa Margarita-Pozo Rd, San Luis Obispo Co., ASU)

(Pinelli & Jordan 1978; TJ; Hebert & Meyer 1984; Weber et al. 1987; Robertson 2002a; Benson 2005; T. Nash 11398, Mendocino Co., ASU)
=C. concolor (fide Lendemer & Westberg 2010)

(Thomson & Ketchledge 1958)
=error for Candelariella dispersa

(Hasse 1908b)
Note: This report is probably a misidentification, since Hasse did not repeat the report in his definitive 1913b paper.

CANDELARIELLA Müll. Arg.
(Fink 1935; TJ; Hale & Cole 1988; Tucker & Bratt 1995; Thomson 1997; Brodo et al. 2001 [p. 207, with color photograph]; Robertson 2003b; Westberg 2004; Benson 2005; Westberg 2005; Knudsen 2006a, 2007b; Westberg 2007c; Knudsen 2009; Knudsen et al. 2009; Knudsen & Kocourková 2009a, 2009c; Glacy et al. 2011; Knudsen & Kocourková 2012a; Rajakaruna et al. 2012, on serpentine, San Benito Co.)
Synonyms: C. cerinella,C. dispersa,Lecanora cerinella,L. vitellina var. aurella,Placodium epixanthum,P. vitellinum var. aurellum

(Westberg 2005, 2007a [Tulare Co., El Dorado Co.]; Westberg & Nash 2008; Tucker 2009a)
Note: This rare species has been collected also in Wyoming and Montana.

(Westberg 2005, 2007c [Sierra Nevada and Coast Ranges; Los Angeles Co., El Dorado Co., Mariposa Co.]; Westberg & Nash 2008; CA endemic)

(Knudsen 2006b [N of Hotspring Mtn, Cleveland N. F., San Diego Co.]; description in Westberg 2005, 2007b)
Note: This species has also been collected in Arizona and Texas.

(Westberg 2005, 2007b [Mendocino, San Diego, and Tulare counties])

(Westberg et al. 2011, from Fresno, Inyo, and Tuolumne counties)

(Westberg 2005, 2007b; Knudsen & Kocourková 2010a, citing Hasse collections; Tucker 2010; Knudsen & Kocourková 2012a)
Note: Collections are known from Ventura Co., San Luis Obispo Co., Santa Barbara Co., Kern Co., Los Angeles Co., Madera Co., Monterey Co., ASU, SBBG, UCR.

(Pinelli & Jordan 1978; TJ; Wetmore 1983; Hale & Cole 1988; Wright 1997; Bratt 1999; Doell et al. 1999; Brodo et al. 2001 [p. 208, with color photograph]; Knight et al. 2002; Robertson 2003b; Westberg 2004; Benson 2005; Westberg 2005; Carlberg et al. 2007; Knudsen 2007b; Westberg 2007c; Knudsen et al. 2009; Knudsen & Kocourková 2009c; Rajakaruna et al. 2012, on serpentine, San Benito Co.)

(Herre 1910; Hasse 1913b; Herre 1942a, 1945, 1950a; Volk 1963; Baltzo 1970; Pinelli & Jordan 1978; TJ; Weber et al. 1987; Hale & Cole 1988; Baltzo 1989; Sigal 1989; von Reis 1991; Tucker & Bratt 1995, 1996 [color photograph]; Riefner et al. 2003; Robertson 2003b; Tucker et al. 2004; Westberg 2004; Benson 2005; Westberg 2005, 2007b; Knudsen et al. 2009; Knudsen & Kocourková 2009c, 2010f; Tucker 2010; Knudsen & Kocourková 2012a; Rajakaruna et al. 2012, on serpentine, San Benito Co.)
Synonyms: Lecanora vitellina,Placodium vitellinum
Note: This species occurs from Siskiyou Co. in the north to San Diego Co. in the south.

(Lindsay 1973; TJ; Thomson 1997, 2003; Westberg 2004, 2005, 2007b; Knudsen 2009; Knudsen & Kocourková 2012a; K. Knudsen 15692, Carmel Mtn, San Diego Co., UCR;B. Ryan 12555, Eastern Brook Lakes watershed, Inyo Co., ASU;T. Nash 11237, Onyx Summit, San Bernardino Mts, San Bernardino Co., ASU;T. Nash 8001, S of Pinecrest, Tuolumne Co., ASU)
Note: This species is most common in southeastern U. S.

(Lendemer & Westberg 2010, cited Knudsen collection from San Bernardino Mts)

(Bratt 1999; Bourell 2000, cited J. Doell collection)
=misidentifications, as this is a European species

(Thomson & Ketchledge 1958 [as "Candelaria dispersa"]; TJ; Thomson 1997, 2003)
=Candelariella aurella, fide Westberg (2005)

(Ryan & Nash 1991; Brodo et al. 2001 [pp. 208-209, with color photograph]; Robertson 2003b, 2004; Westberg 2004; Benson 2005; Robertson & Beyer 2005; T. Nash 7056, Ocotillo Wells, San Diego Co., ASU;B. Ryan 31071, Santa Rosa Isl., Santa Barbara Co.;J. Shevock 17560, Kern Plateau, Tulare Co., ASU)
=C. citrina (Westberg 2004, 2005, 2007b)

Candelariella vitellina var. assericola Räsänen

CAPRONIA Sacc.
(Knudsen & Kocourková 2012c)

CARBACANTHOGRAPHIS Staiger & Kalb
Synonyms: Graphis saxorum
Note: Esslinger (2011) retains Graphis saxorum as a separate entity.

CARBONEA (Hertel) Hertel
(Knudsen & Kocourková 2009a, 2009c, 2012a; K. Knudsen 8573, Santa Cruz Isl., UCR)
Synonyms: Lecidea subplebeia Nyl., fide Index Fungorum

(Triebel et al. 1991; Diederich 2003; Robertson 2003b; Knoph et al. 2004; Kocourková et al. 2012; B. Ryan 12735, Eastern Brook Lakes watershed, Inyo Co., on Candelariella spp., ASU)

CATAPYRENIUM Flot.
(Thomson 1987; Sigal 1989; Goward et al. 1994; Ryan & Nash 1991 [whose report was based on a misidentification of C. daedaleum])
Synonyms: Dermatocarpon cinereum,D. hepaticum (Ach.) Th. Fr. s. str., non auct.,Endocarpon cinereum var. cartilagineum,E. hepaticum,E. tephroides
Note: Breuss & Bratt (2001) said it is not known with certainty from CA, but is likely to occur in the Sierra Nevada.

(Breuss & McCune 1994; Breuss & Bratt 2001; Brodo et al. 2001 [p. 571]; Robertson & Robertson 2001 [p. 64, based on their collections from Lake, Mendocino, Solano, and Sonoma counties, confirmed by O. Breuss]; Breuss 2002; Tucker 2002; Robertson 2004; Carlberg et al. 2007)

(Thomson 1987; Breuss & Bratt 2001; Breuss 2002; Robertson 2003b; Knudsen 2004c; Tucker et al. 2004; Knudsen 2006b, 2007b)
Synonyms: Dermatocarpon squamellum,Verrucaria squamella
Note: This very rare lichen may be extirpated from the Santa Monica Mts, which includes its type locality, fide Knudsen (2006b, 2007a).

=Placidium pilosellum (Breuss 1996)

(R. Rosentreter 7234, eastern end of High Peaks Trail, Pinnacles Nat. Monument, San Benito Co., SBBG; the name was misapplied toVerrucaria inficiens pr. p. [Breuss 1998])

=Placidium squamulosum

CATILLARIA A. Massal.
(Hasse 1913b; Fink 1935; TJ; Hertel et al. 2008; Knudsen & Kocourková 2012a, from Santa Rosa Isl.)

(Hasse 1909, 1913b; Fink 1935; Herre 1942c; Thomson & Ketchledge 1958; TJ; Hertel et al. 2008; Knudsen & Kocourková 2010a, citing a Hasse collection)

(Hasse 1913b; Fink 1935; Sigal 1975; TJ; Sigal 1989; Tucker & Bratt 1996; Riefner et al. 2003; Hertel et al. 2008; Knudsen & Kocourková 2009b; Knudsen & Kocourková 2012a)
Synonyms: C. lenticularis var. acrustacea,Lecidea lenticularis f. acrustacea

(Fink 1935, but erroneously based on a Mexican report of Heterothecium endochromum by Tuckerman)

(Herre 1910; Hasse 1913b; Fink 1935 [p. 219]; TJ; Knudsen 2005c; Hertel et al. 2008; L. Sigal, Land's End, San Francisco, San Francisco Co., 23 Mar 1973, ASU)
=Lecania franciscana
Note: Knudsen & Lendemer (2007a) transferred this species to Lecania, but the transfer has been challenged, fide T. Nash.

(Herre 1910; Fink 1935; misidentifications)
=Micarea subnigrata, a European species, not in N. Amer.

CATOCARPUS Hellb.

CATOLECHIA Flot.
Synonyms: Buellia pulchella (Hasse 1908b),Lecidea aliena var. pulchella Schrad. (Hasse 1898a)
Note: Hasse (1898a, 1908b) reports were not retained in Hasse's 1913b Flora, indicating he had changed his mind. The species is said to be arctic/alpine (Purvis et al. 1992) so would be highly unusual for the desert mountain ranges of southern CA.

CAVERNULARIA Degel. =HYPOGYMNIA (fide Miadlikowska et al. 2011)

CERCIDOSPORA Körb.
(Lendemer et al. 2008; Knudsen & Kocourková 2012a; Kocourková et al. 2012; J. Kocourková & K. Knudsen s.n., on Cladonia sp., S. Rosa Isl., Santa barbara Co., PRM, UCR)

(Navarro-Rosinés et al. 2004; Kocourková et al. 2012; K. Knudsen 5775, Rd to Eureka Peak, San Bernardino Co., UCR; onLobothallia spp.)

(Knudsen & Lendemer 2006a [on Xanthomendoza fallax, San Diego Co. and Xanthoria spp.]; Kocourková et al. 2012)

(Triebel et al. 1991 [based on B. Ryan 12510, Rock Creek Cyn, Mono Co., on Lecanora [subg. Placodium] sp., ASU])
=C. macrospora

CETRARIA Ach.
(TJ)
=Tuckermannopsis ciliaris, but CA reports may be misidentifications of T. orbata (fide B. Ryan)

=Tuckermannopsis chlorophylla
Note: Reports such as Jordan (1968) may be based at least partly on this soraliate species.

=Vulpicida viridis (Hale 1969 [erroneously indicated its presence in CA])
Note: Mattsson (1993) reported it only in eastern U. S. W to Arkansas.

CETRELIA W. L. Culb. & C. F. Culb.
(TJ; Ryan & Nash 2002, based on Hasse collections from southern CA; Hinds & Hinds 2007 [p. 150, color photograph only])
Synonyms: Parmelia olivaria,P. olivetorum
Note: This taxon is now probably extinct in CA.

CHAENOTHECA Th. Fr.
(Rikkinen 2003; Williams & Sillett 2007)

(Rikkinen 2003)

(Rikkinen 2003; Williams & Sillett 2007)

(Rikkinen 2003 [as "cf."])

(Rikkinen 1998 [for collections from Mendocino and Humboldt counties]; Rikkinen 2003 [added a collection from Del Norte Co.])

(Herre 1912a [based on A. Herre collection, on redwood post, Oakland hills, 525 ft. elev.;F. T. Bioletti, Sonoma Co., UC]; Tibell 1980; Goward 1999; Rikkinen 2003; Tibell & Ryan 2004)

(Williams & Sillett 2007)

(Tibell 1980; Goward 1999; Tibell & Ryan 2004; B. Ryan 32106, Brown's Creek, Sierra N. F., Madera Co., ASU)

(Jordan 1968; TJ; Tibell 1980; Goward 1999; Baltzo 2002 [repeated Jordan report]; Rikkinen 2003; Tibell & Ryan 2004; Williams & Sillett 2007; Doell et al. 2009; Glacy et al. 2011)

(Tibell 1980; Goward 1999; Rikkinen 2003; Tibell & Ryan 2004)

=C. chlorella (Wetmore 1985)

CHAENOTHECOPSIS Vain.
(Goward 1999; Peterson & Rikkinen 1999; Rikkinen 2003; Robertson 2003b)

(Rikkinen 2003; Kocourková et al. 2012; E. Peterson collections from Trinity Co., on Chaenotheca trichialis)

(Rikkinen 2003)

(Tibell 1981; Goward 1999; Peterson & Rikkinen 1999; Rikkinen 2003; Tibell & Ryan 2004; B. Ryan 22231, near county airport, Mendocino Co., ASU)

(Rikkinen 2003)

(Peterson & Rikkinen 1999; Rikkinen 2003 [as "cf." in latter])

(Goward 1999; Peterson & Rikkinen 1999; Rikkinen 2003)

(Peterson & Rikkinen 1999)

(Rikkinen 2003)

(Rikkinen 2003; Williams & Sillett 2007)

(Goward 1999; Peterson & Rikkinen 1999)
Note: The latter reference described this species as saprobic on wood in CA.

CHIODECTON Ach.
(Tuckerman 1888 [p. 135]; Hasse 1913b)
Synonyms: Llimonaea californica (Sparrius 2004)
=Schizopelte crustosa

CHLOREA Nyl.

=Letharia columbiana

CHROMATOCHLAMYS Trevis.

CHRYSOTHRIX Mont.
(Tønsberg [2004] reported it as common from Mexico to British Columbia; Knudsen 2009; Knudsen & Kocourková 2009a, 2010f; Tucker 2010; Knudsen & Kocourková 2012a; K. Knudsen 4603, Morro Bay S. P., San Luis Obispo Co.)

(Benson 2005)
Synonyms: Lepraria chlorina (Hale & Cole 1988 [but probably an error forC. xanthina or C. granulosa])
Note: This species was not mentioned for the Sonoran region by Tønsberg (2004).

CIRCINARIA Link (Nordin et al. 2010)
(K. Knudsen collection, Joshua Tree N. P.)
Misapplied names: Aspicilia desertorum (fide Knudsen, personal communication)

(Nordin et al. 2010, for name change; CA not mentioned)
Synonyms: Aspicilia contorta,Lecanora contorta,L. calcarea var. contorta
Note: According to Owe-Larsson et al. (2008), at least part of Hasse's material (Hasse 1898a, 1903e) that he calledLecanora calcarea is Aspicilia contorta (Circinaria contorta).

CLADINA Nyl. =CLADONIA (Ahti & DePriest 2001)
(Wright 1992 [identified only to genus]; Tucker & Ryan 2006, based on D. Wright 3079, coast near Dillon Beach, Marin Co., SFSU, det. T. Ahti)
=Cladonia arbuscula subsp. beringiana

Synonyms: Aspicilia calcarea,Lecanora calcarea

(Wright 1992 [identified only to genus]; Goward 1999, based on D. Wright 3007, coast near Dillon Beach, Marin Co. collection, SFSU, det. J. Thomson; Tucker & Ryan 2006; T. Ahti identified it asC. arbuscula subsp. beringiana)
=Cladonia ciliata var. ciliata

(Lindsay 1973; TJ; name misapplied to CA collections of Cladonia portentosa; synonymyfide Ahti [1984])

(Herre 1945; Lindsay 1973; name misapplied to CA collections of Cladonia portentosa)

CLAUZADEA Hafellner & Bellem.
(Kocourková et al. 2008)
Synonyms: Lecidea fuscorubens (Herre 1944b, but Herre misapplied this name to a collection [C. L. Brown 153, 4 mi. NW of Mill Valley, Marin Co., F] of Porpidia thomsonii)

CLIOSTOMUM Fr.
(Tønsberg 1998; T. Tønsberg 14807, E of Lord-Ellis summit, Del Norte Co.)

(Gowan 1990; Bourell 2000; Brodo et al. 2001 [p. 279, with color photograph]; Baltzo 2002; Tucker 2002; Ekman 2004; Tucker et al. 2004; Williams & Sillett 2007; Knudsen 2009; Knudsen & Kocourková 2009b, 2010f; Tucker 2010; Glacy et al. 2011; Benson et al. 2012; Knudsen & Kocourková 2012a)
Synonyms: Biatora mixta,B. mixta var. pacifica,Catillaria griffithii
Misapplied names: C. tricolor (Hasse 1913b; Herre 1910)Lecidea tricolor (Hasse 1898a)

CLYPEOCOCCUM D. Hawksw.
(Etayo et al. 2007, based on K. Knudsen 8297, on Hypocenomyce scalaris, San Jacinto Mts, Riverside Co., UCR; Glacy et al. 2011; Kocourková et al. 2012)

COCCOTREMA Müll. Arg.

COELOCAULON Link

COLLEMA F. H. Wigg.
(Nylander 1900; Wetmore 1985, based on C. Wetmore 50485, Sequoia N. P., Tulare Co., MIN; Brodo et al. 2001 ["widely distributed"]; Hinds & Hinds 2007 [p. 222, color photograph only])

(Hasse 1903c; Herre 1912b; Degelius 1954, 1974; TJ; Goward et al. 1994; Wright 1997 [as "cf."]; Doell et al. 1999; Brodo et al. 2001; Knight et al. 2002; Schultz et al. 2004; Knudsen 2007b; McCune & Geiser 2009; Knudsen & Kocourková 2010f, 2012a)
Synonyms: C. cheileum,C. cheileum f. monocarpum

(Degelius 1974; TJ)

(Schultz et al. 2004; Brodo et al. 2001 [pp. 284-285, color photograph but no CA record]; Knudsen 2009; Knudsen & Kocourková 2012a; K. Knudsen 6940, San Miguel Isl., UCR;T. Nash 32887, Santa Rosa Isl., Santa Barbara Co., ASU)

(Jordan 1968; Baltzo 1970; Lindsay 1973; Degelius 1974; Tucker & Kowalski 1975; TJ; Hale & Cole 1988; Baltzo 1989; von Reis 1991; McGee 1995; Doell & Wright 1996; Tucker & Bratt 1996; Wright 1997; Bourell 2000; Brodo et al. 2001 [p. 285, with color photograph]; McGee 2001; Baltzo 2002; Robertson 2003a; Jovan & McCune 2004; Schultz et al. 2004; Tucker et al. 2004; Benson 2005; Hinds & Hinds 2007 [p. 224, color photograph only]; Knudsen 2007b; Knudsen et al. 2009; McCune & Geiser 2009; Schultz 2009; Tucker 2010; Glacy et al. 2011; Knudsen & Kocourková 2012a; Rajakaruna et al. 2012, on serpentine, San Benito Co.)

(Degelius 1974 [p. 181]; TJ)

(Stone & McCune 2010, from Trinity Co.; Clark 2011)

(Degelius 1974; TJ; Knudsen & Kocourková 2010a, citing a Hasse collection; H. Hasse Exs. 183, 638, Santa Monica Mts, Los Angeles Co., ASU;C. Bratt 3175, Los Osos, San Luis Obispo Co., SBBG)

(Schultz et al. 2004; B. Ryan 21930a, N of Baywood Park, San Luis Obispo Co., ASU, det. M. Schultz)

(TJ; Weber et al. 1987; H. Hasse Exs. 829, Santa Monica Mts, Los Angeles Co., ASU)
Synonyms: Synechoblastus laciniatus
Note: CA is not included in the distribution of this species by Schultz et al. (2004) who did not comment on the Riverside Co. record of Weber et al. or the Hasse collection.

(Hasse 1913b)
=C. leucocarpum Hook. f. & Taylor, but misidentifications for N. Amer.

(Hasse 1903c, as "leucopipta")
=C. pulchellum var. leucopeplum

(Degelius 1974; not in CA fide Brodo et al. 2001 [p. 286]; discussed in Tucker [2002])

(Hasse 1903c; misidentifications for N. Amer., according to Degelius 1954)

COLLEMODIUM Nyl.

COLLEMOPSIS Trevis.
(Hasse 1906; misidentifications of Psorotichia hassei)

(Hasse 1898a; Orcutt 1909)
=Psorotichia segregata
Note: According to Schultz (2004, p. 321), the name Collemopsis segregata Nyl. was misapplied by Hasse to specimens of Lempholemma chalazanum (H. Hasse Exs. 892).

CORNICULARIA (Schreb.) Hoffm.
(Sigal & Toren 1974; TJ; Goward 1999; Brodo et al. 2001 [p. 289, with color photograph]; Carlberg 2003 [based on T. Carlberg 633, Broken Rib Mtn Botanical Area, Six Rivers N. F., Del Norte Co.]; McCune & Geiser 2009)

CORNUTISPORA Piroz

CROCYNIA (Ach.) A. Massal.
(Plitt 1923; TJ; E. Moxley s.n., Griffith Park, Mt. Hollywood, Los Angeles, Los Angeles Co., ASU)
=Septobasidium sp., a non-lichenized fungus

CYPHELIUM Ach.
(Weber 1967b; TJ; Riefner, Bowler, & Ryan 1995 [Orange Co.]; Magney [1999] and Knudsen & Magney [2006] repeated earlier report; Tibell & Ryan 2004; Knudsen 2007b; Knudsen & Kocourková 2012a; B. Ryan 31272, Santa Rosa Isl., Santa Barbara Co., ASU)

(Rikkinen 2003; B. Ryan 25192, Marble Mtn Wilderness, Siskiyou Co., ASU;B. Ryan 11311b, 1 km W of Lassen Volcanic N. P., Shasta Co., ASU)

(Tucker & Bratt 1996 [based on B. Ryan 27084, Monterey Co., ASU]; Tibell & Ryan 2004;B. Ryan 23422, Desolation Wilderness, El Dorado Co., ASU; Brodo et al. 2001 [pp. 292-293, color photograph but no CA report])

(Tibell 1978a; Brodo et al. 2001 [p. 292]; Tibell & Ryan 2004; L. Tibell 7768, San Jacinto Mts, Riverside Co., ASU, SBBG)

CYSTOBASIDIUM (Lagerh.) Neuhoff
(Diederich 2003, 2004; Kocourková et al. 2012; S. Tucker 35479, Soda Springs Ranger Station, near Pillsbury Lake, Lake Co., on Hypogymnia imshaugii,S. Tucker 31841, Indian Valley Cpgd 10.7 mi. W of Downieville, Tahoe N. F., Sierra Co. on Hypogymnia imshaugii, both SBBG, dets. P. Diederich)

(Diederich 2003, 2004 [Mendocino Co. collection on Usnea]; Kocourková et al. 2012;E. Palmer, 1888, San Diego Co., on Usnea sp., SBBG, det. P. Diederich;S. Tucker 28938b, Point Reyes, Sonoma Co., SBBG)

DACTYLOSPORA Körb.
(Tuckerman 1866, p. 26, citing specimen collected by Bolander probably near San Diego, fide Hafellner [2004]; Weber et al. 1987 [asLeciographa parasitica]; Kocourková et al. 2012;K. Knudsen 2734, Palomar Mtn, San Diego Co., UCR)
Synonyms: Buellia parasitica
Misapplied names: Leciographa parasitica (records from bark)
Note: The usual hosts are Pertusaria and Ochrolechia.

Synonyms: Buellia inquilina (Willey 1873a; Hasse 1912, 1915b)
Note: This report needs re-evaluation, as it was reported (H. Hasse, Eden Hot Springs on Lecanora muralis, the wrong host, rather than L. saxicola).

"DENDRISCOCAULON" Nyl.
Note: According to Tønsberg & Goward (2001) the type specimen of D. umhausense, the type of the generic name Dendriscocaulon, is representative of cephalodia of Lobaria. Therefore, D. umhausense is a taxonomic synonym of Lobaria amplissima. The disposition of other species of Dendriscocaulon is uncertain. Tønsberg & Goward (2001) and Jovan & McCune (2004) reported CA records under Dendriscaulon sp.

DENDROGRAPHA Darb.
(Brodo et al. 2001 [p. 297]; Tehler 2002; W. Weber L-42837, San Clemente Isl., Los Angeles Co., ASU)

(Sundin & Tehler 1996; Lohtander et al. 1998; Tehler 2002 [p. 166]; Knudsen & Kocourková 2012a; CA endemic)

(Ertz & Tehler 2011; T. Nash 40721, Patrick's Point S. P., Humboldt Co., ASU;W. Weber s.n., Seventeen-Mile-Drive, Monterey Co., ASU;K. Knudsen 7749, Santa Rosa Isl., Santa Barbara Co., UCR)
Synonyms: Chiodecton subochroleucum,Dirina franciscana,Roccellina franciscana,Schismatomma cupressum

(Darbishire 1895, 1898; Hasse 1898a; Hasse 1903a, 1903d; Zahlbruckner 1903-1907; Hasse 1913b; Merrill 1923; Darbishire 1935; Fink 1935; Herre 1945; TJ; Riefner, Bowler, & Ryan 1995; Bowler et al. 1996; Lohtander et al. 1998; Brodo et al. 2001 [p. 297, with color photograph]; Tehler 2002; Knudsen 2009; Knudsen & Kocourková 2009a, 2010f, 2012a; Glacy et al. 2011)
Synonyms: D. minor,D. leucophaea f. leucophaea,D. leucophaea f. minor,Roccella leucophaea,R. leucophaea var. minor Misapplied name:Roccella babingtonii (von Reis 1991,fide Tucker 1999)

(TJ; West & Doell 1995; Robertson & Robertson 2001)
=D. leucophaea
Note: Many reports are based on D. alectoroides f. parva; Herre's reports of fertile material are based onD. leucophaea [Tuck.] Darb. f. leucophaea or D. alectoroides f. alectoroides, since f. minor and f. parva are sterile.

DERMATOCARPON Eschw.
(Doell et al. 1999 [as "cf."]; Heidhmarsson 2000; Heidhmarsson & Breuss 2004; Knudsen 2006a, 2007b; Knudsen et al. 2009; Knudsen & Kocourková 2009c, 2012a; C. Wetmore 73929, Old Ranch Cyn, Santa Rosa Isl., Santa Barbara Co., [det. S. Heidhmarsson, MIN]; see alsoD. miniatum)

(Amtoft et al. 2008 for description, CA not mentioned; Tucker 14860A, 6 mi. N of Oroville, Butte Co., SBBG;

(C. Wetmore 50149, 50797, Sequoia N. P., Tulare Co., MIN;L. Janeway 10070 & Castro, Sierra Nevada, Tuolumne Co., SBBG)

(Heidhmarsson & Breuss 2004; Tucker et al. 2006; Knudsen & Kocourková 2012a; Rajakaruna et al. 2012, on serpentine, San Benito Co.; W. Weber L-42878, San Clemente Isl., Los Angeles Co., ASU)

(Breuss & McCune 1994)
Note: This species has also been collected in Oregon.

(Brodo et al. 2001 [pp. 297-298, with color photograph]; Tucker 2002; Robertson 2004; Hinds & Hinds 2007 [p. 236, color photograph only]; B. Ryan 24666a, end of Clark Fork Rd, edge of Carson-Iceberg Wilderness, Alpine Co., ASU; Butte and Siskiyou county collections also)
Synonyms: D. aquaticum,D. fluviatile,D. weberi

(Amtoft et al. 2008 for description, CA not mentioned; C. Bratt 4755, railroad grade entrance to Central Camp, Madera Co., SBBG;S. Tucker 36299, on Kelbaker Rd, 13 mi. E of Baker, San Bernardino Co., SBBG)

(Baltzo 1970; Tucker & Kowalski 1975; TJ; Hale & Cole 1988; Baltzo 1989; Doell et al. 1999; Brodo et al. 2001 [p. 299, with color photograph]; Heidhmarsson & Breuss 2004; Benson 2005; Robertson & Beyer 2005; Villella 2010; Rajakaruna et al. 2012, on serpentine, San Benito Co.)

(Ryan & Nash 1991; B. Ryan 12611a, 12617a, Eastern Brook Lakes watershed, Inyo Co., ASU;J. Shevock 17571, Kern Plateau, Tulare Co., ASU)

(Heidhmarsson & Breuss 2004; S. Parish 3527, San Bernardino Co., ASU)

(B. Ryan 30982, Middle Cyn, Santa Catalina Isl., Los Angeles Co., ASU;J. Marsh 6961, Prisoner's Harbor, Santa Cruz Isl., Santa Barbara Co., ASU; previously reported only from Arizona [Heidhmarsson & Breuss 2004])

(Knight et al. 2002)
Note: This species has previously been reported from inland western states (Colorado, New Mexico) and Mexico.

(Thomson 1984; Weber et al. 1987; Sigal 1989; misidentifications of Clavascidium spp., especially C. lacinulatum)

(Tuckerman 1866; Bolander 1870; Herre 1906; Hasse 1908b; Herre 1910; Hasse 1913b; Merrill 1923; Imshaug 1957; Baltzo 1970; Pinelli & Jordan 1978; TJ; Baltzo 1989; Ryan & Nash 1991; von Reis 1991; Tucker & Bratt 1995; Bowler et al. 1996; Wright 1997; McGee 1998; Robertson et al. 1998; Brodo et al. 2001 [pp. 298-299, with color photograph]; Baltzo 2002; Knight et al. 2002; Robertson 2003a, 2003b; Blauman 2004a; Benson 2005; Robertson 2005c; Robertson & Beyer 2005; Carlberg et al. 2007; Hinds & Hinds 2007 [p. 237, color photograph only]; Villella 2010; Glacy et al. 2011)
Synonyms: Dermatocarpon miniatum var. complicatum,Endocarpon miniatum
Note: D. miniatium is still commonly accepted; the opinion of Heidhmarsson (2000) that most collections labeled D. miniatum from N. Amer. are D. americanum, is controversial.

DESMAZIERIA Mont.

DIMELAENA Norman
(Sheard & Mayrhofer 1984; Mayrhofer & Sheard 2004; Knudsen 2009; Knudsen & Kocourková 2009b, 2012a; T. Nash 32580, Santa Cruz Isl., Santa Barbara Co., ASU)

DIRINA Fr.
(TJ; Brodo et al. 2001 [p. 305, with color photograph]; Tehler 2002; Knudsen 2009; Knudsen & Kocourková 2010f, 2012a; W. Weber L-42620, San Clemente Isl., Los Angeles Co., ASU)
Synonyms: D. catalinariae f. catalinariae,D. catalinariae f. sorediata

(C. Bratt 11791, between Emerald Bay and Parsons Landing, W end of Santa Catalina Isl., Los Angeles Co., SBBG;S. Tucker 35261, Cabrillo Drive, Caspar Point, S of Fort Bragg, Mendocino Co., SBBG)

DIRINARIA (Tuck.) Clem.
(Kalb 2004; B. Ryan 21988b, San Bruno Mtn, San Mateo Co., on rock, ASU;S. Chaney L-1463b, San Miguel Isl., Santa Barbara Co., SBBG)

Dirinaria aegialita (Afzel. ex Ach.) B. J. Moore

(C. Bratt 9151, West Anacapa Isl., western end of island, between Rat Rock and cpgd, Ventura Co., SBBG =probable misdetermination)

Dirinaria picta (Sw.) Schaer. ex Clem.

(Riefner, Bowler, & Ryan 1995; R. Riefner collections from Sonoma, Ventura, and San Luis Obispo counties; misidentifications. which have been identified by S. Tucker asPhyscia poncinsii [Riefner 88-78] and Trapeliopsis steppica [Riefner 92-190, 92-408])
Note: R. Riefner collections from Sonoma, Ventura, and San Luis Obispo counties have been identified by S. Tucker as Physcia poncinsii (Riefner 88-78) and Trapeliopsis steppica (Riefner 92-190, 92-408).

DUFOUREA Ach.
(Fink 1935)
=Dactylina madreporiformis
Note: Fink report for CA was an error, being based on a Tuckerman (1866) report of Dactylina madreporiformis from the Rocky Mountains; the species is not known in CA.

ECHINODISCUS Etayo & Diederich

ECHINOTHECIUM Zopf (accepted in 2011 Esslinger list)

EDRUDIA W. P. Jord.
(Jordan 1980; Hale & Cole 1988 [p. 8]; Wright 2000; H. Thiers 15228, Farallon Is., San Francisco Co., ASU; CA endemic)
Synonyms: Caloplaca constipans,Lecanora constipans,Placodium constipans,Polycauliona constipans

ENDOCARPISCUM Nyl.

ENDOCARPON Hedw.
(Breuss 2002; Knudsen 2007b; Knudsen & Kocourková 2009c, 2012a; S. Tucker 37922, Jasper Ridge, W of Palo Alto, San Mateo Co., SBBG;K. Knudsen 6128, Weir Cyn, Santa Ana Mts, Orange Co., UCR)

(Hasse 1915b; Fink 1935; TJ; Breuss 2002; Tucker 2010; Knudsen & Kocourková 2012a; C. Bratt 8498, Santa Rosa Isl., Santa Barbara Co., ASU, SBBG)

(Knudsen 2005c, 2007b; C. Bratt 5217, Santa Barbara Isl., Santa Barbara Co., SBBG;K. Knudsen 617, Santa Monica Mts, Los Angeles Co., UCR)

(Orcutt 1885, 1903, 1907; Herre 1910; Hasse 1913b; Fink 1935; TJ; Hebert & Meyer 1984; von Reis 1991; Bratt 1993; Goward et al. 1994; Bowler et al. 1996; McGee 1998; Doell et al. 1999; Brodo et al. 2001 [pp. 308-309, with color photograph]; Robertson 2001; Baltzo 2002; Breuss 2002; Doell 2002; Knight et al. 2002; Robertson 2004; Tucker et al. 2004; Benson 2005; Robertson 2005c; Carlberg et al. 2007; Hinds & Hinds 2007 [p. 241, color photograph only]; Knudsen 2007b; Rosentreter et al. 2007 [with photograph]; Knudsen 2009; Knudsen & Kocourková 2009a, 2009c, 2010f; Tucker 2010; Knudsen & Kocourková 2012a; B. Ryan 31599b, Santa Cruz Isl., Santa Barbara Co., ASU, det. O. Breuss;T. Nash 8457, SW of Parker Dam on Colorado River, San Bernardino Co., ASU, det. O. Breuss)
Synonyms: E. adnatum,E. lepidallum,E. subnitescens

(Breuss 2002; Knudsen & Kocourková 2012a; T. Nash 32426, terraces NE of Fraser Point, Santa Cruz Isl., Santa Barbara Co., ASU)

ENTEROGRAPHA Fée
(W. Weber L-1306, Monterey Co., as E. pallidella)

(Villella & Carlberg 2012)
Note: This species is foliicolous on the fern Polystichum munitum, on Vaccinium ovatum, Picea sitchensis and Abies grandis.

EPHEBE Fr.
(Goward 1999; J. Shevock 14256, Western Divide Hwy., Co. Rd M-107, Tulare Co., CAS, UC, det. B. Ryan)

ERIODERMA Fée
(Ellyson & Sillett 2003; B. Ellyson LU-40-II-1, Prairie Creek Redwoods S. P., Humboldt Co., HSU, reported by Wright [2001a])

ESSLINGERIANA Hale & M. J. Lai

EUOPSIS Nyl.
Synonyms: Pyrenopsis pulvinata (Sigal 1975, 1989)
Note: The L. Sigal collection (Little Red Mtn, Mendocino Co., 13 June 1973, SFSU) was misdetermined.

EVERNIA Ach.
(Bolander 1870; Orcutt 1885; Hasse 1895, 1897; McClatchie 1897; Hasse 1898a, 1903a; Herre 1906, 1907; Orcutt 1907; Herre 1910; Hasse 1913b; Merrill 1923; Herre 1945, 1950a; Thomson & Ketchledge 1958; Jordan 1968; Lindsay 1973; Pinelli & Jordan 1978; TJ; Sigal & Nash 1983; Weber et al. 1987; Baltzo 1989; von Reis 1991; Riefner, Bowler, & Ryan 1995; Tucker & Bratt 1995; Bowler et al. 1996; Doell & Wright 1996; Tucker & Bratt 1996; Hill 1997; Wright 1997; McGee 1998; Goward 1999; Bourell 2000; Brodo et al. 2001 [pp. 312-313, with color photograph]; Robertson 2001; Baltzo 2002; Ryan 2002; Robertson 2003a; Blauman 2004a; Jovan & McCune 2004; Tucker et al. 2004; Benson 2005; Robertson 2005a, 2005b; Carlberg et al. 2007; Knudsen 2007b; Williams & Sillett 2007; Knudsen 2009; Tucker 2010; Rotter 2010; Villella 2010; Glacy et al. 2011; Benson et al. 2012; Knudsen & Kocourková 2012a)

(Howe 1911; Fink 1935; but misidentifications for CA)

(Tuckerman 1866; Bolander 1870; Hasse 1895, Herre 1906, 1907)
=Letharia vulpina

FLAVOPARMELIA Hale
(Nash & Elix 2002; Hinds & Hinds 2007 [p. 250, color photograph only]; Knudsen & Kocourková 2009c, based on K. Knudsen 6344, Weir Cyn, Orange Co., UCR, only second report for CA; Glacy et al. 2011)

(Baltzo 1989; von Reis 1991; West & Doell 1995; Bowler et al. 1996; Doell & Wright 1996; Tucker & Bratt 1996; Bratt 1997; Hill 1997; Wright 1997; McGee 1998; Robertson et al. 1998; Tucker 1999; Bourell 2000; Brodo et al. 2001 [p. 317, with color photograph]; Robertson 2001; Baltzo 2002; Nash & Elix 2002; Robertson 2003a; Jovan & McCune 2004; Tucker et al. 2004; Robertson 2005b; Carlberg et al. 2007; Hinds & Hinds 2007 [p. 251, color photograph only]; Knudsen 2007b, 2009; Knudsen & Kocourková 2009a, 2009c, 2010f; Rotter 2010; Tucker 2010; Glacy et al. 2011; Benson et al. 2012)
Synonyms: Parmelia caperata,P. flavicans sensu Tuckerman,P. herreana,P. perlata var. flavicans,Pseudoparmelia caperata

Flavoparmelia subcapitata (Nyl. ex Hasse) Hale ex DePriest & B. W. Hale

Synonyms: Parmelia conspersa var. subconspersa,Parmelia rutidota
Note: Collections from CA under this name are misdeterminations.

FULVOPHYTON Ertz & Tehler

FUSCOPANNARIA P. M. Jørg.
(J&osl

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Constancea 85: Tucker, Catalog of California Lichens

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Shirley C. Tucker Cheadle Center for Biodiversity, Department of Ecology, Evolution & Marine Biology, University of California, Santa Barbara, CA 93106-9610 USA; Santa Barbara Botanic Garden, Santa Barbara, CA; and Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803 tucker@lifesci.ucsb.edu Type all or part of a lichen name into the search box.

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Using lichen communities as indicators of forest stand age and conservation value

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Using lichen communities as indicators of forest stand age and conservation value

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Lace lichen has three qualities that make it an ideal candidate for the state lichen of California:

It is easy to recognize even by those not very well acquainted with lichens

It is common throughout much of California-growing along the coast from the northern to the southern borders and up to 130 miles inland

It is a strikingly beautiful lichen.

While small in stature, lichens play a big role in the ecosystem. With nearly 1,900 species of lichens in California, they contribute to our region's rich biological diversity. Lichens are known for their sensitivity to air pollution and climate, and are being used across California to monitor air quality and climate change. Lichens are an integral part of the cryptobiotic crusts that stabilize desert soils. Additionally, animals use lichens for food, nesting material, and camouflage. Humans have found a number of uses for lichens as well. Possibly the most promising is in the area of medicine. Lichen extracts are being studied for their antibacterial properties.

CALS sees this designation as an important step in increasing public awareness of the significant roles that lichens play in our natural environment. Calling attention to lichens by recognizing one of them as the California State Lichen creates an opportunity for us to learn about and celebrate the things that make California special.

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California's State Lichen: Lace lichen ( Ramalina menziesii ) - California Lichen Society

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Lace lichen has three qualities that make it an ideal candidate for the state lichen of California: It is easy to recognize even by those not very well acquainted with lichens It is common throughout much of California-growing along the coast from the northern to the southern borders and up to 130 miles inland It is a strikingly beautiful lichen.

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If you want to better understand what lichens are, where they grow, how they reproduce, and how to identify them, this is the class for you! Expert lichenologist, Jesse Miller, will enlighten you with the biology, ecology, and identification of these weird and wonderful composite organisms.

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I﻿n this Speaker Series talk by lichen expert Dr. Frank Bungartz, learn all about what lichens are, what they look like and where they can be found, as well as the fundamental role they play in ecosystems. Dr. Bungartz will share his research on lichen diversity and function in the Sonoran regions, Galapagos, and Ecuador.

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Lichens: What They Are and Where They Grow

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A great overview from the British Lichen Society

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A lichen is not a single organism; it is a stable symbiotic association between a fungus and algae and/or cyanobacteria. Like all fungi, lichen fungi require carbon as a food source; this is provided by their symbiotic algae and/or cyanobacteria, that are photosynthetic. The lichen symbiosis is thou…

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Marine Fungi - Cassie Ettinger, PhD. Mushroom Revival Podcast

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Marine Fungi - Cassie Ettinger, PhD. Mushroom Revival Podcast

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Alex 0:22
What is going on mushroom family Welcome back to another episode of mushroom revival podcast. We are unbelievably obsessed with the wonderful, wacky world of mushrooms. We're bridging the gap between you our lovely, exuberant special listeners and the wonderful wacky world of mushrooms and fungi. We bring on guests and experts from all around the globe to geek out with us and go down mushroom rabbit holes to explore how incredible mushrooms are. We are mushrooming the culture around mushrooms and we're so excited to swim or surf into this next episode. Let's get it started.

Lera 1:09
All About marine fungi. We are welcoming Dr. Cassie editor who is currently pursuing her postdoc at the University of California Riverside in the department of microbiology and plant pathology. Welcome, Cassie. Thanks so much for giving us some time.

Cassie 1:25
Yeah, thanks for having me here. It's been I mean, it'll be a pleasure, I'm sure. Yeah, so I'm a postdoc at the University of California Riverside. In Dr. Jason stages lab, we study fungal phylogenomics. So lots of looking at fungal trees, thinking about their evolutionary history and doing comparative genomics to kind of get at their function. I previously was a graduate student and Jonathan eisenerz lab at the University of California Davis, where I studied the seagrass microbiome and also looked at the fungi associated with seagrass, which I'll talk to you guys more about today.

Lera 2:02
And we always like to ask the origin story and what got you into funneling your research into microbiology, but then furthermore, into fungi?

Cassie 2:11
Yeah, you know, it depends on if you ask me or my mom, how this got started, she'll say that she bought me a microscope when I was really young, and that I became obsessed with looking at microscope slides and looking at, you know, these things like pond water under the microscope, and that it was all her and her idea. But um, you know, I don't remember any of that. Sorry, mom.

Alex 2:32
Throw her under the bus.

Cassie 2:34
I mean, I do you know, I support education for children of STEM. And so I do think that that probably played a role. But it was really later in my education I was getting I read Jurassic Park, I was really interested in kind of the evolution of humans and how, you know, how do we get here? How did we become what we are? And I kind of went into this into undergrad thinking about evolution, thinking about how do we study evolution. So I started thinking more and more about genetics. And then I got the opportunity to study in the lab of Dr. Ellen Sims at the University of California, Berkeley. And so she studies plant microbe associations, specifically looking at some bio system mutualistic relationships between these plants and these bacteria. And so that got me thinking about what how organisms are interacting and how cool and different bacteria are, how a lot of life on this planet would not exist without relationships with bacteria. So humans, we have the mitochondria that used to be a bacteria that an ancient ancestor of humans and golf, right. And then now we have this relationship that's so intertwined. And what we are, that's how we have our energy plants. Same thing happened with chloroplasts. And so thinking more about how these interactions between different organisms evolved through time. And thinking about microbes specifically is how I got into graduate school. And so I joined Dr. Jonathan eisenerz. Lab, he's this big microbiome person in our lab there. We did microbes on everything, right? Cats, koalas, the space station, different buildings, seagrass frogs. And so when I joined, he just gotten a huge grant to look at the seagrass microbiome. And so I was like, okay, great plants, microbes are interactions, thinking about what they might be doing, thinking about how did these interactions evolve through time? This is great. And then when I started reading the literature, looking at what's been done looking at what we know, it was really clear that we knew nothing about the fungi associating with these sea grasses, these marine plants. It was just it was kind of shocking, really that because on land we know that fungi especially mycorrhizal fungi are very Really important for plant nutrient uptake. And were really important for the movement of the ancestor of plants onto land. And because of that increased nutrient uptake that they're getting from this association with these fungi. And so the fact that nobody really looked to see, you know, do the sea grasses have those mycorrhizal fungi? And if they don't, are they still associating with fungi? What's happening? That was kind of shocking to me. And also very exciting, right? At the kind of the wild west of looking at something that nobody else had looked at before. And so that's kind of how I got involved with marine fungi. And I've kind of stuck there because it is this really exciting kind of novel area that people have just kind of ignored for a very long time.

Alex 5:44
Yeah, I mean, most mycology that you think of, or mycologists their terrestrial basket fillers, you know, they're they're out porcini hunting in the mountains, but you don't think of people on a, on a canoe or something. Or scuba diving, looking for fungi. And surprising I mean, what 71% of our planet is water. And 97% is the ocean. But you know, there's rivers, there's creeks, there's ponds, there's lakes, there's water in our atmosphere, there's, there's so much water on the planet, and we don't really, or at least I don't associate water with fungi. But you know, and that's so exciting. It's why we're unbelievably passionate about mushrooms and fungi is this field that it's barely even scratched yet it has unbelievable amount of potential. And so can you give our listeners maybe a little one on one? And for us a little one on one on marine fungi? What are they? I'm sure people are imagining little cap and stem mushrooms floating in the ocean or something like that. But what exactly is going on?

Cassie 6:57
Yeah, so I think probably most of marine fungi, or at least what we know, so far, is going to be microscopic. And so a lot of these associations are not going to be able to see with the naked eye. So unfortunately, we're not gonna have these beautiful mushrooms that we're just finding and you know, maybe one day we will find them, maybe we just haven't found them yet. I do know that there are some freshwater mushrooms that do exist and that have been found. So it's only a matter of time really, if you think about it. But yeah, so these are going to be microscopic organisms they're going to be probably living for the most part on are inside of other organisms. So honor and seagrass on our end, corals, honor and fish in their guts, or they're going to be living in their tissues. And then they're going to also be some fungi that are swimming around in the actual water system. And a lot of these are going to be associated with other organisms and some of those organisms you might not be able to see with the naked eye either. So there's a lot of fungi associated with diatoms, which are microscopic, you carry out there are some a lot of fungi associate with phytoplankton. And so these associations are things that are really important, especially for our world, and especially thinking about our changing ecosystem and climate change. And but we're not actually seeing them with our eye. And so you do need some sort of microscope to see them.

Lera 8:19
And can you describe where these fungi are found on the taxonomic tree? And if they are kindness and filamentous, or more Eastlake, or if they have a flagella to help them swim? What do they look like?

Cassie 8:31
Yeah, so what has been done is very limited, but what we're seeing so far is that we have a lot of kind of these more basal lineages of fungi. So a lot of chytridiomycosis to some of these lineages that we don't know a lot about like a filetto my Kota and Rosella mycota. These are the kinds of lineages that we're seeing a lot more of than we might expect. And there are also ascomycota, and basidiomycota. Often these are going to be found associated with organisms. And so they're going to be more found in yeast like morphology, or they're going to be hyphae, like so a lot of these organisms form pseudo high fees, so they're not true hyphal stages. And so you're gonna have a lot more of these kind of yeast or sporulating. fungi in terms of a flagella, that'll just be the kitcher do my Kota, best study on my Kota and ask them I could have lost that. So they have a flagella for their spores. And so that spore comes from around and then find a host usually where they'll form their sexual stage and release more spores.

Alex 9:37
Putting the theory of panspermia aside that mushrooms came from space or fungi came from space. it you know, most of life came from the ocean. And so are these marine fungi, the ancestors of terrestrial fungi or land, mushrooms and fungi that we see around like chanterelles and things like that.

Cassie 9:57
Fungi at some point would have come on to land I believe that was before ask him my code and the city on my Kota evolves and they evolved during that transition onto land or approximately there and then an evolutionary time. So things like Kindred are going to be more closely, or at least going to be more similar in their traits to maybe ancestral fungi, which would have been marine. And then we actually have a lot. There are two or three lineages in the city of myco, in the ASPCA myco, that have actually started to make this transition back into the marine environment. And we see this happening several different times, especially in the ASCO, my coda, and a couple of different lineages. And so it's not just fungi evolving. And then coming on to the onto land, we're actually seeing land fungi returning to the marine environment, which is one of the harshest environments to re enter. So it's kind of crazy that they're doing this so many times across these different lineages of fungi, it kind of speaks to their ability to adapt, and have these kind of really cool mechanisms of not only just adaptations, but different kinds of metabolites and products that they're making. They're very adaptable. They're very hardy. It's kind of crazy, especially when you compare it to you know, the only animal that ever went back into the marine system was was whales really, right? That's kind of like, and then for when we think about plants, sea grasses are the only flowering plant that has made that transition. But when you look at fungi, there are so many more species that have made that transition back into the marine environment. And it's kind of a testament to fungi in their adaptation potential.

Alex 11:39
I had no idea that whales would back into the water, they were on land at one point, that's nuts. whales are crazy. They just hold their breath, though, and they're huge. I cannot believe they haven't evolved gills. And that just blows my mind that they live in a place that can't breathe.

Cassie 11:59
Why? Because the evolution of lungs was so difficult that going back it was easier to just develop a blowhole than to redevelop gills.

Lera 12:10
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Lera 13:38
That is fascinating. And obviously, the fungi that are living in the ocean must be extremely salient, tolerant, and they're living underwater and that most of the fungi that we know here on land, they need access to oxygen within the air. So are these fungi getting oxygen? Or are they anaerobic? Or do they have some sort of system in place to allow them to get the oxygen from the h2o that they're living in?

Cassie 14:05
Yeah, so there's a lot of dissolved oxygen in the water column. And so that's how like fish will get their oxygen, they're just taking the dissolved oxygen through their gills, fungi are able to just absorb that dissolved oxygen in the water column as well. As you get down into the sediment in the sand and you go start to go deeper. So if we start looking at some really deep sediment from really deep in the ocean, that's where you're gonna start to find no oxygen. And that's where we might start to find some of these anaerobic fungi. We know from human gut studies that there are anaerobic fungi that exist. There's a limited number of them so far that have been identified. And I think that as we start to learn more about the marine ecosystem, and as we start to learn more about kind of fungi generally, especially in some of these environments, where they've been under studied, we might find, you know, a significant number more some of these anaerobic fungi that are doing something very good In order to survive.

Alex 15:02
That's a bummer. I was hoping you'd say they have a blowhole. And it's funny because I haven't had much research into marine fungi. And it's shocking to me that we've only discovered an estimated 5% of the ocean, which is mind blowing to me. And I'm afraid of deep ocean because of that fact right there. I there, I believe there's some crazy stuff down there that's waiting to eat me. But I'm because there's only 5% discovered, you know, is that a combination with so little research? So, so little mycologist actually doing this research? Do you believe that there's just an incredible amount of species that we've just yet to uncover? and marine biology?

Cassie 15:56
Yeah. Oh, 100%. You know, we know so little about the ocean generally. And we know so little about marine fungi that there's got to be, you know, 1000s upon 1000s, if not millions of species, as it is, when we think about land fungi, there are between 100,200 1000 species that we know about and have kind of classified. And it's estimated that really there should be about two to 3 million fungal species on land. And so if we don't know that little about terrestrial fungi, and we already know so little about marine fungi, only 1500 approximately have been classified that way so far. You know, it's, it's anybody's guess how many there really are. So yeah, I would be really excited to be able to know in like 50 years, or 100 years.

Alex 16:43
There might be a fungi with a blowhole. There might be yet.

Cassie 16:49
There's a mushroom with a blowhole. I mean, your wildest dreams could come true with gills it has been.

Lera 16:56
Yeah, exactly. So how do you like have you personally found any new species? And how do you search for these things? Are you just going to seagrasses and basically swabbing them on a petri plate and doing PCR? What does this look like? Yeah, so

Cassie 17:12
I've done two kinds of studies. One is to try and get culture the fungi directly from samples in the marine environment and see what we get. The problem with this approach is that it's going to prioritize things that are fast growing, and things that we already know what they are, because the kinds of media we're using to grow them have been the same media that have been used for years, you know, we're feeding them the same things that people have fed them for years, we're gonna find the same kinds of things that people have found, because we're providing, you know, the same kinds of nutrients. And so I think that you kind of have to get creative in what you provide, you know, media in order to find new organisms. And so part of that, it's, it's difficult to find new things, period. And then it's difficult to find new things when you don't know their growth conditions. And this is a problem that the bacterial field has, as well, as you move to DNA based studies, which is the other part of my work, where you're just surveying the environment, serving the DNA that's present, and then saying, Okay, what actually is there, even though we're not growing all these things, and you find so many more different things, and that's where we're finding all of these chytridiomycosis to these a few little Mikoto sequences. And those things are going to need different growth conditions than the conditions that have been used for so many years. And they're going to need a lot of people do like baiting where you put out a bucket, and then you put feathers or snakeskin in the bucket, and that'll bring the fungi and kind of enrich them. And then you're able to find the kids using the baby hair. If it's really blonde. These are some of the methods that

Lera 18:52
Why feathers, snakeskin and baby hair?

Cassie 18:55
I think it has to do with chitin and some other compounds that are in them. I don't, yeah, I have no idea. It's just kind of crazy things that were used in olden times that kind of were like, Oh, this works. We're gonna keep doing it. And yeah, I mean, those methods are successful at getting kids in wrenched and getting them out. And so like a lot of these kind of methods are old. And as we learn more from DNA data, what's there as we can determine what kind of genes they have, we might be able to determine, oh, look, it has, you know, this gene for this carbon compound, we'll put that in the media and suddenly now we're able to culture this organism, right? So a lot of what we're doing right now with marine fungi is more from a DNA based perspective, just because we're finding such a breath of diversity there. And we're not limited and by the culturing, but we're also doing these culturing based assays. And what we're finding is, you know, a lot of these generalists tax a lot of Penicillium Aspergillus, and it's not that these things aren't important. I think that these things are critically important in these ecosystems. They're just they're more studied per se than some of these other interesting lineages that we know so much less about.

Alex 20:11
And that's particular, particularly because of researchers looking for natural products specifically, you know, penicillin type antibiotics or new drug discovery in these extreme environments, right?

Cassie 20:28
Yeah, no, exactly. A lot of there's a lot of interest in natural products discovery, these things, again, are found everywhere. They're found on land. They're found in freshwater systems. And they're found in the Marine system, because of their high ability to adapt to these kind of really different and distinct habitats. And that leads to these really cool natural products that can be then used for Research, or anti pollution or whatever your favorite causes, right? You're gonna find some sort of natural product, because fungi are amazing. And they're making all sorts of really cool things. And so because of that, they're Yeah, they're more studied.

Alex 21:05
We had an episode with Nick money, who's a researcher, and one of the things that he was researching back in the day was, you know, how bueller's drop is associated with our water cycle and carrying spores. And so spores would be drifted up in the air currents tract water droplets. And his theory is that they might have an influence on on rain and weather. And that's, you know, a way that that spores are traveled throughout the air. So I got that check on where fungi are in the water water system. But where else do they show up? Because, you know, there's oceans, there's creeks, there's ponds, there's lakes, there's bogs, there's marshes.

Lera 21:57
There's ice.

Alex 21:58
There's ice. Yeah, there. I mean, fungi have been found in Antarctica. So

Lera 22:02
There's boiling geothermal, which are there. And all of those places are the spots, all the places.

Cassie 22:10
Yeah, I mean, you're gonna find fungi, no matter where you look, for the most part, I would think, but just with other biodiversity, you know, you have rain forests, you have these beautiful kind of coral ecosystems, or you have these huge kelp forests, like these places where you have hotspots of biodiversity from a macro organism perspective, I bet those are the gonna be the places where you find more diversity at fungi. And that's just gonna be because fungi like to interact with other organisms, right? They're very friendly. So you know, or they can be focused. But um, so I think those are going to be the places where we seen the most kind of blooms of diversity, but even in places where they're kind of desolate, like the desert, there are a lot of fungi out there, and bio crests, and all sorts of cool things are happening. So they're not limited, which is, which is really exciting. So I want to rewind just a little bit and ask you about is the benefit to being able to culture these under studied fungi, the ability to analyze their metabolites. And that's just something that you can't do with straight up DNA. So there are a couple of benefits. The first is when you have a single organism, you can do all sorts of experiments, right? So you can start to look at how it divides, you can look at specifics in its morphology, you can look at specific interactions with other organisms, right, you can see that you can track specific molecules or specific proteins, you can genetically modify it, you kind of can get into this very tractable system of manipulation. And so yeah, you can then look at specific metabolites. When you're looking at an environmental sample, things get really complicated really quickly. You can still look at metabolites, but then it becomes very difficult to track a single metabolite back to a single organism and even track a single organism back to all the DNA that belongs to that organism. You have under studied lineages, fungi, nobody has sequenced the genome of that fungi, right. So now you have all these pieces of DNA and you're like, Okay, does this piece go with this lineage of fungi? Or does it go with this other understudy lineage where we also don't have a genome or have any idea? And how do I decide which piece goes in this genome with this organism? And how do I know I don't have five individuals of the same organism, that now I'm lumping together so it is a little bit yes in tech. But as we develop better methods for doing this, a lot of this work is now done in bacteria. There's a lot of work done on via environmental samples. There are a lot of new methods that allow you to do these kinds of fine kind of splitting apart of multiple puzzle pieces and different puzzles. Now in some of those methods are being applied to fungi with some success. And as we continue to develop the methods that'll just get better and better. But ideally, eventually you're going to want a culture so you can do some experiments. And then you can start saying, Okay, I have fungi one and fungi two and fungi, one I think is beneficial to the seagrass plant and fungi. Two, I think, is a pathogen. And so what happens if I interact the two together? Are they going to, you know, suddenly, I'm going to see that pathogen affecting the seagrass negatively, or are they going to both become pathogenic? Or what's going to happen is we have multiple organisms interacting, because in real life, it's not just one organism interacting with our plants or our hosts are an environment. It's a community. Do you have an ocean Agha that you use? Or I'm just curious about the very medium itself? Yeah, so you can take seawater filter it to hopefully remove most of the living material, and then sterilize it. Keep it in the dark for a couple of weeks. And then you can use that in your media. Or you can use there's something called Instant ocean, it comes in a box, it's for aquariums, and it's essentially just a salt that you add to your media and it's supposed to approximate the ocean.

Lera 26:13
That is so cool. Is

Alex 26:18
Agar agar is derived from red algae. Is that from the ocean? Yeah. There you go. Cool. One of my favorite stories of collecting fungi from the ocean and just showing the unbelievable resilience of fungi were these researchers called jamstack. I'm not really sure what that stands for. But in 2012, it used a deep sea drilling vessel on a seabed 80 kilometers off Hashi, no hay. And they drilled 12,000, or sorry, 1200 meters below the water surface. And they drilled into the sea floor and picked up a sample. They found 69 different types of fungi. I think they're all spores. And one species that they put on ag Gar actually grew out, and they found out it was over 20 million years in hibernation. And not only did the mycelium grow out, but it made a little fruiting body on the cigar. And this was a schizo philam species of mushroom, like a cousin of schizophrenia and commune which has over like 30,000 mating types. And to think of everything, it's like finding an apple tree seed underneath the ocean, and planting it in soil. It not only grows a tree, but you can pick it apples off the tree. Unbelievable the resilience of fungi. What kind of percentage of fungi. Do you find living versus maybe are in hibernation? Maybe there?

Cassie 28:06
Yeah, I mean, we we just have no idea. And this is one of the biggest questions I think there is in the Marine mycology world is whether or not the fungi that we are seeing are active in the marine environment, or whether they are just either dormant spores that have been there for a really long time, or whether they're just passing through, right. And so there's a lot of work that needs to be done to look at things that are actively growing. We know from a lot of work done with other organisms, right? Like we can see that the fungi are actively growing inside of seagrass tissues, for example, we can see some of these fungi actively degrading compounds. But there's still so many fungithat we're finding that we're like, are you active? Are you just here? And I think we just don't know yet. You know, I would love to know the percentage of fungi that are active at any time. In the marine environment. I don't even think we know that for bacteria, either. The percentage of bacteria that are actively, you know, doing things versus the number that are just kind of dormant. And so yeah, this is a big open question in this field. And I really hope someone comes along and figures out, you know, do we just have this huge seabank of fungi from you know, the Jurassic or the Cretaceous, or all these really ancient times that we aren't seeing on land right now? And if we drilled really far down, are we going to be able to find them? And if we do find them, are they still viable? Right? We know that they're very resilient. We see that there are so many fungi, especially in the marine environment. It's a very, very, you know, salty, sailing, low oxygen, lots of stressors. So if you're able to survive in the marine environment, Yeah, why not survive for 20 million years.

Lera 29:56
It's also very cold in the ocean, which is sounding a lot Organisms don't like so that resilience, high pressure. Yeah, definitely. Speaking of cold pressure places have any samples from probably not the bottom of the Mariana Trench. But, you know, heading that way. Have you found any fungi? Deep down?

Cassie 30:16
Yeah, so there's been some work in the Gulf of Mexico looking at deep sea deep sea floor fungi, both from a culturing perspective, and from a DNA based perspective, and they have found fungi. There, a lot of the ones they're getting back from the culture collections are going to be again, these kind of generalist, everywhere fungi, like the penicillin and then Aspergillus, but they are seeing, you know, one real tractable fungi that once you bring them up or Okay, and are able to survive at, you know, atmospheric pressure that they're growing, they're in the lab, and then it's matching what, you know, generally everyone is fighting for the DNA based data, which is, we see a large number of either fungi where we just have no match to any database at all about what these could be. We know they're fungi, but we just have no idea what they are or they're going to be in that kitchen video my Kota, one of these other lineages where we kind of have a little bit of an idea of what's happening but we still don't know very much.

Alex 31:21
So I'm gonna put on my not all mushrooms are quote unquote, good and sunshine rainbows hat. And so one of our passions is entomopathogenic fungi. And so typically you think of like corcept they attack bugs, but they you know, infect and enter pads and or is it arthropods? I think they attack arthropods. And, you know, some arthropods are lobsters and barnacles and crabs and a lot of other creatures. And I looked it up and actually, most, you know, you know, like whales, dolphins, a lot of fish are susceptible for fungal diseases, and then rotifers, even tardigrades were found infected in the maritime and arctica. Do you think all sea creatures are just susceptible to fungi? His wrath and domination?

Cassie 32:28
Yeah, I mean, I think that we're gonna find as we kind of expand our knowledge of marine fungi to more organisms, and more places on this planet, especially thinking about different kinds of habitats that they are living in, we're gonna find one, we're gonna find fungi everywhere, they're going to be beneficial, they're going to be pathogenic, and they're going to just be kind of hanging out. They're going to, you know, be crossed that whole range. So it won't surprise me to find some of these fungi being pathogens. I we know that they parasitize diatoms in the Arctic. And whether those associations are truly parasitic, and not actually some sort of beneficial relationship, I can't remember if they've, you know, said that for sure. But we know that there are at least living in these associations. And I know that I think it's sea turtles that there's a fungal pathogen that affects sea turtles. But a lot of these other fungal pathogens and fungal diseases from a historical point of view end up not being fungi. seagrass has, yeah, so seagrass Wasting Disease, for a really long time was thought to be caused by a fungal pathogen. It turns out, it's a header upon a header. ICANN is just another kind of microbial eukaryotes. It's a marine slime mold. And so it looks very similar to fungi, but it's just giving fungi a bad name. There are also a lot of fish diseases that end up being Oh, my seats, which for a really long time began because of morphology, they were thought to be fungi. And then when you start to look at DNA based data, you're like, No, no, dude, no bra. No, they're not. These are not fungi. And so they've just been giving fungi a really bad name for a really long time. So I do think that we'll find a lot of fungal pathogens, but I think what we'll find is a lot of these things that we think are fungal pathogens are just really other microbial eukaryotes that are causing disease. And so you know, fungi are just one of many microbial eukaryotes out in the marine ecosystem. And so we're talking about marine fungi and that's really exciting. But just as understudied as marine fungi are there are many, many, many other understudied lineages out there in the marine ecosystem that are microbial.

Alex 34:46
And, you know, you talk about giving a bad name and yeah, I think Paris parasites and whole parasitic is bad in and of itself and has a bad connotation. It's all about perspective. You know, we just had a researcher on talking about the honey fungus. And it's, you know, for a lot of people, it's super destructive, and it kills, you know, 1000s of trees, and it just demolishes whole forest. But for other, you know, parts of the ecosystem, it could make prairies and it could help a lot of other animals and plants. And so for this perspective, it's like, well, it could kill fish, but it might help, you know, balance out the entire ecosystem. So it's all, it could be beneficial for another creature. And so it's all a matter of perspective. And I think good and bad is totally subjective. And humans love to slap on those labels, but it's really not true. They're just, it is what it is. And and that's just the way the universe works. And it works in mysterious ways.

Cassie 35:56
Yeah, and you can have closely related organisms, where one is really, really detrimental, and one is really, really beneficial. So like, the kitchen that is causing these amphibian declines globally, like that's really bad, right? whereas there are other threads that are really important for the carbon cycle. And they're associated with phytoplankton. Alright, so just because these two things are both fungi doesn't mean that all fungi are good, or all fungi are evil, fungi or just fungi.

Lera 36:29
So let's get into your research and the associations with fungi and seagrasses. And why study this, obviously, fungi play a crucial role in the health of an organism. But I would love to hear what you found and why you're dedicating so much of your resources on this research.

Cassie 36:50
Yeah, so the reason we wanted to focus on sea grasses is because they also reentered the marine environment from land or their ancestors. And so they themselves have a really interesting evolutionary history. It happened two to three times so seagrasses, it's a group of organisms that aren't closely related. And so we were really interested in looking at whether when they re entered the marine environment, they're bringing fungi from land with them, or whether they're forming novel associations with marine fungi. And so that was kind of the basis of the second half of my dissertation was kind of answering these questions or trying to start to answer these questions. But the first thing you have to do before you can answer any question is kind of survey the system and say, like, Okay, what would I expect naturally to be happening here? Who's here, where they present? And what kind of diversity can I expect? And so the first thing I did was, look, I looked locally at Bodega Bay, California, I used high throughput DNA sequencing to look at a fungal marker gene, just one gene that you can use to identify kind of the diversity of organisms there based on databases that exist from known fungi. And so what I found was, when I looked at the fungi associated with seagrasses, focusing specifically on one species, zoster Marina, or eelgrass, which is really common in the Northern Hemisphere, so if you ever go out, and you're in the Northern Hemisphere, and it's low tide, sometimes you can see these seagrass beds and walk in them. And so focusing on that species, what I found was that up to 75%, and even 100% of the DNA sequences that we had that were fungal, were unable to be classified. Beyond just this is a fungal sequence, we couldn't put it into a fungal phyla. And that was because we're using these databases that had been based on land fungi. And there isn't a lot known about marine fungi. So there was nothing to match to. And so as I started to do this, and I was looking at this, I was like, Okay, well, but some of these things are really, really, really abundant making up, you know, 40% of a sample event, just one individual sequence. So what I did was I got a bigger piece of that sequence by designing some specific targeted primers based on my smaller sequence and that allowed me to identify that the biggest kind of player at least locally to Bodega Bay was in the kitchen to my Kota and it was a lubu mice Italia species. And that's, again in the kitchen to my Kota. It's in a group that is known to be parasites of freshwater diatoms and also of algae and so we kind of hypothesize that may be seagrasses as a marine plant, are providing a novel kind of habitat for these organisms that they're associating now with sea grasses like the freshwater ones are associated with algae or diatoms. So that was kind of our first study. And then in my second study, we did a cultural based essay, right, so we took samples and we cultured them, we identified what we found using, again, one marker, Gene and PCR. And what we found was, we found a lot of penicillin, I think almost half of what we found was penicillin, it was kind of crazy, we had something. But we also found several kind of black yeasts, we found some plant pathogens, and we found some things that could be possible plant endophytes, that are providing some sort of beneficial function for the plant as well. So we did get a nice range of things that kind of were more general from across the range of things that have been found in are known to be marine fungi to things that are just kind of considered terrestrial fungi or could be everywhere. And so we also found a couple, you know, we found some bacteria and some on my seat. So it was kind of a really friendly place, full of all sorts of microbes. And then in my latest study, which hasn't actually come out yet, although it's available online, we kind of expanded that first study using DNA sequencing now to look at a global scale. So not just looking at Bodega Bay, California, but now looking at the entire northern hemisphere, looking at the fungi associated with seagrass trying to say something about whether it's always associating this one species Oster, Marina eelgrass, if it's always associating with the same fungi, or is it forming novel associations in each location that it's found in? So are they kind of adapted locally? Or the fungi themselves adapted locally? Are we seeing large patterns where we have this very kind of strong conservation of fungal partners. And so what it looks like is that a lot of the fungi are coming from a local area. So it does look like there's a lot of localized, you know, adaptation, whether that means that the fungi haven't adapted over long periods with the sea grasses, sea grasses themselves don't move very much, right, they're a plant. So it could be that we were looking too broadly, for that kind of, to answer that kind of question. But we are seeing some conservation, they're always associated with lots of kitra to mycota. They're always associated with lots of novel lineages that don't match any database that we have right now. And there are some lineages in the sword area, my seats, which includes known plant endophytes. So beneficial potential beneficial partners where they don't really match to anything closely. And so these could be novel lineages within that group that are associating with these plants as well and providing some sort of function that's either beneficial, or again, we don't really know the function, since it's just, it's very kind of early days. But we'll be able to hopefully find out one day, I'm hoping that we get more at function as we learn more and more about what's happening. And again, as these methods improve, to look at kind of these environmental survey data in terms of more of genomic regions, because again, this is all done with one gene. And you can imagine a genome is 30,000 plus genes. So as you start to scale up, you can start to answer much broader questions.

Alex 43:20
One of the I was just trying to look it up. And I couldn't find the actual original study, but I believe it was Yellowstone National Park, and I could be wrong, but in one of their acid pools, it really or thermo, thermal pools, which is, I think, a really high pH as well. Really, really hot, incredibly hot water. And they found these plants thriving along the edges. And like, How the hell do these plants survive in this crazy environment? And they found that I'm not sure if there's bacteria in there, but I know there is fungi, endophytic fungi associated with these plants and, and they isolated each individually. So the plant couldn't survive alone in that high heat or the fungi, but together they could. And so that was pretty nuts. And I know you just said that. You don't know the benefit of these fungi. But if you had to guess Do you think they have a role in solidity? or?

Cassie 44:26
Yeah, I think the most obvious answer is nutrient uptake. It's always hard to get nutrients no matter where you are. And so a lot of these associations that do form are because you need some sort of either energy or you need some sort of nutrient that you're not able to get. So I think that could definitely be a possibility. We also know that some of these organisms can be important for degrading like toxic, toxic compounds. So bacteria are known for degrading sulfur in environments. fungi can also degrade lots of different kinds of compounds. So it's also possible that In association with like plant roots, seagrass roots, they could be doing something like that in the sediment. I mean, they're also Yeah, they could be providing protection against pathogens, right. So we know that from land plants that if you have an association, sometimes that'll prevent a pathogen from coming in by excluding that pathogen or by producing some sort of either antibacterial, antifungal. So there's a lot of different kind of possibilities for what could be happening in this environment. And I have a lot of hypotheses. Even about specific fungi that could be about what could be happening. But again, you know, there's just it's so it's so frustrating to stay so little sometimes, but you know, we are still so like, nascent field. I wish I could, you know, tell you the definite answer to your question, because I think it is really cool. And I think it's really important. And I think as we learn more, we'll we'll know, I mean, I think as we look at other animals, like, you know, like arthropods, and crabs in some of these other organisms that are in the Marina, aren't whales, right? Well, if we look at their guts, we're gonna find that fungi are really important for digestion, they're gonna be really important for immune response, they're gonna be really important and a bunch of different ways. And so I think, you know, I mean, I wouldn't be surprised to I know that they're important for carbon cycling, and so they're going to be really important for carbon sequestration, and, you know, climate change. And so like, they have all these kinds of things that we can point to and be like, yeah, fungi are probably really important for that. And I would love for us to be able to say, yeah, marine fungi 100%. They're the most important thing for that. And, you know, we're just not there. I mean, I think, you know, part of it is funding part of it is that it's such a new field. And yeah, I wish again, I you know, if we could have a conversation again, in like, 50 years. It is, yeah, I guess we'll still be around. Yeah, yeah. I mean, hopefully, we'll still be.

Lera 47:06
around too. So. But that's so true, what you were sharing. I mean, now more than ever, we have a responsibility to track our behaviors and our influences on the environment. Yeah, with all of the changes going on in the world, and the resources that we're taking from the earth, it's definitely important to understand what exactly we're doing when we choose to make a rubber tree farm or throw plastic in the ocean, because we don't know where else to put it. And if we're going to do these impetuous actions, I think we should be pouring money into understanding the implications of that whole thing. Hopefully, one day, the government will fund these types of things like they do in other countries. I know China is throwing money at researchers, and it's pretty amazing. I'd love to see that happening here.

Alex 47:56
That I mean, that's a good beginning to question that I was really interested in is I have a background in micro remediation. I didn't even think about marine fungi that didn't even cross my mind. And when I was studying, and I'm like kicking myself, like duh, and and I know a lot of people in this space are trying to take terrestrial fungi and just shove them in the ocean. And it's like, duh, they're gonna die. And most of them are you have to spend a lot of priming to make them sailing tolerant. Yeah, and you know, one example is Paul Stamets making myco booms. He talks about it in, I think he talks about it in mycelium running, but the just like these straw sausages, with oyster mushrooms, and obviously, it didn't work. But it inspired a lot of people to try to do it to clean up oil spills and things like that, or just shove them in creek beds and and they'll drown and like even stropharia and just, you know, inoculating wood chips and then trying to shove it in a creek bed. And it just coming up with constant failure. And yeah, I haven't come across research about marine fungi being used for micro remediation. But again, I haven't even piqued the surface. So have you come across marine fungi being used for oil spills or microplastics or for other pollutants that are just wreaking havoc on our oceans or rivers and other waterways?

You know, I actually haven't I thought that was you know, that's a really good question. I think somebody should be doing that. I know a lot of people who are thinking about bacterial remediation using some of the same bacteria that have been found after things like the BP Horizon oil spill, so I think, you know, as researchers we probably should be and and this is across the board. A lot of times fungi kind of fall behind. You know, bacteria step up first, fungi kind have come up after. And so I think this is another scenario where bacteria have kind of paved the way for fungi to come in and kind of be like, haha, we were always better at certain things as well, you know, like, for example, bacteria cannot break down, like higher weight polycyclic aromatic hydrocarbons, they just can't do it and fungi can come in and break down those kind of heftier molecules, which is awesome. And I knew some researchers actually met him here in Austin, Texas, at a local lab here and they made there's fungi, I might butcher the first part, but pesi to the opsis microspore.

Lera 50:42
There's a culture in our fridge right now.

Alex 50:44
Oh, cool, awesome. But it was it was named like the plastic eating fungi. And it got a lot of headlines. A lot of them are like semi bullshit. But, but I mean, it could degrade polyurethane really, really, really, really slowly. But like bacteria, and like UV light could probably do a better job doing it. But it was cool. Some Yale researchers found it in the Amazon. And it's new, it sounds really cool. It's a BuzzFeed headline. But I you know, it's doing research. And we're finding dozens and dozens, oh, close to 100 different fungi that can degrade forms of plastic over the last even couple years. And so I think that is super important for our aquatic ecosystems. But then we're bound to have another BP oil spill. And and there's tons of other pollutants that just get dumped into waterways on a daily basis that either are are going checked or unchecked. And people just don't know about it, radiation as well just kind of, it's still leaking into the ocean. And so if we can find these super extreme a file fungi that can partner with bacteria, partner with other organisms and find these solutions for our world's greatest problems, I think that's an incredible and also, you know, culturing Penicillium and other fungi to have new antibiotics and new drugs. So we can keep being healthy and make the world a better place. So thank you for being a frontier in this industry. I think it's, it's huge. And someone's got to do this work. So kudos to you. Thank you.

Cassie 52:34
Thank you.

Lera 52:36
So if you were to be speaking to a room of mycologists or myco files, much like this podcast probably is, what are some things you would say to surprise them about marine or aquatic fungi? What are some characteristics that you just don't see with the passivity of my seats and the ascomycota that we know and love? And what are just some of your favorite fun facts about aquatic fungi? Okay,

Cassie 53:03
Um, first they exist. That's my favorite. Fun fact. That's, like always a hard sell. I feel like that's the fun one. People don't really think about them. And then it's always like, No, no, I studied them, they really do exist. And they're really important. So I like to start with that one. The other one is that, and we kind of touched on this a little bit. So many of the sequences that we get out of samples from the marine environment, there's no match that we have in current databases of fungi, no match at all. So if you're thinking, you know, right, exactly, like, we just have no idea what these things are, it's just so kind of so wild west, it's even beyond whitelist. It's like galaxies and galaxies of just unknown fungi out there in the marine ecosystem. And we just have no idea. And so that's kind of an infinite amount of potential, that potential is infinitely great. I mean, they're probably doing really critical things. In our ecosystem, there's, you know, critical things for humans that they could do for us if we study them. And then that's, you know, probably also really, really, really something that we should be thinking about more and more. Another kind of fun fact is that there are marine lichens. And they live alone. And yeah, so some of these lichens only grow in the Marine system, and so they need the high salt to survive. And again, lichens are combinations of bacteria and fungi working in concert together to form this kind of organism looks like a moss but isn't a moss. And so I think that's just so cool, because one, it's these interactions between multiple organisms always super cool. And then too, because some of these can only be found in the kind of title regions are the marine environment, which is kind of crazy to think why would you live someplace that's so extreme, but they do. So that's cool as well.

Alex 55:00
We were joking. What yesterday the other day that that the the fungi that attacked tardigrades in the Antarctic maritime were like, they're the, they're the Vikings of fungi. They're like how how brutal can we get? Like, yeah, I'm gonna go to the coldest the most uncomfortable environment I could possibly find and just drive like the most resilient creature on the planet like, and I'm going to do it and I'm going to survive. They're like little Vikings, it's crazy. And I will I will never look at whales at the same time that.

Lera 55:37
You've sent us on a YouTube rabbit hole for later tonight, that's for sure.

Alex 55:41
Yeah, I think you know, I was studying different ecos biodiversity of ecosystems in Ecuador. And one of the really important ecosystems was the the marshes and how important kind of coastal landscapes are. And that degradation has huge implications for biodiversity. And it, there's so, so important and, and they're being degraded at such an immense rate. And so if those endophytes, or other types of fungi have this, you know, beneficial relationship with these coastal plants to help those ecosystems from degrading, that's massive. Also, you know, the sea turtles that are getting fungal infection that save the whales, you know, if if we can find you know, a penicillin that helps with that fungal infection, or maybe it's not even a fungal infection, maybe it's a new Mikoto or something else. That would be great, and help save the whales and sea turtles and clean up pollution. And I mean, they're just so cool, find new antibiotics, new everything. And just to discover it, just to discover it, you know, what I mean? I mean, I have a, you know, I get trapped in a rabbit hole of like, well, what is it good for, you know, and just, it's hard to just stand, stand back and just be like, it is what it is. And I don't have to use it. It just is beautiful, just because it it, it exists. And to dive into the 95% of the ocean that we have never discovered and probably 99.999% of marine fungi that haven't been discovered. And to know that, like your first Fun fact that they exist, first of all is unbelievable. So marine fungi for the wind.

Cassie 57:41
No, I mean, a lot of what I do his natural history, right? I'm a natural story. And I'm going around, and I'm kind of being like, okay, who's here, let's document who they are. And kind of making kind of a collection of sequences or isolates and kind of saying, Hey, this is who we find. And then someone else can come along and say, Okay, I'm taking this organism, and I'm gonna, you know, start to do experiments and look at function, and I'm just gonna go off on my ship and like, sail around and be the historian and the Explorer and do this kind of discovery based science because somebody needs to do it. Right? You can't get to Applied Science without first discovery based science. Right? That's how you find things that are useful for applications. You somebody has to go discover these things in the first place. And so yeah, I mean, I think, again, everybody who's listening to go, you know, one takeaway is, you know, fun scientist, be someone who stands up for science and make sure your kids or your neighbor's kids or your nieces, your nephews, make sure they're getting educated in science, and they know how important science is and not just science that's, you know, affecting you directly. Like, you know, right now everybody's, you know, trying really hard and praying for Coronavirus vaccine, right? That's the big thing right now. But um, you know, a lot of basic research went into the vaccines that are being, you know, generated today, people were studying these things for years, looking at natural bat populations, looking at natural viruses that are existing, and that research was built on to make the vaccine happen. And so they did discovery based research, which then led to an applied application. But if they'd never done that discovery based research, we wouldn't get a vaccine for another five years. Right. So it's kind of like putting your foot forward before you need it. Because again, if we don't put our foot forward now looking for these things, if the way that our ecosystem is changing as global climate change is happening as oceans are acidifying, a lot of these fungi might I mean, although they're very tolerant, resilient, so maybe they wouldn't be gone. But I mean, they could you know, they could just disappear with us, never knowing about them or anything. About what they could do. And we might miss out an opportunity not just from like a research perspective or even an applied perspective, we might just miss out on knowing about their natural biodiversity or missing evolutionary, interesting evolutionary stories even. Right.

Lera 1:00:18
So marine fungi, definitely. And as I was doing some research on you, I stumbled upon this website called stress, which was an acronym that was hilariously cherry picked from shed light and the dark lineages of the fungal tree of life. Could you talk about this project and what's going on there?

Cassie 1:00:41
Yeah, so that project, I'm a contributor on and it's being led by Dr. Laura Selman. And it's about these kind of dark yeasts. They're, they're dark in coloration. So they're black, these black yeasts. And this black coloration has kind of occurred throughout the fungal tree a couple different times. They're not each other's closest relatives. So this black color is evolving differently in each of these lineages. And they're all kind of able to survive in these really, really crazy extreme environments. Obviously, I'm involved because the marine environment has a lot of these black yeasts. But they're also found in the Antarctic, they're found in deserts, a lot of the work is being done in deserts. My lab mate, Tanya is working on desert crust, black East fungi. And so the whole idea behind this project is if we sequence the genomes of these black yeasts from these different environments, across the tree of fungi from these different lineages that have adapted to and become black and coloration in our extreme over a tolerance, these extreme conditions, can we identify commonalities between them that have occurred? In response to these kinds of extreme conditions? Can we identify genes that might be related to being tolerant? And the evolutionary history of these genes? Right? So they're obviously evolving separately? Because they've each kind of evolved them differently? So are they occurring in the same gene? Is it always the same kind of gene or same kind of protein or same kind of function or molecular mechanism that's resulting in this black coloration? And this tolerance? Or are they just doing totally different things? And they're all beautifully black? I think that, you know, that's kind of the idea behind it. So I think what's going to happen first is we'll sequence them, I believe them, we're going to be doing some work, where we expose them to different stressors, and see how that changes the genes they make the metabolites they make, and start to kind of try and figure out what's common between these different groups. And what's the same.

Lera 1:02:55
Just to add to that list of extreme environments? I'm not I don't think these are use like fungi by Gladys forum and all the other fungi that are found in Chernobyl, Fukushima, radioactive places. They all share this dark pigment that this melanin, I'm assuming it's melanin in the disease, the yeasts. But that's such an interesting question to know if they independently evolved to produce this pigment to survive.

Cassie 1:03:22
Yeah, and if it's the exact same pigment, right, if you're evolving the same pigment, even if you use a different mechanism to get there, that's really interesting. And that means that pigment itself is really, really important and could have really interesting applications. Put it in your, like houses and the paint and all sorts of things. I mean, I, I don't know they're all fungi are kind of just a limitless thing. microbes in general, a limitless resource for us to kind of appreciate and explore.

Alex 1:03:53
I'm gonna ask a very broad question. And we went over it, probably the whole podcasts. And so I guess I'll rephrase it. If I was gonna ask, you know, if you could see any research in this marine fungi field, what would you like to be done? I'm guessing it's everything. So what do you think is priority? What do you think is the the number one thing that you would love to see research in this field?

Cassie 1:04:21
Yeah, I think I would like to see two things happen. The first is I think that we need much more surveying done of the marine environment. So it needs to be just generally more studies looking at Who is there? Because we've only kind of touched you know, the surface only a couple of different kinds of organisms Do we know there's so much more out there so many more environments and habitats to look at? So first, I think kind of some kind of global survey that goes in depth and law. It could be several surveys, just more research generally about who's in the marine environment. And then the second is getting at that question of activity that we talked about earlier. And really digging down into What percentage of these organisms are active, and that could involve a lot of different kinds of studies looking at, you know, active metabolites and tracing them back to specific fungi, that could be some sort of staining to see fungal cells growing actively in these environments. But I think that also needs to occur. And then I guess I only said two, but a third would be, just generally we need more genomic resources for these these systems, right? You can only do so much if there's nothing matching in the database. Right? It's great found, you know, a really exciting understudied organism, but it's really hard to get out what they're doing. If you don't know anything more than a 20, you know, 250 base pair piece of DNA 250 letters worth, it's not very much. So we need a way more genomic resources. And in order to do all three of these things we need, you know, more support more money, and more scientists. So if you're listening, and you're like, marine mycology, that's for me, there are several labs now around the world that are doing this work. And so you could become the next marine mycologist. Right. So you know, I think we need some passion in this field.

Lera 1:06:15
I believe I saw a kit. I don't know if it was directly linked from your website, or what but it seemed like the type of thing that a citizen scientist or someone who kind of casually practices science, much like a lot of our listeners, they can buy this kit and kind of help with the documentation of these fungi.

Cassie 1:06:35
Yeah, I think you're thinking of our seagrass microbiome sampling kit, perhaps. And so we sent that out to different labs and different scientists and in the community, and also in universities, and they sent us back samples for those projects. So I don't think you can get that kit anymore. But there are other ways to become involved. You know, the first is tell everybody that read fungi exist.

Lera 1:07:08
Share this podcast.

Cassie 1:07:10
Yeah, exactly. Share the podcast. There is an Ocean Sampling day, it's more focused, it happens every year. Globally, it's more focused on, you know, actual macro organisms. It's not solely focused on fungi, but just any kind of increase in ocean science is going to end up helping the marine fungal realm. And then finally, I don't know if you guys have heard or talked about fold scope. Fold scope is an origami microscope, it's like, I think it's like $25, if you're an education, you think you can get them for free or discounted. But otherwise, if you're just a private citizen, or just a private person who's you know, you can buy one or buy several, and it's a little origami microscope, and you can, you know, take it out. And if you are walking on the beach one day and you find some driftwood or something you're interested in, you can take a look at it under the microscope, that you just pull out of your pocket. And then you can take a picture on your phone. And maybe if you think it's really cool, you can send it to someone or you can put it on naturalist. I don't know if they take those yet, but you can start documenting, you know what's happening microscopically. And if you do happen upon a marine mushroom, one with a blowhole or not, you know, you can contact you your local mycologist or get on Twitter and contact someone else who's in like the mycology field. You know, we love I think anyone, especially if you're a scientist on Twitter, or on social media, being contacted with something really cool. So I don't know if you guys have seen the fungi that we're growing on. What are they called?

Alex 1:08:51
The Twinkies. Oh, yeah. We're actually we're, we're bringing on Brian, on our show soon. And he was one of the researchers who did it Twinkies.

Lera 1:09:03
But yeah, that's so great testament to just regular people keeping Twinkies in their basement. And then voila, he finds something novel and extremely interesting.

Cassie 1:09:13
Yeah, exactly. So if that's you, you're you know, scuba diving or, you know, walking on the beach one day with your, your dog or your, your cat if you're, you know, InVenture cat person. And you see something really interesting and exciting, you know, share it with, with scientists. I mean, we love that kind of stuff. And, you know, that's how some of these things get found. I think that's how there's a freshwater basidiomycota mushroom. I think that's how that was found with somebody, you know, was just they found it in a river one day, right? You know, there's so much ocean out there. And you know, most of us can't swim in most of it because it's so deep, but for what we can get to, if you find something cool and interesting, share it.

Lera 1:09:57
Awesome. I'll have a link to the Fold scope and your website in the show notes. But is there any other place you would send people to follow your work?

Cassie 1:10:10
You know, Twitter is probably the best place to follow my work. I think it's probably if you're really interested in the community about science, but don't, you know, have a lot of scientists that you're interacting with yet I think Twitter is the best place in terms of trying to follow multiple scientists in the community. I know that's where I read most of the papers. That's where I find the papers relevant to me is I follow scientists, and you know, they tweet about, I just published a new article, here it is, and oftentimes, when they link those articles, if they are publishing them someplace that's closed access, which I don't think people should publish in. But that's another story. I think that science should be open to everybody, especially when people pay for it with tax dollars. But oftentimes, even if it's closed access, authors will have access to that article, when they tweet about it, that link will be open. And so you can go read it, even if you would normally not be able to access it. So that's a good way to get at papers if you don't want to be paying money for them.

Alex 1:11:15
Yeah, we have one final question that we ask all of our guests on our show. I'm going to tweak it a little bit. Because your marine fungi. So if marine fungi had the mic, the microphone and could say one thing to the whole human race. What would they say?

Cassie 1:11:35
Don't you forget about me.

Lera 1:11:39
Love it.

Cassie 1:11:40
Yeah, I think I mean, that's the big one, right? They exist, they want to be heard. They want to be, you know, known about I think that's, I mean, that's the really the biggest thing at this point for the field is, marine fungi exist. They have really critical functions, and they're really cool. So don't forget about and they won't forget about you.

Lera 1:12:02
I love that, strike a deal.

Alex 1:12:04
I'm picturing these like dog fungi wagging their tail, like when you forget about me. Or when you come home, they're like, hey, my owners. We're not people. But yeah, thanks. Thanks for coming on our show. That was that was really awesome. I learned a lot. I had no idea about the world of marine fungi. And now you open a door in my brain, and heart to marine fungi of how incredibly important they are, that they exist, and they're abundant. And it really is just such a testament of how unbelievably resilient fungi are, and how much we really just, we don't know anything. And that's so exciting. So thank you and thanks to all of our listeners for tuning in and tuning in with us to the mushroom family. If it's your first time listening, welcome. If you are a reoccurring family member, welcome back. We love you equally, and sending out a big fungal hug to anywhere, wherever you are in the globe. Or in space, we are in the ocean, we are sending you a big hug. And, you know reach out please we want to hear from you if you have any future topics that you want us to dive into or guests that you want us to bring in our show. And it really helps us out if you could leave a review. You know, we want to hear from you whatever is legit. In your experience. We want to want to hear what's genuine in your experience. So yeah, leave a comment leave a review, share with your friends on social media on the web or in person next time you're actually interacting with real life human beings and head over to our site Marshall revival calm if you want to check out a whole line of mushroom functional mushroom products. We also have a bunch of blog posts and a lot more of our podcasts. If you're just listening to this if you're on like Apple iTunes, or Apple podcasts or Spotify, this is a video as well. So head over to our website and we will have a little video thumbnail where you can watch the video portion.

Lera 1:14:24
Thank you so much, Cassie, and thank you everyone for tuning in.

Alex 1:14:28
And as always, much love and the spores be with you.

Transcribed by https://otter.ai

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Explore the mysteries of underwater fungi. Meet Dr. Cassie Ettinger and learn about marine fungi, evolution, and surveying. Discover more. Tune in and listen!

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In the UK

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In Occidental, CA

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Camp 2023 will be January 13-16, 2023

What is SOMA Camp?

SOMA Camp is an annual gathering of mushroom enthusiasts sponsored by the Sonoma County Mycological Association. This four-day weekend is held in January, and is an almost non-stop event with activities, lectures, and workshops focused on learning about wild mushrooms.

The camp, a benefit for the SOMA Scholarship fund, is packed with mushroom forays, specimen tables, slide shows, and top-notch speakers.

Nestled in acres of oak, madrone, tan oak, redwood, and Doug-fir near Occidental, California, we will move breezily from class to woods to dining feasts, enjoying it all. There is so much to take in!

COVID-19 Updates:

To assure camp attendees safety during these uncertain times, all SOMA Wild Mushroom Camp tickets are subject to restrictions and requirements put in place by SOMA, the CYO facility and facility ownership we rent for the event, and all local and/or state government authorities as it pertains to proof of COVID-19 vaccination, proof of negative COVID-19 test, social distancing, wearing personal protective equipment, age restrictions, or similar measures (see the SOMA website for more details). If we are unable to hold the SOMA Wild Mushroom Camp, you will receive a refund for event cancellation.

Children under 12 are not allowed to attend Camp.

At this point, we expect the state and/or local guidelines will still require masks to be worn when indoors or in crowded situations.
Generous donors to SOMA Camp 2020
Activities

Mushroom forays, gourmet mushroom cuisine, classes and workshops on mushroom identification, cooking, dyeing, paper-making, medicine making, photography, cultivation, and more. Classes and workshops include

Great Food

And, of course, there will be excellent wild mushroom cuisine. Check out the menu Julie Schreiber created for last year's Sunday feast, and just try not to salivate:

2020 Camp Menu (29 KB)

Also: Recipes from camp published in Gourmet Mushrooms website

Location and Accommodations

The CYO lodge. Photo © Darvin DeShazer.

SOMA Camp is held at CYO Retreat Center, a wonderful modern conference center near Occidental, about an hour north of San Francisco. The spacious, modern buildings are set amongst 225 acres of great mushroom habitat, including mixed oak, redwood, and Douglas-fir forests. Please note that CYO does not permit pets anywhere on their property.

Bunk beds in the CYO Camp cabins. Photo © Darvin DeShazer.

Lodging is in shared, heated, upscale cabins with hardwood floors, designer bunks and personal cubbyholes. There are six bunks per cabin, although all beds are usually not filled. The cabins are bright, clean, and airy. The shared restrooms and showers are, in most cases, a short walk from the cabins. Elders are lodged close to the restroom facilities. Vehicles may be parked near the cabins.

Shared cabins are not suitable for young children, so unless your group is large enough to occupy a cabin by itself (minimum of 8 in the group), please do not register children under 4 years old for onsite accommodation.
Please note that CYO does not allow pets -- no dogs, no cats, not even if you keep them in your vehicle or RV or camper.
Off-site lodging options are also available nearby.
Map to the CYO Camp "
What to Bring

Here's a list of things we suggest you bring to Camp. What Should I Bring?

Work Exchange

To get details on the work exchange program and submit an application, visit the Work Exchange page "

Vendors

Want to sell stuff at SOMA camp?

1. Fill out the Vendor Agreement Form and send it via snail mail, or if you're savvy enough to send by email, see the next step!:
SOMA
P.O. Box 7147
Santa Rosa, CA 95407

2. Please tell the SOMA Camp Director to expect your application via the Contact page.

SOMA Vendor Agreement Form
More Info

For more general camp info, email the SOMA Camp Director

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Sonoma County Mycological Association | SOMA Camp

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SOMA Camp is an annual retreat to learn about wild mushrooms, sponsored by the Sonoma County Mycological Association. The Sonoma County Mycological Association (SOMA) is a non-profit group of professional and amateur mushroom enthusiasts in Northern California dedicated to educating the public about wild mushrooms and their uses.

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Addressing uncertainty: how to conserve and manage rare or little-known fungi

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Addressing uncertainty: how to conserve and manage rare or little-known fungi

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Discusses varying approaches to fungal conservation including providing adaptive management guidelines and strategies for resource managers to conserve fungi based on incrementally improving knowledge from experience and conservation research

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The power of citizen science to advance fungal conservation

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The power of citizen science to advance fungal conservation

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Go community science!

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Visual guide to the identification of rust fungal spore stages

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Fungicolous Fungi, aka fungi that eat fungi!

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Fungicolous Fungi, aka fungi that eat fungi!

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Abstract

The plant microbiome has proven to be an essential and often overlooked aspect of plant physiological ecology. Plant interactions with microbes are thought to have enabled the transition of plants from aquatic to terrestrial systems, thus co-evolving for millions of years. Consequently, microbes have important consequences for plant performance, nutrient cycling, and potentially even plant species ranges. However, our knowledge of these processes derives from only a few model systems. My dissertation explores these relationships in coast redwood forests where, despite their notoriety, plant-microbial relationships remain unexplored. Redwoods are the largest and some of the oldest plants on Earth, yet their geographical ranges are very constrained. As such, redwood forests serve as an excellent system to explore plant-microbial interactions and how they might expand or limit species ranges.

In Chapter 1, I demonstrate two unexpected and important findings related to the redwood root mycobiome. First, I show for the first time that, in addition to its expected association with arbuscular-mycorrhizal fungi (AMF), redwood roots are also associated with with ecto- and ericoid mycorrhizal fungi. To our knowledge, this is the first evidence that this predominantly AMF-associated tree is also colonized by the other two primary types of mycorrhizal fungi. These findings challenge the common practice of AMF-specific sequencing methods and the paradigm that plant species are assumed to associate with only one type of mycorrhizal fungi. This is important because it may link this tree species to the surrounding trees and shrubs that co-occur in these habitats. Secondly, I describe unique structures, which I call "rhizonodes", that show many parallels in microbial community assembly to well-described nodules in N-fixing plants where rhizonodes act as reservoirs of AMF in the redwood roots. The presence of rhizonodes similarly are a unique finding that seem to occur in other predominantly AMF-associated tree species, but have been widely overlooked. We posit that these structures may be important domiciles for AMF in many of the upwards of 80% of plant species predicted to form relationships with this group. These findings also suggest that arbuscular mycorrhizal fungi (AMF) may play key roles in redwood physiology.

In Chapter 2, I focus on redwood association with AMF and the functional consequences of these interactions for plant hosts. I found that mycorrhization of coast redwood proceeds a number of downstream consequences for redwood hosts including in morphology, growth, allocation, hormonal physiology, drought-response, and leaf-level physiology. In addition, I found that mycorrhizal seedlings demonstrate progressively higher rates of photosynthesis compared to non-mycorrhizal seedlings in response to rising CO2. Together, these findings indicate that mycorrhizal fungi are likely to become increasingly important more broadly for plant response to climate change.

In Chapter 3, I demonstrate the importance of site-specific water-availability on the root-associated bacterial community in redwood. Previous work on crop plants has shown that artificial drought selects for monoderm bacteria, or bacterial taxa with a single, thick cell-wall layer. I present evidence of similar trends for a long-lived tree species in response to local water-availability. While the consequences of interactions with these types of bacteria remain unknown, as increased intensity and severity of drought are predicted as a result of climate change, I highlight the importance of testing the downstream consequences of monoderm versus diderm dominated bacterial communities on plant physiology, nutrient cycling, and ecosystem function.

Taken together, these studies suggest that the root microbiome is an important axis in understanding the response of redwood forest to climatic and environmental change predicted in the Anthropocene. Further, our study of a basal gymnosperm highlights important gaps in our understanding and categorization of plant-microbe interactions and emphasizes the importance of future investigations on non-model plant organisms.

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The Redwood Microbiome: Microbial community composition and functional consequences of plant-microbe interactions for the tallest species on Earth

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Author(s): Willing, Claire | Advisor(s): Dawson, Todd | Abstract: The plant microbiome has proven to be an essential and often overlooked aspect of plant physiological ecology. Plant interactions with microbes are thought to have enabled the transition of plants from aquatic to terrestrial systems, thus co-evolving for millions of years.

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Where the ‘Wood-Wide Web’ Narrative Went Wrong

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Where the ‘Wood-Wide Web’ Narrative Went Wrong

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A compelling story about how forest fungal networks communicate has garnered much public interest. Is any of it true?

Read the full publication here: https://www.nature.com/articles/s41559-023-01986-1

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O ver the past few years, a fascinating narrative about forests and fungi has captured the public imagination. It holds that the roots of neighboring trees can be connected by fungal filaments, forming massive underground networks that can span entire forests - a so-called wood-wide web. Through this web, the story goes, trees share carbon, water, and other nutrients, and even send chemical warnings of dangers such as insect attacks. The narrative - recounted in books, podcasts, TV series, documentaries, and news articles - has prompted some experts to rethink not only forest management but the relationships between self-interest and altruism in human society.

But is any of it true?

The three of us have studied forest fungi for our whole careers, and even we were surprised by some of the more extraordinary claims surfacing in the media about the wood-wide web. Thinking we had missed something, we thoroughly reviewed 26 field studies, including several of our own, that looked at the role fungal networks play in resource transfer in forests. What we found shows how easily confirmation bias, unchecked claims, and credulous news reporting can, over time, distort research findings beyond recognition. It should serve as a cautionary tale for scientists and journalists alike.

First, let's be clear: Fungi do grow inside and on tree roots, forming a symbiosis called a mycorrhiza, or fungus-root. Mycorrhizae are essential for the normal growth of trees. Among other things, the fungi can take up from the soil, and transfer to the tree, nutrients that roots could not otherwise access. In return, fungi receive from the roots sugars they need to grow.

As fungal filaments spread out through forest soil, they will often, at least temporarily, physically connect the roots of two neighboring trees. The resulting system of interconnected tree roots is called a common mycorrhizal network, or CMN.

When people speak of the wood-wide web, they are generally referring to CMNs. But there's very little that scientists can say with certainty about how, and to what extent, trees interact via CMNs. Unfortunately, that hasn't prevented the emergence of wildly speculative claims, often with little or no experimental evidence to back them up.

One common assertion is that seedlings benefit from being connected to mature trees via CMNs. However, across the 28 experiments that directly tackled that question, the answer varied depending on the trees' species, and on when, where, and in what type of soil the seedling is planted. In other words, there is no consensus. Allowed to form CMNs with larger trees, some seedlings seem to perform better, others worse, and still others seem to behave no differently at all. Field experiments designed to allow roots of trees and seedlings to intermingle - as they would in natural forest conditions - cast still more doubt on the seedling hypothesis: In only 18 percent of those studies were the positive effects of CMNs strong enough to overcome the negative effects of root interactions. To say that seedlings generally grow or survive better when connected to CMNs is to make a generalization that simply isn't supported by the published research.

Other widely reported claims - that trees use CMNs to signal danger, to recognize offspring, or to share nutrients with other trees - are based on similarly thin or misinterpreted evidence.How did such a weakly sourced narrative take such a strong grip on the public imagination?

We scientists shoulder some of the blame. We're human. Years ago, when the early experiments were being done on forest fungi, some of us - the authors of this essay included - simply got caught up in the excitement of a new idea.

One of us (Jones) was involved in the first major field study on CMNs, published more than 25 years ago. That study found evidence of net carbon transfer between seedlings of two different species, and it posited that most of the carbon was transported through CMNs, while downplaying other possible explanations. This is what's known as "confirmation bias," and it is an easy trap to fall into. As hard as it is to admit, it was only due to our skepticism of the recent extraordinary claims about the wood-wide web that we looked back and saw the bias in our own work.

Over decades, these and other distortions have propagated in the academic literature on CMNs, steering the scientific discourse further and further away from reality, similar to a game of "telephone." In our review, we found that the results of older, influential field studies of CMNs have been increasingly misrepresented by the newer papers that cite them. Among peer reviewed papers published in 2022, fewer than half the statements made about the original field studies could be considered accurate. A 2009 study that used genetic techniques to map the distribution of mycorrhizal fungi, for instance, is now frequently cited as evidence that trees transfer nutrients to one another through CMNs - even though that study did not actually investigate nutrient transfer. In addition, alternative hypotheses provided by the original authors were typically not mentioned in the newer studies.

As these biases have spilled over into the media, the narrative has caught fire. And no wonder: If scientists themselves could be seduced by potentially sensational findings, it is not surprising that the media could too.

Journalists told emotional, persuasive, and seductive stories about the wood-wide web, amplifying the speculations of a few scientists through powerful storytelling. Writers imbued trees with human qualities, portraying them as conscious actors using fungi to serve their needs. Fantasy moved to the foreground, facts to the back. In an odd kind of mutual reinforcement, the media blitz may have convinced experts in other subfields of ecology that the claims about CMNs were well-founded.

The episode underscores how important it is for journalists to seek out a broad range of expert opinions, and to challenge us scientists when our assertions aren't clearly backed up by rigorous research. By directly asking scientists questions such as "What other phenomena could explain your results?" and "How many other studies support this hypothesis?" journalists may be able to better understand and convey some of the uncertainty around scientific conclusions. The best science writing can capture the hearts and minds of the public, but it must be true to the evidence and the scientific process. If not, the consequences can be far-reaching, affecting policy decisions that impact real people.

There are many captivating and scientifically well-grounded stories we can tell about fungi in forests - and we should. Mycorrhizal fungi underlie many of our favorite edible mushrooms, including truffles, chanterelles, and porcinis. And some herbs in the understories of forests, rather than photosynthesizing sugars like a normal plant, use CMNs to connect to trees and steal their sugars. Forests are fascinating places, marked by a rich diversity of interactions between plants, animals, and microbes. The stories are endless. We just have to tell them with care.

Melanie Jones is a professor in the Biology Department at the University of British Columbia's Okanagan campus. She and her students have been studying mycorrhizal fungal communities in forests, clearcuts, and wildfire sites in British Columbia for 35 years.

Jason Hoeksema is a professor in the Department of Biology at the University of Mississippi. His research addresses a diversity of questions regarding the ecological and evolutionary consequences of species interactions on populations, communities, and ecosystems.

Justine Karst is an associate professor in the Department of Renewable Resources at the University of Alberta. She has been studying the mycorrhizal ecology of forests for 20 years.

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Where the 'Wood-Wide Web' Narrative Went Wrong

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Opinion | A fascinating story about forest fungal networks has captured the public imagination in recent years. Is any of it true?

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Learn about mycorrhizal symbioses from Dr. Laura Bogar!

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Learn about mycorrhizal symbioses from Dr. Laura Bogar!

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Laura Bogar - Symbiotic systems: understanding cooperation between tree roots and soil fungi across scale

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The Recovery of Soil Fungi Following a Fire

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The Recovery of Soil Fungi Following a Fire

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The need and opportunities for including fungi in biodiversity databases and conservation activities  

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The need and opportunities for including fungi in biodiversity databases and conservation activities  

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Greg Mueller on Fungal Conservation at NatureServe BWB 2021

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Greg Mueller on Fungal Conservation at NatureServe BWB 2021

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An exploration into the degradation of lignin by fungi

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Mushroom Bioregions of the United States - Christian Schwarz

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Mycological Association of Washington DC

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Mushroom Bioregions of the United States - Christian Schwarz

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Re-examining the evidence for the mother tree hypothesis – resource sharing among trees via ectomycorrhizal networks

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Re-examining the evidence for the mother tree hypothesis – resource sharing among trees via ectomycorrhizal networks

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Seminal scientific papers positing that mycorrhizal fungal networks can distribute carbon (C) among plants have stimulated a popular narrative that overstory trees, or ‘mother trees’, support the growth of seedlings in this way. This narrative has far-reaching implications for our understanding of forest ecology and has been controversial in the scientific community.

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The emergence and coalescence of fungal conservation social networks in Europe and the U.S.A.

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The emergence and coalescence of fungal conservation social networks in Europe and the U.S.A.

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Fungal Conservation Issues and Solutions

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Fungal Conservation Issues and Solutions

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A SPECIAL VOLUME OF
THE BRITISH MYCOLOGICAL SOCIETY

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Developing a comprehensive strategy for fungal conservation in Europe: current status and future needs

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Developing a comprehensive strategy for fungal conservation in Europe: current status and future needs

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Delimitation of Funga as a valid term for the diversity of fungal communities: the Fauna, Flora & Funga proposal (FF&F)

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Delimitation of Funga as a valid term for the diversity of fungal communities: the Fauna, Flora & Funga proposal (FF&F)

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Flora, fauna and FUNGA!!!

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Recognition of the discipline of conservation mycology 

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Recognition of the discipline of conservation mycology 

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A way forward for wild fungi in international sustainability policy

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A way forward for wild fungi in international sustainability policy

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A Field Guide to the Rare Fungi of California’s National Forests

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A Field Guide to the Rare Fungi of California’s National Forests

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Molecules. 2021 May; 26(10): 2948.

Henry Lowe, 1, 2, 3, ⁴ Ngeh Toyang, 2, ³ Blair Steele, 1,* Henkel Valentine, ¹ Justin Grant, 1, ⁵ Amza Ali, 1, ⁵ Wilfred Ngwa, ⁶ and Lorenzo Gordon ⁷

Raffaele Capasso, Academic Editor

Abstract

The psychedelic effects of some plants and fungi have been known and deliberately exploited by humans for thousands of years. Fungi, particularly mushrooms, are the principal source of naturally occurring psychedelics. The mushroom extract, psilocybin has historically been used as a psychedelic agent for religious and spiritual ceremonies, as well as a therapeutic option for neuropsychiatric conditions. Psychedelic use was largely associated with the "hippie" counterculture movement, which, in turn, resulted in a growing, and still lingering, negative stigmatization for psychedelics. As a result, in 1970, the U.S. government rescheduled psychedelics as Schedule 1 drugs, ultimately ending scientific research on psychedelics. This prohibition on psychedelic drug research significantly delayed advances in medical knowledge on the therapeutic uses of agents such as psilocybin. A 2004 pilot study from the University of California, Los Angeles, exploring the potential of psilocybin treatment in patients with advanced-stage cancer managed to reignite interest and significantly renewed efforts in psilocybin research, heralding a new age in exploration for psychedelic therapy. Since then, significant advances have been made in characterizing the chemical properties of psilocybin as well as its therapeutic uses. This review will explore the potential of psilocybin in the treatment of neuropsychiatry-related conditions, examining recent advances as well as current research. This is not a systematic review.

Keywords: magic mushrooms, psilocybin, psychedelic, neuropharmaceuticals, neurotherapeutics, addiction, anxiety, depression, cancer, psychopharmacology

1. Introduction

The word "psychedelic" ( psyche (i.e., the mind or soul) and delos (i.e., to show)) has Greek origin and was first coined by psychiatrist Humphry Osmond in 1956 [ 1, 2], who had been conducting research on lysergic acid diethylamide (LSD) at the time. Psychedelics are a class of hallucinogenic drugs ("hallucinogens") that produce mind-altering and reality-distorting effects, known as hallucinations, once ingested. Hallucinations typically trigger delusions, emotional swings, feelings of detachment and derealization. Hallucinogens are generally classified into two main categories, (1) dissociative drugs, such as dextromethorphan (DXM), ketamine Salvia divinorum and Phencyclidine (PCP) [ 3, 4] and (2) classic serotonergic and dopaminergic hallucinogens that interact with serotonin and dopamine receptors, respectively.

Classes of classic serotonergic and dopaminergic hallucinogens include (1) Lysergamides (amides of lysergic acid)-LSD/LAD, and ergotamine, (2) Phenethylamines such as MDMA (ecstasy), MDMA-like drugs such as p-methoxy methamphetamine (PMMA), mescaline and mescaline-derived compounds like TMA, DOM, DOET, DOI (2,5-dimethoxy-4-iodoamphetamine), and DOC (2,5-dimethoxy-4-chloroamphetamine), and (3) Tryptamines such as N,N-dimethyltryptamine (DMT) and its derivatives alpha-methyltryptamine (AMT), 5-methoxy-N,N-dimethyltryptamine (5-MeO-DMT) and 5-methoxy-N,N-diisopropyltryptamine (5-MeO-DIPT), and psilocin (4-hydroxy-N,N-dimethyltryptamine also known as 4-OH-DMT) and psilocybin ([3-(2-Dimethylaminoethyl)-1 H-indol-4-yl] dihydrogen phosphate. In addition to psilocin, other metabolites of psilocybin include; (1) 4-hydroxyindole-3-yl-acetaldehyde (4H1A), (2) 4-hydroxyindole-3-yl-acetic-acid (41-IIAA), and (3) 4-hydroxytryptophol (41-IT) [ 5]. On the same tangent, psilocybin, lysergic acid diethylamide, and lysergic acid amide are classified as indoleamine hallucinogens [ 6].

Classic psychedelic (serotonergic) drugs interact with the serotonin receptors (5-HT/5-hydroxytryptamine receptors) and their subtypes densely located within the brain [ 7, 8, 9]. These receptors mediate emotions and moods such as anxiety and aggression, cognition, sex, learning memory, appetite along with other biological, neurological and neuropsychiatric processes [ 8, 10]. These 5-HT receptors are also located in the central and peripheral nervous systems [ 11, 12]. Serotonin receptors are the target of multiple recreational and pharmaceutical drugs such as hallucinogens, empathogens, antipsychotics, antidepressants, antiemetics, antimigraine agents and anorectics [ 10]. Figure 1 shows the chemical structures of classic psychedelic drugs and the neurotransmitter serotonin.

Of all psychedelic drugs, psilocybin is reported to have the most favorable safety profile [ 13]. Despite the lack of studies investigating the comparative efficacies of psilocybin and psychedelic drugs for the treatment of mood and anxiety disorders, the vast evidence-based data that exist for psilocybin alone suggest that psilocybin may be the most efficacious psychedelic drug for treating such disorders.

In a 2017 Global Drug Survey, it is estimated that approximately 20.6% of people worldwide who used drugs of any type, selectively used magic mushrooms within their lifetime up to that year [ 14]. This review will focus on psilocybin, the main psychoactive component of magic mushrooms (psilocybin-producing mushrooms), that has been utilized for thousands of years in mushroom-worshiping ceremonies in old-world cultures [ 15, 16]. In addition to the known recreational, spiritual, and religious uses of magic mushrooms, there is significant medicinal value, as evidenced by anecdotal reports and scientific studies. Table 1 below lists the diseased states in which psilocybin-assisted therapy is being explored.

Table 1

Diseased State/Condition

Reference

4.

Tobacco addiction

[ 25, 28, 29, 30]

8.

Anxiety disorders such as:

1. Post-traumatic stress disorder (PTSD),

2. Generalized anxiety disorder (GAD),

3. Obsessive-compulsive disorder (OCD)

4. Advanced-stage cancer-related anxiety

5. Psychological distress associated with existential crisis of terminal disease

6. Adjustment disorder with anxiety

[ 26]

[ 26]

[ 31, 32]

[ 33, 34, 35, 36, 37]

[ 26]

[ 26, 38]

9.

Cancer-related depression

[ 33, 34, 35, 36, 37, 39]

10.

Treatment-resistant depression

[ 40, 41, 42, 43, 44]

Mental health and substance-use disorders such as depression, anxiety-related disorders, bipolar disorder, autism, psychoses such as schizophrenia, and substance-dependence disorders are of significant global burden [ 17, 18]. Up to 2020, it is estimated that 1 billion people may be affected by a mental health or substance disorder [ 19]. Anxiety-related disorders were the most burdensome mental health disorders in 2018, affecting an estimated 284 million people [ 20], while depression, the second-most common-affected an estimated 264 million people globally the same year [ 19, 20]. Additionally, in 2018, alcohol-use disorder affected an estimated 107 million people globally, while drug use disorder (excluding alcohol) affected 71 million people globally [ 20]. Suicidality, which also correlates to mental health, is also of global burden. Statistics show that an estimated 800,000 people commit suicide annually [ 21]. With the COVID-19 pandemic, risk factors for mental health and substance-use disorders are expected to be exacerbated, with evidence of increased rates of anxiety, depression and distress [ 22].

With the increase in the rate of mental disorders globally, now exacerbated by COVID-19, psychedelic-assisted psychotherapies, particularly psilocybin-assisted psychotherapies, may alleviate some of the challenges that face conventional psychiatric medicine.

In addition to having the potential to treat mood and anxiety disorders, psilocybin has also demonstrated analgesic effects as evidenced by numerous clinical studies on the treatment of cluster ("suicide") headaches [ 6, 47], intractable phantom-limb pain (PLP) [ 51], and chronic pain [ 48]. One possible mechanism of action of this analgesic property is via interaction with nociceptive and antinociceptive pathways [ 48]. In some cases, psilocybin was comparable to or more efficacious than traditional medications such as opioid analgesics [ 6, 50].

A study by Nkadimeng and colleagues report dose-dependent analgesic, antioxidant, and anti-inflammatory properties of a certain Psilocybe natalensis species of magic mushroom [ 49]. Lipopolysaccharide (LPS)-stimulated macrophage cells were treated with three different 24-h extracts (hot water, cold water and ethanol) of Psilocybe natalensis mushrooms [ 49]. Antioxidant effects of Psilocybe natalensis mushrooms were confirmed when all three extracts inhibited lipopolysaccharide-induced nitric oxide [ 49]. Anti-inflammatory effects of Psilocybe natalensis mushrooms were confirmed upon the inhibition of prostaglandin E ₂, and interleukin 1β cytokine [ 49].

1.1. History

Despite thousands of years of psychedelic use in religion and recreation, the earliest known written record of magic mushroom use in the Florentine Codex (a manuscript of ethno-graphical research of Mesoamerica, particularly of Mexico and the Aztecs, compiled between 1529 and 1579 [ 10, 15, 63, 65]

Classic psychedelic compounds like psilocybin, mescaline (isolated from the peyote cactus in 1897 by Arthur Heffter) [ 66] and dimethyltryptamine have been used in religious ceremonies in indigenous societies in South and Central America for centuries [ 66, 67, 68, 69, 70, 71].

Nine years later, in 1947, Sandoz began marketing and distributing LSD as a psychiatric drug for the treatment of neurosis [ 73], alcoholism [ 74, 75, 76, 77, 78, 79, 80, 81], criminal behaviour [ 82, 83, 84], schizophrenia [ 85, 86, 87, 88, 89], and sexual perversions [ 90]. LSD-25 was also used to treat autism [ 91, 92], and verbal behaviour [ 93].

In 1957, Hofmann received a sample of dried Psilocybe mexicana mushrooms from a mycologist in Huautla de Jiménez in Oaxaca, Mexico [ 65]. This could be considered the beginning of the "second psychedelic renaissance". To identify and convince himself of the mushroom's bioactivity, Hoffman used paper chromatography to separate the various components of whole extracts of mushrooms, by ingesting each separated fraction [ 65]. The active fraction was then chemically characterized, crystallized and called psilocybin [ 65, 94]. Hofmann and colleagues subsequently elucidated the structure and synthesis of psilocybin in 1958 [ 5, 94, 95, 96] and a minor component of the extract, psilocin, a dephosphorylated form of psilocybin [ 65]. In the 1960s, Sandoz Pharmaceuticals (Basel, Switzerland) distributed Indocybin TM, a psychotherapeutic drug, in pill form, containing 2 mg psilocybin [ 65]. This period also saw experimental therapeutics with psilocybin as a probe for brain function [ 2], psilocybin for recidivism [ 97] and with psilocybin as an entheogen in religious people (divinity students) [ 98].

From the 1960s and 1970s, recreational use of psychedelics became central to the "hippie", counterculture in the United States, and this ultimately fueled the United States Drug Enforcement Agency to prohibit psychotropic substances such as LSD, DMT ( N, N-Dimethyltryptamine), Psilocybin and Mescaline, and label them as Schedule 1 drugs under the Controlled Substances Act 1970 (USA). As a result of this historical association with the highly sensationalized "hippie", counterculture at the time, there has been lingering stigmatization of such substances, which has, in turn, hindered scientific research and innovation in psychedelic therapeutics [ 13], until recently.

1.2. Transition to Modern-Day Clinical Studies

Traditionally, the pharmaceutical industry, in reflection of societal understanding and governmental acceptance, rejected psychedelic research for a long time. Only recently has psychedelic research slowly made its reintroduction back into the paradigm of modern science and many clinical studies confirm the potential of psilocybin-assisted therapy as a promising adjunct to psychotherapy [ 15, 99].

Early clinical studies with hallucinogens report the use of LSD-25 to treat the typical intractable behaviour seen in early infantile autism and childhood schizophrenia [ 88, 91, 100]. By the 1960s, over 40,000 individuals took part in psychedelic research studies, albeit with less rigorous clinical standards [ 101].

Amidst this renewed interest in psychedelic research, pharmaceutical interest has also increased. In 2018 Compass Pathways Ltd. (London, UK) received U.S. Food and Drug Administration (USFDA) approval of "breakthrough therapy" status for a psilocybin treatment they developed for treatment-resistant depression [ 104]. In the same year, the USFDA also approved SPRAVATO ®, a ketamine analog developed by Johnson and Johnson for use in patients suffering from treatment-resistant depression [ 105]. In 2019, Usona Institute received USFDA "breakthrough therapy" status for a psilocybin treatment for major depressive disorder (MDD) [ 106].

Refer to Figure 2 for the historical timeline of psychedelic drugs and Figure 3 a-m for examples of magic mushrooms (psilocybin-producing mushrooms). Over 100 species of mushrooms of the genus Psilocybe produce psilocybin [ 2, 107].

The John Hopkins Psychedelic Research Unit claims recognition for being the first to research psilocybin since the 1970s [ 108]. Between 2015 and 2020, nearly 550 grants have been awarded to research institutes engaged in psychedelic research [ 109]. In modern-day research, the majority of classic psychedelic neurotherapeutics research is focused on psilocybin's potential in mood and anxiety disorders such as cancer-related psychiatric distress [ 2]. Table 2 below lists major institutes and organizations involved in psychedelic research.

Table 2

Institute or Organization

Some Publications/Areas of Study/Clinical Trials

References to Psilocybin Studies.

1.

Center for Psychedelic and Consciousness Research (John Hopkins University, USA)
Founded in 2019.

1. Psilocybin can occasion mystical experiences having substantial and sustained personal meaning and spiritual significance.

2. Survey of subjective "God encounter experiences": Comparisons among naturally occurring experiences and those occasioned by the classic psychedelics; psilocybin, LSD, ayahuasca, or DMT

3. Effects of psilocybin-assisted therapy for major depressive disorder: A randomized clinical trial.

4. Psilocybin acutely alters the functional connectivity of the claustrum with brain networks that support perception, memory, and attention.

5. Subjective features of the psilocybin experience that may account for its self-administration by humans: a double-blind comparison of psilocybin and dextromethorphan.

6. Optimal dosing for psilocybin pharmacotherapy: Considering weight-adjusted and fixed dosing approaches.

[ 45, 103, 108, 110, 111, 112, 113, 114, 115]

5.

Cybin, Corp.
(Toronto, ON, Canada)Founded in 2019.

1. A psilocybin drug targeting MDD (in phase 2a and phase 2b of clinical trial).

2. A phase 2 clinical trial investigating the delivery of psilocybin through an oral film.

3. A study into a transdermal, "slow-dose" psilocybin delivery mechanism.

4. A study on clinical safety and efficacy of targeting micro-dosing anxiety, ADHD and overall cognitive flexibility.

6.

Multidisciplinary Association for Psychedelic Studies (MAPS).
Founded in 1986.

v. Positron emission tomography and fluorodeoxyglucose studies of metabolic hyper-frontality and psychopathology in the psilocybin model of psychosis.

vi. Neurometabolic effects of psilocybin, 3,4-methylenedioxyethyl-amphetamine (MDE) and d-methamphetamine in healthy volunteers. A double-blind, placebo-controlled PET study with [18F] FDG.

vii. The pharmacology of psilocybin.

viii. Acute psychological and physiological effects of psilocybin in healthy humans: a double-blind, placebo-controlled dose-effect study.

1. Psilocybin can occasion mystical-type experiences having substantial and sustained personal meaning and spiritual significance

2. Response of cluster headache to psilocybin and LSD.

3. Psilocybin links binocular rivalry switch rate to attention and subjective arousal levels in humans.

4. Mystical-type experiences occasioned by psilocybin mediate the attribution of personal meaning and spiritual significance 14 months later

5. Novel psychopharmaceutical therapies for psychiatric disorders: psilocybin and MDMA

[ 5, 47, 68, 108, 117, 118, 119, 120, 121, 122]

7.

Harvard Psilocybin Project
(Department of Psychology at Harvard University, USA).

1. Harvard-Concord Prison Experiment (1961-1963) studying the effects of psilocybin-assisted psychotherapy on rates of recidivism and the effects of consciousness-expanding drugs on prisoner rehabilitation.

2. Reactions to psilocybin administered in a supportive environment.

3. A new behavior change program using psilocybin.

8.

Heffter Research Institute (founded and Incorporated in New Mexico, USA 1993).

1. Pilot study of the 5-HT2AR agonist psilocybin in the treatment of tobacco addiction.

2. Psilocybin-assisted treatment for alcohol dependence: a proof-of-concept study.

3. Rapid and sustained symptom reduction following psilocybin treatment for anxiety and depression in patients with life-threatening cancer: a randomized controlled trial.

4. Psilocybin-assisted group therapy for demoralized older long-term AIDS survivor men: An open-label safety and feasibility pilot study

5. Safety, tolerability and efficacy of psilocybin in 9 patients with Obsessive-Compulsive Disorder.

[ 23, 28, 32, 35, 53]

10.

Department of Psychiatry (Yale University, USA).

1. The role of psychedelics in palliative care reconsidered: A case for psilocybin

2. The Yale Manual for Psilocybin-Assisted Therapy of Depression (using Acceptance and Commitment Therapy as a Therapeutic Frame)

3. Clinical trial: Psilocybin for the Treatment of Cluster Headache; Safety and Efficacy of Psilocybin for the Treatment of Headache Disorders

4. Psilocybin-Induced Neuroplasticity in the Treatment of Major Depressive Disorder.

[ 124, 125, 126, 127]

11.

Canadian Centre for Psychedelic Science.

1. Micro-dosing as a response to the meaning crisis: a qualitative analysis.

2. Micro-dosing Psychedelics: Subjective Benefits and Challenges, Substance Testing Behavior, and the Relevance of Intention.

[ 128, 129]

2. Examples of Psilocybin Producing Mushrooms

Psilocybin is produced by many species of mushrooms that are distributed globally [ 5]. These include countries such as the USA, S.E. Asia, Europe Mexico and Central America [ 15, 16, 65]. The Psilocybe cubensis mushroom is the most widespread species of the Psilocybe genus [ 15, 16, 63].

3. Psilocybin Synthesis

Psilocybin may be synthesized in a number of ways. Figure 4 is one example of how psilocybin may be converted from L-tryptophan. In humans, psilocybin is rapidly dephosphorylated to psilocin (4-hydroxy- N,N-dimethyltryptamine) by alkaline phosphatase in the liver [ 65, 142] and nonspecific esterase in the intestinal mucosa [ 143]. In rodents, psilocybin is completely converted to psilocin before it enters systemic circulation [ 5] ( Figure 5 ). It is psilocin that is the main pharmacologically active substance in magic mushrooms, not psilocybin [ 5, 144], despite the common conception that it is psilocybin that produces the psychotomimetic effects. Psilocybin is considered a prodrug to psilocin [ 145].

3.1. Production of Synthetic Psilocybin

As a result of the increased need for psilocybin in recent years, due to renewed research focus, the market demands have to be met through synthetic psilocybin production [ 146]. Even though there is interest in the extraction of psilocybin from naturally growing or cultivated mushrooms, the psilocybin yield obtained (0.1-0.2% of dry weight) is not economically viable for drug research and development, and such may be limited to just recreational uses [ 143]. The observed variations in batches of psilocybin extracted from different sources further complicate the dependence on psilocybin directly extracted from mushrooms [ 146].

The bioengineering of psilocybin has also been explored, which successfully can significantly reduce chemical synthetic costs through the production of psilocybin from cheaper start-up materials such as glucose. Following the elucidation of the biosynthetic pathway for the production of psilocybin in P. Cubensis in 2017 [ 151], bioengineering has led to the production of psilocybin in the filamentous fungi Aspergillus nidulans, with yields of up to 1.16 g/L [ 152]. Other methodologies have since been developed with an increased titer of 1.16 g/L, relying on the in vivo bioconversion of substrates 4-hydroxyindole, serine and methionine by Escherichia coli ( E. coli) [ 153]. This method is currently not scalable as it relies on expensive startup substrates which can be used to produce psilocybin in cheaper chemical synthesis methodologies. A methodology for de novo production of psilocybin and tryptamine derivatives in Saccharomyces cerevisiae, utilizing knowledge of the psilocybin biosynthetic pathway elucidated in P. cubensis [ 154]. The pathway is supplemented with a novel cytochrome P450 reductase enzyme resulting in improved yields of 627 ± 140 mg/L of psilocybin and 580 ± 276 mg/L of psilocyn [ 154].

The production of psilocybin and psilocyn from S. cerevisiae is a significant achievement in developing cheaper psilocybin synthesis methodologies. Given the extensive use of S. cerevisiae industrially, as well as limited tryptophan derivatives produce, S. cerevisiae use for psilocybin production can significantly improve consistency in titer as well as optimize downstream processing [ 155].

Continuous research is needed nonetheless for the optimization of psilocybin synthesis. Given the upward trend in psilocybin research in recent years, the industry can only further benefit from optimized synthesis methodologies.

3.2. Mechanism of Action of Psilocybin

Psilocin reacts agonistically with serotonin (5-hydroxytryptamine) type 2A (5-HT 2A) receptors to produce a "mystical-like" hallucinatory effect [ 5, 99] ( Figure 5 ) due to induced frontal hyper-frontality [ 5], which in turn mediates its anti-depressant and anti-anxiety effects [ 15, 68]. One possible anti-depressant mechanism of action of psilocybin is via deactivation or normalization of the hyperactivity of the medial prefrontal cortex (mPFC) [ 156, 157, 158]. During depression, the mPFC is typically hyperactive [ 159].

Anti-depressant properties of psilocybin are mediated via modulation of the prefrontal and limbic brain regions, with the inclusion of the amygdala [ 160]. The amygdala plays an essential role in perception and emotion-processing networks [ 158]. In cases of depression, an individual typically loses responsiveness to emotional stimuli [ 44]. On the same tangent, it is also suggested that the hyper-frontal metabolic pattern produced after psilocybin administration and 5-HT 2A receptor activation is comparable to metabolic patterns produced in acute psychotic episodes in chronic schizophrenics [ 65].

It is also reported that psilocybin binds with high affinity to the 5-HT 2A serotonergic receptor subtype, but with low affinity to the 5-HT 1A serotonergic receptor subtype [ 5]. The interaction of psilocybin and psilocin with 5-HT 2A receptors to produce psychotomimetic effects has been confirmed in experiments with ketanserin, a 5-HT 2A antagonist that attenuates the effects of psilocybin [ 5, 72]. In addition to interaction with 5-HT 2A receptors, it is also suggested that the psychopharmacological action of psilocybin may also be mediated by non-5HT2 receptors [ 7, 143, 158]. Psilocybin and psilocin also interact with the 5-HT 1D and 5-HT 2C receptor subtypes [ 5].

Psilocybin is reported to result in significant changes in brain dynamics and functional connectivity (FC) between areas of the brain [ 160, 161, 162, 163]. Psilocybin-induced alteration in brain connectivity involves the disintegration of associative networks and integration of sensory function networks [ 65]. It is suggested that this dissociation may mediate the subjective effects of psilocybin use and a state of unconstrained cognition [ 65]. On the same tangent, a possible mechanism of action behind psilocybin's psychotomimetic effects are via interactions with feedback loops between the cortex and thalamus [ 5]. Psilocybin administration produces general cortical activation [ 65]. This is confirmed by increased levels of the cerebral metabolic rate of glucose (CMRglu) in the prefrontal cortex, anterior cingulate, temporal cortex, and putamen [ 63]. This increase is positively correlated with hallucinatory "ego dissolution" [ 65]. The metabolic rate of glucose (MRGlu) also increased in distinct right-hemispheric frontotemporal cortical regions [ 118].

Serotonin 5-HT 2A receptors are distributed in multiple areas of the brain that play a role in psychosis and psychotic symptoms, such as the cerebral cortex (prefrontal cortex) and periphery [ 72], striatum, ventral tegmental area, and thalamus [ 164].

It is also hypothesized that schizophrenia (and possibly other mood and anxiety disorders) is characterized by dysregulation/disbalance of serotonin and dopamine [ 168]. In acute psychoses, one study even concludes that 5-HT 2A and 5-HT 1A serotonergic receptors play an important role in the modulation of striatal dopamine release. This suggests that psilocybin may have significant potential in the treatment of schizophrenia and possibly other psychiatric disorders [ 168]. In another study, psilocybin was indirectly responsible for an increase in endogenous dopamine via a decrease in 11C-raclopride binding potential bilaterally in the caudate nucleus (19%) and putamen (20%) [ 169].

A 2021 study by Grandjean and colleagues investigated the effects of psilocybin on functional connectivity (FC) across the entire brain region in mice [ 170]. One possible mechanism of action by which psilocybin produces anti-depressant effects is via interaction with/alteration of the default-mode network (DMN) [ 171]. Using resting-state fMRI, psilocybin was shown to decrease functional connectivity within dopamine (DA)-associated striatal networks, in addition to demonstrating alteration (increase) of FC between 5-HT-associated networks and cortical areas [ 170]. This study confirms the interaction of psilocybin with the mesolimbic dopaminergic pathway to produce neural and psychological effects [ 170]. Data presented in another murine study suggest that psilocin, an active metabolite of psilocybin, has been shown to increase the concentrations of both extracellular dopamine and 5-HT in the mesoaccumbens and/or mesocortical pathway [ 172]. This presents yet another possible mechanism of anti-depressant action of psilocybin/psilocin, that is, the ability to increase dopamine, a neurotransmitter that is responsible for the regulation of emotions and even an individual's physical well-being [ 173]. On the same tangent, concentrations of both extracellular dopamine and 5-HT in the ventral tegmental area (VTA) were not affected [ 172]. This further suggests that, in addition to the ventral tegmental area (VTA), the brain's reward circuity may also be influenced by other regions of the brain.

5-HT 2A activation and subsequent activation of postsynaptic α-amino- ٣-hydroxy- ٥-methyl- ٤-isoxazole propionic acid (AMPA) receptors by psilocybin is associated with increased glutamate concentration. Glutamate is responsible for normal, healthy brain functioning [ 174].

Psilocybin treatment, in some cases with psychological support, also resulted in increased responsiveness to positive emotional stimuli in the right amygdala [ 44, 175] and decreased/normalization of responsiveness to negative or neutral emotional stimuli [ 112, 158, 176, 177, 178, 179]. Psilocybin was also shown to attenuate amygdala activation in response to threat-related visual stimuli [ 177] and reduced threat-induced modulation of the primary visual cortex by the amygdala [ 177]. The amygdala modulates the primary visual cortex via top-down connectivity [ 177].

Barrett and colleagues also suggest that psilocybin may even influence brain plasticity as confirmed by the persisting positive effect and increased amygdala response to positive emotional stimuli up to one month post psilocybin treatment [ 112].

Another fMRI study [ 181] reports a decreased functional connectivity between the amygdala and the ventromedial prefrontal cortex (vmPFC) in response to fearful and neutral (but not happy) faces after psilocybin treatment. The ventromedial prefrontal cortex (vmPFC) is responsible for emotional processing, action, cognitive behaviour and goal-orientation, and demonstrates top-down inhibitory control on the amygdala [ 181]. It is suggested then that psilocybin treating, which decreases functional connectivity between amygdala and the ventromedial prefrontal cortex (vmPFC) in response to fearful and neutral (but not happy) faces, also decreases the top-down inhibitory control that the vmPFC has on the amygdala, and ultimately results in increased amygdala activity [ 181]. In medication-naïve individuals, decreased functional connectivity between the amygdala and the left rostral prefrontal cortex (left rPFC) is characteristic of major depressive disorder [ 187].

Also characteristic of depression and schizophrenia is an alteration of serotonergic signalling [ 188]. Thus, drugs that target serotonergic receptors in the prefront cortex may be of clinical importance [ 188].

3.3. Effects of Magic Mushrooms

Perceptible psychological effects of psilocin correlate with plasma levels between 4 ng/mL and 6 ng/mL [ 142]. Hasler and colleagues estimate the bioavailability of psilocin to 52.7% (after 10-20 mg psilocybin ingestion) [ 142]. After a rapid increase in plasma levels of psilocybin, followed by a plateau for approximately an hour, psilocybin levels wane significantly until barely detectable after 6 h [ 142].

Subjective effects may last between 3 and 6 h [ 5], after which effects subside to negligible levels [ 41]. The effects of psilocybin may be classified into four categories: (1) Perceptual, (2) Cognitive, (3) Emotional and (4) Ego Dissolution [ 99]. More simply, the effects of psilocybin use may be divided into psychic and somatic effects [ 5] ( Table 3 ).

Table 3

Psychic Effects in Humans and Animals (in Medium Dose (12-20 mg p.o.)

Somatic Effects in Humans (Barely Noticeable/Secondary Pharmacological Effects) [5]

1. Stimulation of affect/affective activation [ 5],

2. Hypnagogic experience [ 5],

3. Enhanced ability for introspection [ 5],

4. Mystical-type experience, which predicted the success of the therapy and likelihood of persisting positive benefits [ 9, 15],

5. Alterations of thought and time sense [ 5],

At 8-12 mg p.o., i.m.;

1. Accelerated heart frequency [ 189],

2. Slowed heart frequency [ 189],

3. Increased reflex tendineae [ 189],

4. Decreased reflex tendineae [ 189],

At 0.11 mg/kg p.o, similar effects were observed in another study [ 190]. At 1.5 mg increased to 25 mg p.o. in three doses per day, for 21 consecutive days, another study reported no significant aberrations in the parameters above [ 191].

In clinical studies, the clinical outcome, and acute and long-term subjective effects of psilocybin administration are measured using questionnaires such as the Subjective experience (5D-ASC) [ 72], the Beck Depression Inventory (BDI) [ 72], the Profile of Mood States (POMS) [ 69], the State-Train Anxiety Inventory (STAI) [ 72], the Mystical Experience Questionnaire [ 72], and the Quick Inventory of Depressive Symptoms (QIDS) [ 72]. Table 4 lists additional acute and long-term, subjective effects of psilocybin administration. Table 5 lists participants' first-hand experiences and subjective perspectives during and after psilocybin in a 2016 phenomenological study conducted by Zamaria and colleagues [ 15].

Table 4

Effect

Reference

1.

Positive changes in personality and increased altruism. This may, in turn, have wider benefits to society and the global environment.

[ 192, 193, 194, 195, 196]

11.

Sustained/persisting improvement in attitudes and behaviour.One study reports substantial decreases in depressive and anxious symptoms persisting up to 6 months after a single active treatment.
In another study, participants report positive persisting effects in areas of mood, behaviour, and attitudes after up to 14 months after psilocybin therapy.

12.

Improved psychological flexibility and feelings of personal meaningfulness, and subsequent improved psychological outlook.
Ability to reframe how a patient views their medical conditions, themselves, their lives and relationships with others.

[ 192]

Table 5

Subjective, First-Hand Accounts of Experience with Psilocybin Treatment

Reference

1.

[ 15]

2.

Changes in outlook

[ 15]

3.

[ 15, 196]

4.

Peace and Happiness

"Incredible, profound calmness and stillness"

"Happiness and contentment"

"Persistent happiness and joy"

[ 15]

5.

[ 15]

6.

Physical/Mental

[ 15]

3.4. The Possible Entourage Effect Phenomena in Magic Mushrooms

The phenomenon of the entourage effect suggests that the sum of the contributing parts of a botanical or biological system produce a greater, synergistic effect in comparison to the effect of each individual part when presented alone. The entourage effect is mostly associated with Cannabis sativa L.

Although psilocybin is the most popular and the most abundantly produced psychoactive compound/tryptamine derivative in magic mushrooms, other tryptamine derivatives such as psilocin [ 206], baeocystin [ 207], norbaeocystin [ 207], norpsilocin [ 207] ( Figure 6 ) and the beta-carbolines such as harmane and harmol [ 208], may also enhance the effects of psilocybin and the efficacy of psilocybin treatment [ 208, 209]. Thus, it is likely that these hallucinogenic compounds may work in tandem to produce a synergistic effect [ 208, 210, 211, 212, 213].

It should be noted that the ingestion of magic mushrooms, with multiple compounds present, will likely produce a different effect to the ingestion of a single, isolated compound, like pure psilocybin [ 208]. This is due to a difference between the pharmacology of whole magic mushrooms and a single, isolated pure compound [ 208]. This also suggests a synergism of multiple compounds in the mushroom.

In a marble-burying behavior study in mice that mimics anxiety and obsessive-compulsive disorder (OCD), Matsushima and colleagues report the findings that, at the same dose of 0.1 to 1.0 g/kg, a psilocybe argentipes mushroom extract was more effective than pure psilocybin alone at reducing marble-burying behaviour without affecting overall locomotion [ 213]. This too suggests the probable synergistic involvement of multiple bioactive active compounds in the mushroom extract [ 213].

In a species of magic mushrooms known as Inocybe aeruginascens, aeruginascin, a trimethylammonium analogue of psilocybin, is also produced in addition to psilocybin and baeocystin [ 214, 215]. Aeruginascin demonstrates a high affinity for the 5-HT 1A, 5-HT 2A, and 5-HT 2B serotonin receptors [ 216] in producing euphoria-based hallucinogenic effects and, likely modulate the pharmacological action of psilocybin and the psilocybin-experience [ 217]. Norpsilocin is also a potent 5-HT 2A receptor agonist and is even reported to be more potent and possibly more efficacious than psilocin [ 207], while other the tryptamine derivatives baeocystin and norbaeocystin may serve as prodrugs to the bioactive compounds norpsilocin and 4-hydroxytryptamine, respectively [ 207], Baeocystin is a direct precursor to psilocybin [ 218], although it is not hallucinogenic by itself [ 207].

Further research is necessary to determine potential synergies amongst these compounds and other active and inactive molecules produced by magic mushrooms, and to determine the bioactivity of each compound on its own. On this tangent, practitioners should consider that some patients may require individualized treatments that may require a combined treatment approach as opposed to treatment with a single compound. Table 6 lists some factors that affect therapeutic/clinical outcome of psilocybin administration.

Table 6

Factor

Reference

1.

Extra-pharmacological elements (as with any drug). These include age factors, body weight, body size, muscle mass, genetics, drug tolerance, drug interactions, drug purity, dosage, gender, recreational consumption and inexperience with recreational drug use, past experiences with drug use, mindset, setting (context in which drug is used), experimental setting, social interaction, cultural influences, medical history, placebo design and response to placebo, and drug instrumentalization (instruments used to administer drugs).

[ 192, 205, 219, 220, 221, 222, 223, 224, 225]

2.

Mindset

Patient attitude and expectations (psychological flexibility/ outlook)

Preconceptions of treatment

3.

Setting

Use of religious and spiritual imagery

Use of a purpose-built facility

[ 192]

4.

Psychological support

Intensive clinical care/contact

Supportive and reassuring interaction with therapists/sitters.

Reliable induction of "mystical experience" by clinician/therapist. Mystical experiences after psilocybin administration directly correlate with therapeutic outcome and persisting positive subjective effects.

[ 15, 192]

6.

Treatment type

Some patients may require personalized/individualized treatment which may involve combination therapy with other drugs. Drug interactions may likely affect psilocybin treatment.

Treatments with mushroom extracts as opposed to pure isolated psilocybin may also have different outcomes.

7.

Type of mood or anxiety disorder

3.5. Adverse Effects, Risks and Contraindications

To reiterate, psilocybin is a Schedule I controlled substance as defined by the United Nations 1971 Convention on Psychotropic Substances. By this definition, psilocybin is considered to have a high abuse potential and is currently not accepted medically. In uncontrolled settings such as in recreation, abuse of psilocybin may lead to what is referred to as a "bad trip". This is an undesired or even traumatic physical and emotional experiences characterized by altered visual perception, extreme distress, fear, lack of coordination, derealization, depersonalization, paraesthesiae, heightened fright, panic-attacks, traumatic flashbacks, paranoia, delirium, short-term psychosis and other symptomology characteristics of schizophrenia [ 228, 229, 230, 231, 232, 233]. This undesired physical experience may also be accompanied by nausea, vomiting, mydriasis, headache, chills and drowsiness [ 229, 230, 234]. Some symptoms may even persist. A "bad trip" is typically treated with benzodiazepines [ 228].

Mushroom toxicity is also a risk associated with some species of psilocybin mushrooms. Though rare and typically accidental, mushroom poisoning is also a risk, and may lead to minor gastrointestinal illness (such as gastroenteritis), erythromelalgia, rhabdomyolysis, intestinal fibrosis, hypertension, hyperreflexia, liver failure, renal failure, convulsions, bradycardia, and tachycardia [ 228, 230, 235]. Mushroom poison may also require medical intervention or emergency hospitalization [ 230, 231]. In general, alcohol and other drugs may exacerbate the psychological and physical risks of psilocybin abuse [ 229]. On the same tangent, individuals with a personal or family history of severe psychotic and psychiatric disorders are discouraged from using psilocybin, and by extension, other psychedelics [ 236].

In general, psilocybin is reported to have the most favourable safety profile of all psychedelic drugs [ 13, 237, 238]. Thousands of years of anecdotal evidence in addition to modern-day scientific studies confirm that psilocybin has low physiological toxicity, low abuse/addictive liability, safe psychological responses, no associated persisting adverse physiological or psychological effects during or after use [ 2, 5, 22, 102, 158, 239, 240]. Psilocybin overdose is very rare [ 241, 242]. One such report of psilocybin overdose and subsequent fatality was specifically due to cardiac arrest, some 2-3 h after psilocybin ingestion, in a 24-year-old female who, 10 years prior, had a heart transplant due to end-stage rheumatic heart disease [ 243].

In patients with mental or psychiatric disorders, suicidal ideation and auto-mutilation are possible risks of magic mushroom ingestion and, though rare, have been documented in the literature [ 244]. Another risk is the possibility of exacerbating psychotic symptoms [ 192]. As a result, having psychotic disorders such as schizophrenic tendencies is a contraindication for undergoing psychedelic-assisted psychotherapy, particularly psilocybin-assisted psychotherapy [ 245].

It is also reported that repeated psilocybin use will build high tolerability but will not lead to physical dependence [ 5, 158, 246]. Cross-tolerance with other psychedelics such as LSD and mescaline [ 7, 228, 247]) is also a possibility. Discontinued psilocybin use does not typically cause adverse physical effects or symptomology related to drug withdrawal [ 228]. There is also a chance that psychological withdrawal may occur [ 228].

The Registry of Toxic Effects of Chemical Substances (RTECS) has assigned psilocybin a therapeutic index of 641, associated with a relatively better safety profile in comparison to nicotine and aspirin, with values of 21 and 199, respectively [ 102]. Essentially, this means that psilocybin has very low chronic toxicity, moderate acute toxicity, negligible public health and criminal effects [ 233]. To date, there is no standard value for a lethal dose at neither the recreational nor medicinal levels in humans [ 240].

3.6. Pharmacokinetics of Psilocin

To reiterate, the effects of magic mushrooms are dependent on the species of mushroom (and ultimately the concentration of active metabolites in a given species), an individual's mindset an individual's body type (particularly weight, metabolism) and an individual's level of tolerance.

Psilocybin has a shorter half-life and duration of action when given intravenously [ 5, 142]. On the same tangent, psilocin has approximately two-thirds of unaltered (3-10%) psilocybin and glucoronidated metabolites are excreted through the kidneys after approximately 3 h [ 5]. Because the oral bioavailability of psilocin is 52.7% (after 10-20 mg psilocybin ingestion) [ 142], as a result, it is typically administered orally, but may also be administered intravenously, with comparable efficacy. Table 7 is a list of pharmacokinetic data on psilocin. Figure 7 shows the metabolic pathway of psilocybin.

Table 7

Type of Administration

Mean Half-Life of Psilocin

Elimination Constant (kC)

Absorption Constant (ka)

References

1.

Mouth (PO)

135 min

0.307/h

1.307/f

[ 245]

2.

Mouth (PO)

163 min

-

-

[ 142]

3.

Intravenous

74 min

-

-

[ 142]

After oral administration, most psilocybin, psilocin and glucoronidated metabolites are excreted via the kidneys, typically after about three hours [ 251]. After about 24 h, almost all psilocybin and psilocin are excreted from the body [ 251].

4. Economic Analysis of Neuropharmaceuticals Market

The increasing rate of global mood and anxiety disorders, particularly depression, the growing cultural and government acceptance, the increasing number of published scientific articles, and decriminalization, the burgeoning psychedelic industry has experienced an increase in economic value and a renewed pharmaceutical interest. This increase in value is also the result of more psychedelic companies going public and an increase in investors coming on board, especially since the COVID-19 pandemic and the subsequent collapse of investable cannabis opportunities [ 255].

In the 2nd quarter of 2019, more than USD 320 million was invested into psychedelic neuropharmaceutical development [ 255], followed by an estimated USD 100 million investment into various psychedelic research and clinical trials in the 3rd quarter of 2019 [ 255]. Globally, the psychedelic therapeutic market is predicted to reach a valuation of $6.8 billion by 2027, from USD 2 billion in 2019, at a growth rate of 16.3% [ 114]. The neurogenic market including mental health drugs, therapeutic services, neurodegeneration drugs and cognitive enhancement was valued at USD 373 billion [ 255]. The FDA's recent approval of SPRAVATO ®, a ketamine analog developed by Johnson and Johnson for use in patients suffering from treatment-resistant depression, and the approval of "breakthrough therapy" statuses for psilocybin treatments for Major Depressive Disorder (MDD) by Compass Pathways Ltd. and the Usona Institute, is also expected to spur the growth of psychedelic research.

Recently, Numinus Wellness Inc. was granted the first Health Canada license to produce and extract psilocybin from mushrooms [ 256]. This hallmark achievement will spur the growth of the synthetic psilocybin market in particular, and will allow for the rigorous scientific investigation of synthetic psilocybin as an alternative therapeutic option to naturally-occurring psilocybin. This achievement will also allow for the wide-scale production of naturally occurring psilocybin and standardization of cultivation, extraction and testing methodologies-and innovation in said technologies, thereof.

5. Conclusions and Future Direction

Psychedelic-assisted therapies may provide new and significant opportunities to current issues in the conventional treatment of psychiatric disorders. Psilocybin-assisted treatment may be feasible, efficacious, toxicologically safe, physiologically well-tolerated, and may have enormous potential in psychiatric medicine, as evidenced by decades of multiple clinical studies and thousands of years of anecdotal reports [ 2, 5, 158]. However, there are limitations that must be overcome before it can become an established part of psychiatric treatment. These limitations include the highly sensationalized global history and lingering negative stigmatization of psychedelic drugs, particularly in the United States, challenges with federal regulations, U.S. Food and Drug Administration (USFDA) and (European Medicines Agency) EMA approval and federal funding for clinical psychedelic studies [ 2], the lack of standardized psychedelic/psilocybin diagnostic and therapeutic practices [ 257], particularly in inducing "mystical experiences" that are essential to the outcome of psilocybin therapy [ 192], lack of larger, more sufficient double-blinded, randomized, clinical studies to assess safety, pharmacology and dose-response relationships for each mood and anxiety disorder [ 158], and challenges with intellectual property (IP) and securing enforceable patents, seeing that mushrooms grow naturally. A result of this IP challenge is the unwillingness of some investors to invest in the psilocybin industry. However, with the COVID-19 pandemic and the subsequent collapse of investable cannabis opportunities, other investors have found this to be the prime time to invest in psychedelics.

As magic mushrooms go mainstream again, multiple U.S. jurisdictions are pushing for the decriminalization of psilocybin mushrooms. In 2019, Denver (Colorado) and Oakland (California) were the first cities to decriminalize (though not legalize) psilocybin and plant and fungi psychedelics such as magic mushrooms, respectively [ 258]. In 2020, Washington, D.C., voted to decriminalize a select few plant and fungi psychedelics such as mescaline and psilocybin mushrooms [ 258, 259, 260, 261]. In 2020, Oregon became the first state to legalize (and decriminalize) psilocybin mushrooms for personal development [ 261, 262]. Other states like California are putting in grassroots efforts to decriminalize psychedelic mushrooms. Despite the efforts of multiple cities and states in North America in decriminalizing psychedelic mushrooms, only until there are changes in the federal regulatory framework and accessibility to federal funding will the psychedelic market reach its full potential.

On the contrary, in Jamaica, psilocybin mushrooms are legal and decriminalized, and there is a budding medical psychedelic tourism industry with the rise of psychedelic retreats like the Atman and Mycomeditations retreats [ 263]. As a result of Jamaica's flexible regulatory framework for psychedelics, overseas companies are coming to the island to set up production and distribution infrastructure for psychedelic mushrooms [ 264]. In the future, we can expect the rise of psychedelic retreats and ultimately, medical psychedelic tourism in Jamaica.

Psychedelic research is also on the rise in Jamaica. In an attempt to convince the WHO to reschedule psilocybin out of Schedule 1 to more favourable scheduling, it is important that Jamaica's growing psychedelic mushroom industry focus on and be driven by scientific research and evidence-based data.

Pioneering plant-based psychedelic research companies such as The Psyence Group, based in Canada, has partnered with the Biotech Research and Development Institute (BRDI) (University of the West Indies, Jamaica), to bring to market novel psilocybin treatments for mental health disorders in Jamaica. Psyence was one of the first to build and operate a federally licensed commercial psilocybin cultivation and production facility in the world [ 130]. Other overseas companies have also partnered with the University of the West Indies (UWI), Mona to conduct psychedelic research and psilocybin clinical trials studying Major Depressive Disorder and Addiction in Jamaica [ 264].

With an estimated 20% of Jamaicans suffering from anxiety and depression now exacerbated by COVID-19, psilocybin-assisted therapy may be a viable solution [ 264].

Additional limitations to psilocybin pharmaceutical research, and psychedelic research in general, include lack of data on psilocybin-drug interactions and combination-medicine studies [ 99], the lack of data on the effects of psilocybin on brain activity/dynamics/structure and neuroplasticity [ 99], and the lack of data on the molecular, neurobiological and psychological mechanisms of action and behavioural effects of psilocybin for each diseased state, and the mechanism of action behind persisting positive effects after psilocybin treatment.

The future of psilocybin-based neuropharmaceuticals may also involve the general research and development of psilocybin drugs, the development of individualized neuropharmaceuticals to meet the specific needs of a given patient, combination therapy of psilocybin or psilocin with other drugs (such as cannabis/cannabidiol) [ 265, 266], conventional psychotherapy, and of non-psychoactive analogues of psilocybin [ 2]. It would also be interesting to study the synergistic effects of psilocybin in combination with other mind-altering and non-mind-altering drugs in the treatment of mood and anxiety disorders. Another interesting area study is the investigation of the possible potentiation of psilocybin's chemical effect by the rituals that often accompany shaman-led sessions, although conversely, this could scientifically be viewed as a confounding variable.

Author Contributions

Conceptualization, H.L. and B.S., Writing, review and editing: H.L., B.S., H.V., J.G., N.T., W.N., A.A. and L.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable. This study did not involve humans or animals.

Informed Consent Statement

Not applicable. This study did not involve humans or animals.

Data Availability Statement

Data sharing is not applicable to this article. No new data were created or analyzed in this study.

Conflicts of Interest

The authors declare no conflict of interest.

Sample Availability

Samples of the compounds are not available from the authors.

Footnotes

Publisher's Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

9. Canal C.E. Serotonergic Psychedelics: Experimental Approaches for Assessing Mechanisms of Action. Volume 252. New Psychoactive Substances; Springer Science and Business Media LLC; Berlin/Heidelberg, Germany: 2018. pp. 227-260. [[ PMC free article] [ PubMed] Google Scholar]

43. Reynolds C.F., III. Psilocybin-Assisted Supportive Psychotherapy in the Treatment of Major Depression-Quo Vadis? JAMA Psychiatry. 2020 doi: 10.1001/jamapsychiatry.2020.2901. [[ PubMed] [ CrossRef] Google Scholar]

45. Davis A.K., Barrett F.S., May D.G., Cosimano M.P., Sepeda N.D., Johnson M.W., Finan P.H., Griffiths R.R. Effects of Psilocybin-Assisted Therapy on Major Depressive Disorder: A Randomized Clinical Trial. JAMA Psychiatry. 2020 doi: 10.1001/jamapsychiatry.2020.3285. [[ PMC free article] [ PubMed] [ CrossRef] Google Scholar]

105. Bahr R., Lopez A., A Rey J. Intranasal Esketamine (SpravatoTM) for Use in Treatment-Resistant Depression In Conjunction With an Oral Antidepressant. P T Peer-Rev. J. Formul. Manag. 2019;44:340-375. [[ PMC free article] [ PubMed] Google Scholar]

129. Petranker R., Anderson T., Maier L.J., Barratt M.J., A Ferris J., Winstock A.R. Microdosing psychedelics: Subjective benefits and challenges, substance testing behavior, and the relevance of intention. J. Psychopharmacol. 2020 doi: 10.1177/0269881120953994. [[ PubMed] [ CrossRef] Google Scholar]

149. Londesbrough D.J., Brown C., Northen J.S., Moore G., Patil H., Nichols D. Preparation of Psilocybin, Different Polymorphic Forms, Intermediates, Formulations and Their. Number WO2019073379A1. Use. Patent. 2019 Apr 18;

153. Adams A.M., Kaplan N.A., Wei Z., Brinton J.D., Monnier C.S., Enacopol A.L., Ramelot T.A., Jones J.A. In vivo production of psilocybin in [ E. coli. Metab. Eng. 2019;56:111-119. doi: 10.1016/j.ymben.2019.09.009. [ PubMed] [ CrossRef] Google Scholar]

175. Carhart-Harris R.L., Roseman L., Bolstridge M., Demetriou L., Pannekoek J.N., Wall M.B., Tanner M., Kaelen M., McGonigle J., Murphy K. Psilocybin for treatment-resistant depression: fMRI-measured brain mechanisms. Sci. Rep. 2017:7. doi: 10.1038/s41598-017-13282-7. [[ PMC free article] [ PubMed] [ CrossRef] Google Scholar]

216. Chadeayne A.R., Pham D., Reid B.G., Golen J.A., Manke D.R. Active Metabolite of Aeruginascin (4-Hydroxy-[[ N, N, N-trimethyltryptamine): Synthesis, Structure, and Serotonergic Binding Affinity. ACS Omega. 2020;5:16940-16943. doi: 10.1021/acsomega.0c02208. PMC free article] [ PubMed] [ CrossRef] Google Scholar]

265. Küçüksen M., Küçüksen A.N. Psilocybin and/or psilocin in combination with cannabinoids and/or terpenes. No. US10729706B2. U.S. Patent. 2020 Aug 4;

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# data[].attributes.attachment_link.description
The psychedelic effects of some plants and fungi have been known and deliberately exploited by humans for thousands of years. Fungi, particularly mushrooms, are the principal source of naturally occurring psychedelics. The mushroom extract, psilocybin ...

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Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers

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Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers

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Abstract

Fungal endophytes, a diverse group of primarily ascomycetous fungi defined functionally by their occurrence within asymptomatic photosynthetic tissues of plants, occur in all major of land plants and in natural and anthropogenic communities ranging from the arctic to the tropics. Because of the tremendous diversity they encompass, ecological questions regarding the interactions of endophytes with the plants in which they live - and with other organisms that in turn interact with endophyte-plants symbiota - are difficalt to address. The goals of this review are to highlight progress, challenges, and frontiers in the study of foliar endophyte diversity, with the ultimate goal of encouraging research that both bridges the gap between, and advances, research in alpha taxonomy and ecology. I focus on four themes that are reflected in the recent and rapidly expanding literature regarding endophyte biology: (1) the taxonomic and ecological distinctiveness of endophytes relative to other nonpathogenic plant-associated fungi; (2) the insights that can be gained from studies that consider genotypes as the relevant unit of biological organization, especially in the context of traditional species-level taxonomy and robust methods that tie these genotypes and species together in an explicit evolutionary context; (3) the context-dependency of endophyte communities, highlighting the importance of both the identify of host plants and the geographic location in which plants occur; and (4) the complexity of the endophyte-pathogen-saprotroph continuum, and the challeges and exciting frontiers that lie in understanding the evolutionary relationships and ecological lability of fungi that exhibit these ecological modes. I argue that never before has the study of lineages phylogenetic endophytic fungi been more exciting or more tractable, and that the potential for endophyte researchers to inform diverse areas of biology has never been greater.

Introduction

Endophytic fungi, a polyphyletic group of highly diverse, primarily ascomycetous fungi defined functionally by their occurrence within asymptomatic tissues of plants, are found in above-ground tissues of liverworts, hornworts, mosses, lycophytes, equisetopsids, ferns, and seed plants from the arctic to the tropics, and from agricultural fields to the most biotically diverse tropical forests. Their cryptic lifestyle, ubiquity, and richness within individual plants, coupled with emerging evidence of their often-overlooked ecological importance, have inspired growing enthusiasm regarding these little-known fungi over the past four decades. In particular, David Hawksworth's much-discussed estimates of fungal diversity at a global scale (Hawksworth, 1991, Hawksworth, 2001) engendered tremendous enthusiasm for understanding endophyte diversity. Since 1991, a growing number of surveys - built on the pioneering work of Carroll (e.g., Carroll and Carroll, 1978, Carroll, 1986, Carroll, 1988), Fisher (e.g., Fisher et al., 1986, Fisher and Petrini, 1990), Petrini (e.g., Petrini and Müller, 1979, Petrini et al., 1979, Petrini et al., 1982, Petrini, 1985, Petrini, 1986, Petrini, 1991), Sieber (Sieber 1989), Stone (e.g., Stone 1986), and others (e.g., Bloomberg 1966; Espinosa-Garcia & Langenheim 1990; Johnson & Whitney 1989; Legault et al. 1989a,b; Rodrigues and Samuels, 1990, Spurr and Welty, 1975) - have generated a great deal of interest regarding the contributions of these cryptic microfungi to fungal systematics, plant and fungal ecology, evolutionary biology, and applied research ranging from biological control to bioprospecting. This interest is manifested in journal publications focusing on the abundance and/or diversity of fungal endophytes associated with above-ground tissues of non-grass hosts, which have increased in frequency from ca. 1.2 papers/yr (1971-1990) to >15 papers/yr (2001-early 2007; Web of Science search, February 2007). These totals include only English-language papers and exclude numerous outstanding contributions in edited volumes, theses, dissertations, and published abstracts (e.g., Stone, 1986, Petrini, 1986, Carroll, 1991; Stone et al. 2000) as well as review papers (e.g., Saikkonen et al., 1998, Saikkonen et al., 2004).

Concomitant with the explosion of research on endophyte diversity has been a rapid increase in work focusing on interactions with host plants, ultrastructural and colonization studies, characterization of novel metabolites, and other emergent topics related to endophytic symbioses (from 0.8 papers/yr in the 1970s to >200 papers/yr over the past six years). This body of literature has highlighted the ways in which endophytes associated with foliage of most plants differ taxonomically, ecologically, and in terms of diversity relative to the special clavicipitaceous endophytes of grasses (reviewed by Saikkonen et al., 1998, Clay and Schardl, 2002). Together, these studies have established the prevalence of horizontal transmission (Arnold & Herre 2003), the timelines that underlie colonization of new leaves (Herre et al. 2007), the phylogenetic relationships of endophytes (Higgins et al. 2007), their sensitivity to environmental perturbations (Helander et al., 1993, Lappalainen et al., 1999), their biochemical diversity (Strobel & Daisy 2003; Gunatilaka 2006; Zhang et al. 2006), and the previously overlooked ways in which they influence the ecological phenotypes of the plants they inhabit. For example, Pinto et al. (2000) showed that symptomless infections by Colletotrichum musae and Fusarium moniliforme decrease photosynthetic efficiency in maize and banana. Bing and Lewis (1991) showed that the entomopathogen Beauveria bassiana can grow as an endophyte and protect maize against an important herbivore (European corn borer, Ostrinia nubilalis). Redman et al. (2002) showed that a horizontally transmitted endophyte can provide thermal tolerance for plants. Arnold et al. (2003) showed that diverse assemblages of endophytes decrease lesion formation and leaf death due to Phytophthora sp. in the chocolate tree, Theobroma cacao, whereas Arnold and Engelbrecht (2007) demonstrated that seedlings of that species lose water more quickly under severe drought when endophytes are present. The subtlety of these interactions is notable: plants typically show no observable change in growth rate, biomass accumulation, root:shoot ratio, or other easily quantifiable characteristics following inoculation (Arnold 2002). Yet when plants are challenged by biotic or abiotic stressors, the importance of endophytes becomes clear. Together, these studies represent the tip of a very large iceberg: only a tiny fraction of plant-endophyte symbioses has been assessed to understand the costs and benefits to hosts of harboring these fungi in their photosynthetic tissues.

One of the exciting and challenging aspects of endophyte ecology lies in understanding those costs and benefits in the context of the nearly bewildering diversity of foliar endophytes. A powerful tool in this endeavor consists of placing these diverse endophytic associations in an evolutionary and ecological context (Thompson 2005). It has long been recognized that the outcomes of microbe/host interactions can be influenced by the genetic diversity of symbionts, the ways in which they are acquired from the environment, their ability to co-colonize individual hosts, their direct and indirect interactions, and their own evolutionary history, encapsulated by the genomic architecture associated with pathogenicity or other ecological modes (see Herre et al., 1999, Loftus et al., 2005, Maynard-Smith and Szathmary, 1997). Inasmuch as recent works have shown that there are few golden rules for predicting the directionality of species interactions along the mutualist-parasite continuum, it has become clear that understanding the context of those interactions is critical for interpreting their ecological and evolutionary significance (Agrawal et al. 2007). An important aspect of that context lies in understanding the evolutionary origins of symbioses. Steps in this direction are being taken with large-scale phylogenetic analyses of endophytes (Arnold et al. 2007b). More fundamentally, however, knowledge is still needed regarding endophyte diversity at the levels of genotype, species, clades, and function: despite an accumulation of numerous studies, we still lack a comprehensive understanding of the diversity of fungi capable of forming endophytic symbioses with plants in any given ecosystem.

The goals of this paper are to highlight progress, challenges, and frontiers in the study of foliar endophyte diversity. Far from an academic question, understanding endophyte diversity has implications for ecologists seeking to understand basic aspects of plant-fungal associations; agriculturalists seeking to apply endophytes in biological control programmes or exploring the genes or genomic features that underlie pathogenicity; bioprospectors searching for efficient methods to uncover novel secondary metabolites; mycologists interested in elucidating the structure of the fungal tree of life; and evolutionary biologists seeking to understand the evolutionary origins, stability, and future of species interactions.

Although only a small portion of the growing literature on endophytes can be reviewed here, several emergent properties of endophyte communities are becoming clear, with major implications for understanding fungal diversity at levels from the genotype to ecological function. This review focuses on four central theses. First, foliar endophytes are largely distinct from other nonpathogenic, plant-associated fungi. In some cases, leaf endophytes represent or are dominated by different major lineages of Ascomycota (e.g., compared to endo-, ecto-, and ectendomycorrhizal fungi); in other cases, they represent distinctive species or genotypes whose close relatives colonize roots or other tissues. Second, the relevant level of biological organization for estimating the diversity and specificity of endophyte communities may lie below the species level - that is, at the level of genotype - and will also be informed by phylogenetic studies that provide an evolutionary perspective at the family and ordinal level. Third, foliar endophyte communities are shaped both by the identity of host plants and the geographic location in which those plants occur. Communities typically include a mix of common and often generalist species, and rare species whose host specificity and geographic structure are difficult to assess. One major challenge lies in disentangling rarity and specificity; another lies in understanding the evolutionary implications of context-dependent endophyte assemblages. Fourth, some foliar endophytes may also act as pathogens and saprotrophs, in some cases attacking or decaying hosts with which they do not form endophytic associations. However, the frequency and nature of overlap among these communities is not yet clear, with inferences currently limited by methodological issues and by the ecological lability of many fungi. Finally, it is clear that the foundation provided by earlier studies, combined with recent technological and methodological advances and the increased accessibility of distinctive biomes, place us at the cusp of significant steps forward in our understanding of endophyte biology. In the final section of this paper, I highlight several frontiers in elucidating the diversity - and thus the ecological and evolutionary context - of endophytic symbioses.

Section snippets

Foliar endophytic and root-inhabiting communities

Leaves and roots represent the most dynamic interfaces between plants and their environment. Fungi that inhabit these biologically active tissues may share characteristics that allow them to grow and persist in an ever-changing biochemical milieu, or in the context of rapidly changing gene expression as host tissues grow and age. At the same time, fungi colonize roots in a context fundamentally distinct from fungi in the phyllosphere: whereas rhizosphere fungi occur in a matrix that, in many

Understanding diversity and specificity: below the species level

Petrini (1991) pointed out that the relevant level of biological organization in endophyte biology may lie below the species level - at the level of genotypes, or in the terminology of plant pathology, formae speciales. This would come as no surprise to plant pathologists, who have long recognized the ability of different infraspecific pathovars (in bacteria) or biotypes/ formae speciales (in fungi) to associate with different hosts, and manifest fundamentally different interactions with

Understanding diversity and specificity: above the species level

In the study outlined above, we observed no meaningful, species-specific differences in the communities of endophytic fungi associated with seven sympatric species of Quercus (Hoffman et al. unpubl. data). Only one oak endophyte was found in foliage of another non-oak host. Does this suggest some degree of host specificity at the level of plant genus, or perhaps at a higher taxonomic level? It is impossible to say without further sampling. However, several studies have shown that especially in

Context-dependence and the structure of endophyte assemblages

Implicit in estimates of fungal diversity at a global scale are assumptions regarding the similarity in fungal communities among different hosts and geographic regions. In general, however, very little is known regarding the turnover in endophyte species composition among biogeographic regions. A major challenge lies in comparing surveys conducted in different areas, which often rely on different culturing media, tissue fragment sizes, treatment of tissue following harvesting, and species

Endophytes, pathogens, saprotrophs: communities of uncertain overlap

Even if a given endophyte is capable of infecting multiple host species, its interactions may demonstrate functional or ecological specificity: an endophyte from one host species, while capable of colonizing a second, may not interact with both hosts in a similar manner. A wealth of plant pathology literature shows that fungal pathogens with complex life cycles inhabit different host species at different life stages, and that their interactions with those hosts differ markedly (Agrios 2005).

Examining endophytes associated with early-diverging lineages of green plants

Most studies have focused on endophytic fungi of angiosperms and conifers. Surveys of early-diverging lineages of plants are important for elucidating the evolutionary history of the endophytic symbiosis. Interestingly, Davis et al. (2003) show that cultivable endophytes associated with early-diverging lineages such as liverworts contain members of highly derived lineages of Ascomycota (e.g., Xylariales) rather than early-arising fungal taxa (see James et al. 2006). Similarly, studies of

Conclusions

Understanding the ecology, evolution, and importance of fungal endophytes is a daunting prospect given the tremendous number of fungi capable of forming endophytic associations and their uniqueness relative to other plant-associated microbes. However, never before has the future of endophyte biology been more compelling. By expanding surveys to include early-diverging lineages of plants, we will gain insight into the evolution of endophytic symbioses over the history of green plants. By

Acknowledgements

I thank Anita Bhakta, Lindsay Cook, Mariana del Olmo Ruiz, Mary Jane Epps, Cara Gibson, Dylan Grippi, Mali Gunatilaka, Michele Hoffman, Ming-Min Lee, Jason Ong, Fabiola Santos R., Mary Shimabukuro, and Jana U'Ren for discussion and assistance in collecting the new data presented here. For helpful discussion, I thank David Maddison, Julia Maddison, François Lutzoni, and Robert J. Steidl. This work was supported by the College of Agriculture and Life Sciences at the University of Arizona, the

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Understanding the diversity of foliar endophytic fungi: progress, challenges, and frontiers

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Fungal endophytes, a diverse group of primarily ascomycetous fungi defined functionally by their occurrence within asymptomatic photosynthetic tissues...

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All about the incredible, cryptic communities of fungi living in plants!

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Get current with what we know and what we don't know regarding Freshwater Fungal Biology

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Marine fungi: opportunities and challenges 

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Marine fungi: opportunities and challenges 

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CESAM, Department of Biology, University of Aveiro, 3810-193 Aveiro, Portugal

Author to whom correspondence should be addressed.

1. Introduction

Fungi are ubiquitous organisms widely distributed in ecosystems, including marine environments [ 1, 2, 3]. Marine environments represent the last frontier of biodiversity. Even though marine habitats account for 70% of the surface of the planet, they still remain biologically unexplored. Fungi are key players in terrestrial and marine environments representing a substantial proportion of the microbial diversity on Earth [ 1].

Over time, different definitions of marine fungi have been used. Marine fungi were originally defined based on their physiological characteristics, such as the requirement of more than 30% salinity to grow [ 4]. The first attempt to define 'marine fungi' and still the most quoted definition was given by Kohlmeyer and Kohlmeyer [ 5]. These authors restricted 'marine fungi' to two ecological groups: obligate and facultative marine fungi. Obligate marine fungi are those that grow and sporulate exclusively in a marine or estuarine habitat; facultative marine fungi are those from freshwater or terrestrial milieus, able to grow and sporulate in marine environments. However, this distinction is not always easy nor clear to establish, and it is somehow controversial. Later, Jones et al. [ 6] labelled 'obligate' marine fungi as those isolated from submerged substrates or sediments from marine environments. The term "marine-derived fungi" has been extensively used in the field of natural product chemistry [ 7]. Recently, Pang et al. [ 8] reviewed the use of the terms "marine fungi" and "marine-derived fungi" and proposed a wide-ranging definition. These authors replaced Kohlmeyers' definition by a broader concept. From this point forward, marine fungi are defined as any fungus able to: (i) grow and/or sporulate (on substrata) in marine environments; (ii) form symbiotic relationships with other marine organisms; or (iii) adapt and evolve or be metabolically active in marine environments.

In the past, marine fungi were viewed as an exotic group, relatively species-poor, with low abundance. Over the last two decades the use of culture-independent approaches and, more recently, of next-generation sequencing methods have started to disclose a considerable hidden fungal diversity from a wide range of environments [ 9]. In this respect, only recently, marine fungi have attracted attention and are yet to find a prominent place in biotechnology [ 3].

Marine fungi are a biochemically diverse group of organisms representing a promising source of novel bioactive natural compounds. The secondary metabolites produced by marine fungi include terpenes, steroids, polyketides, peptides, alkaloids, and polysaccharides. These metabolites are mainly associated with antimicrobial, anticancer, antiviral, antioxidant, and anti-inflammatory activities [ 3, 10]. Considering this wide range of activities, these metabolites hold great promise since they can be used for drug discovery and medical, pharmaceutical, agriculture and cosmetic applications [ 3]. Besides being a source of bioactive compounds, marine fungi are also recognized for their metabolic capacities for bioremediation. This capacity aids, for instance, in the degradation of recalcitrant cell wall compounds (marine fungi express catalases, laccases, peroxidases) and environmental contaminants (e.g., toxic pollutants and microplastics) [ 11].

2. Origin and Diversity of Marine Fungi

The origin of fungi remains unclear. Fungi are presumed to have evolved in the late Proterozoic, about 900-570 million years ago (mya) ( Figure 1) [ 12, 13, 14, 15]. However, according to the Ongeluk fossils, the fungal clade is considerably two to three times older than current age estimates [ 16]. The basalt from the Palaeoproterozoic Ongeluk Formation in South Africa suggests that fungi have inhabited submarine volcanoes approximately 2400 mya. Most of the species described in marine ecosystems have relations to terrestrial species. In fact, fungi transitioned several times from marine to terrestrial environments, and vice versa [ 17]. During evolution in the Precambrian (from the formation of Earth about 4600 mya to the beginning of the Cambrian Period, about 541 mya), cooling events and marine salinity decrease, resulted in the increase of dissolved oxygen, allowing the transition of non-marine early fungi to marine niches [ 18]. The existence of a terrestrial runoff or different migration trajectories from terrestrial to marine environment [ 19] was accompanied by several adaptations in response to these environmental changes [ 20]. However, the origin of marine fungi is still discussed.

2.1. Challenges and Adaptions

Fungi in the sea face substantial challenges compared to the terrestrial compartment. Figure 2 shows some of these challenges, and the molecular and morphological adaptations of fungi to thrive in the marine environment. High levels of salinity lead to osmotic and ionic stress. However, fungi can control their turgor through a conserved pathway known as the high-osmolarity-glycerol (HOG) signaling pathway. This pathway is responsible for the regulation of the salt efflux pumps and the production of osmolytes compatible with cellular functions [ 21]. Another evident molecular adaptation is the production of gels and slimes by lignicolous marine fungi (colonizers of driftwood or submerged wood) which may retain secreted enzymes at the substrate [ 21]. Additionally, a range of morphological adaptations in fungal structures and in the spore-dispersion strategies contributes for the success of marine fungi ( Figure 2). One example of morphological-adapted fungi are chytrids (Chytridiomycota), also known as zoosporic true fungi, that depend on their zoospores for dispersal in water [ 22]. Although chytrids are one of the early diverging fungal lineages [ 22], and are the most common fungal group in marine habitats [ 23, 24, 25, 26], there is no sufficient evidence to show that the ancestral chytrids were marine [ 27]. This gap is largely due to the lack of molecular data in Chytridiomycota [ 22].

2.2. Diversity

Recent advances in high throughput sequencing technologies stimulated a new wave of research in marine mycology, revealing an increase of fungal diversity in the marine realm. However, using culture dependent methods, the most common taxa which have been recovered are predominantly allied to the phyla Ascomycota and Basidiomycota, to which more than 90% of the total described marine species belong [ 22]. In marine environments, the phylum Ascomycota is represented by the subphyla Pezizomycotina, Saccharomycotina and Taphrinomycotina, while Basidiomycota is represented by Agaricomycotina, Pucciniomycotina and Ustilaginomycotina [ 1, 28].

The subphylum Pezizomycotina, includes the classes Dothideomycetes, Eurotiomycetes and Sordariomycetes, which comprise the highest number of species described [ 7]. In this context, some of these classes include many marine hyphomycetes, a diverse ecological group that contains species able to alternate their life cycle between aquatic and terrestrial habitats. This ecological group is often associated with leaf litter, driftwood, water, algae, marine animals, and halophytes. Marine hyphomycetes have probably also evolved from terrestrial fungi with some morphological adaptations to colonize marine habitats. Yet, attempts to taxonomically resolve several taxa incertae sedis in these subphyla are currently ongoing. Additionally, yeast-like fungi within the phyla Ascomycota and Basidiomycota have been found in marine environments [ 1].

The total fungal diversity has been the subject of much discussion. It is estimated that the number of fungal species ranges from 1.5 to 5.1 million [ 29, 30]. Marine fungi represent less than 1% of the known species [ 10, 29, 30], thus remaining a poorly characterized group. It has been estimated that the number of marine fungi range from 10,000 to 12,500 species [ 29], although more recently Garzoli et al. [ 31] suggested that up to 1 million species are yet to be discovered. The most up-to-date number of described marine fungal species until February 2021 is only 1901, distributed in 769 genera, 226 families, 88 orders, 22 classes and seven phyla into Aphelidiomycota, Ascomycota, Basidiomycota, Blastocladiomycota, Chytridiomycota, Mortierellomycota and Mucoromycota ( Figure 3, www.marinefungi.org (accessed on 9 January 2022) [ 32]). This estimate includes yeasts and filamentous fungi and other basal fungal lineages.

Over the last two decades, attempts to understand the diversity and function of fungi in marine habitats has also been made through culture-independent approaches [ 23, 26, 33]. More recently, next-generation sequencing methods have been used to disclose a considerable number of fungal species from a wide range of marine environments [ 23, 34]. However, from the known marine fungal species, some of them have a limited number of ITS (internal transcribed spacer region) sequences and are mostly identified based on the conserved 28S or 18S rRNA genes (large and small subunits of ribosomal RNA, respectively). The analysis of these conserved regions is not always reliable to delimitate fungal species. Therefore, multi-gene phylogenetic analyses allied with morphological characteristics are crucial for a correct species identification. Furthermore, genome sequencing approaches are critical to understand the evolution of fungi particularly those associated with early diverging lineages [ 22].

3. Diversity of Marine Fungi Habitats and Their Ecological Roles

Fungi are key players in terrestrial and marine environments representing a substantial proportion of the microbial diversity on Earth [ 22]. However, even though marine habitats account for 70% of the surface of the planet, they remain biologically unexplored. This is especially evident when considering microbial life in these environments, most specifically its fungal component. Despite many difficulties to isolate fungal species from marine environments, researchers continue to make progresses towards uncovering marine fungal species by exploring new habitats. Marine fungi have been recovered from organic and inorganic substrata ( Figure 4): mangrove plants, macroalgae, seagrass, coral reef, drift- and submerged wood, sponges, sea ice, sea garbage, and coastal and open-ocean water columns [ 35, 36, 37]. As mentioned, using high-throughput sequencing technologies, researchers have also found marine fungal species on deep-sea and benthic sediments, hydrothermal vents, oxygen-deficient environments and in global surface waters [ 23, 26, 33]. Table 1 summarizes studies (from 2015) of marine fungi diversity covering different substrata.

Although marine fungi are ubiquitous, some fungal species are found only in certain geographic regions, such as the tropics, subtropics, temperate or polar waters [ 149], or in specific substrates ( Table 1).

To sustain the biodiversity and marine ecosystem functioning, the energy fixed by primary photosynthetic producers in the ocean is controlled to various trophic levels [ 22]. Microorganisms play a key role in nutrient recycling and in the regulation of energy flow in marine ecosystems [ 22]. From these microorganisms, marine fungi are one of the major components in marine food webs and occur as saprobes, mutualists, endobionts and parasites [ 22]. As saprobes, fungi can colonize and transform the organic matter originated from plants, algae, and animals into valuable nutrients. As mutualists, fungi can be associated to organisms such as sponges or protozoans, where both individuals benefit. As endobionts, fungi can provide energy to the host or even be commensals benefiting from host protection. As parasites of phytoplankton, macrophytes, algae, and animals' marine fungi can cause leaching of dissolved organic matter and destruction of their host populations [ 22]. Cryptomycota and Chytridiomycota are considered as early diverging fungal lineages, displaying physiological adaptations for inhabiting aquatic ecosystems, and contributing to marine food webs [ 150]. For example, Senga et al. [ 151] showed that parasitic fungi, such as chytrids (Chytridiomycota), utilize living diatoms efficiently. Additionally, chytrids can change the quality and quantity of algal dissolved organic matter, thus influencing higher trophic levels. Therefore, by virtue of chytrids' interactions with diverse living or dead organisms, marine fungi can transform and incorporate organic matter into the food web regulating the energy flow in marine ecosystems [ 1]. Similarly, members of Cryptomycota are parasitic zoosporic fungi exhibiting a similar life cycle to chytrids (e.g., free-swimming stage), and are typically found in freshwater, soil and in some marine habitats. In addition to chytrids, Cryptomycota fungi are dynamic players on microbial food webs and can parasitize many phytoplankton species such as diatoms, green algae, and dinoflagellates [ 152]. Despite the potential role of Chytridiomycota and Cryptomycota as mycopesticide formulations, such is still unexplored, mainly due to cultivation difficulties.

4. A Source of Potential Bioactive Compounds

The identification of novel natural products appears to be a robust approach to the approval of new drugs and therapies [ 34]. Therefore, there is the need to create new, safer, eco-friendly, and sustainable substances as alternatives to chemically synthetized products. Natural products are pharmacologically or biologically active chemical compounds or molecules (often below 1000 Da), found in nature and produced by a biological source [ 34]. Additionally, high molecular weight compounds such as proteins and polysaccharides also may show therapeutics potential. Referred to as secondary metabolites, these compounds are not directly involved in any primary function related to growth, development, and reproduction of an organism [ 153]. However, they are more commonly associated with organism's survival prospects, such as, defense, competition, and communication [ 154].

Penicillin, the first natural product antibiotic, produced by the fungus Penicillium notatum (syn. P. rubens and previously known as P. chrysogenum) was discovered by Sir Alexander Fleming in 1928 [ 155]. This event fueled the exploration of microorganisms as sources for antibiotics, initiating the golden era for the discovery of other natural products from fungi. Some studies were focused on an intensive exploration of new natural products with biologically active properties, from marine sources. Initially, the study of marine natural products was limited to organisms easy to collect such as corals and sponges. For example, the toxin tedanolide was isolated from the sponge Tedania ignis, while prostaglandins were isolated from the Caribbean Sea whip Plexaura homomalla [ 156]. Moreover, many natural products may also be synthesized by marine microorganisms [ 157]. In this respect and considering that only about 5% of the world's fungal taxa have been described, marine fungi have recently attracted attention for being a plentiful source for new chemical entities. However, marine fungi still represent an underexplored group, and researchers are yet to discover their full biotechnological potential [ 158, 159, 160, 161].

In 1945, the first group of natural products from marine fungi was described as cephalosporins, a class of β-lactam antibiotics isolated from the Acremonium chrysogenum (previously known as Cephalosporium chrysogenum) [ 162]. Later, in 1977, Okutani identified gliotoxin as a new type of the antibiotic diketopiperazine isolated from a marine fungus Aspergillus sp. obtained from deep-sea sediments [ 163]. Thenceforward, the number of antibiotic compounds isolated from marine fungi was rapidly increasing [ 162]. More than 3500 marine fungal secondary metabolites have already been reported [ 164], but a high number surely remains untapped. Such may be related to the unexploited marine ecological niches and their almost ubiquitous distribution, as well as to the high number of silent biosynthetic clusters in the genomes [ 34, 159]. Figure 5 shows some classes of metabolites produced by marine fungi and their associated biological activities.

Most of the research on secondary metabolites of marine fungi have been focused on a few genera: Penicillium, Aspergillus, Fusarium, and Cladosporium [ 60, 159]. However, studies of natural products from marine fungi continue to increase and have been expanded to other genera [ 159]. These studies have demonstrated that marine fungi represent a tremendous source of secondary metabolites for drug discovery [ 157]. The number of studies published increases every year, with most of them coming from species associated with different substrata and new habitats. Most of these metabolites are derivatives of those found on terrestrial fungi but hold significant differences in their biological activities (sometimes more effective and more specific).

Currently, 14 marine natural products are approved as drugs and more than 30 natural products are in different phases of clinical trials [ 165]. Despite the large number of new natural products from marine fungi, Plinabulin (diketopiperazine class) is the only one isolated from a marine fungus (Aspergillus sp.) that is currently under clinical trials by BeyondSpring Pharmaceuticals [ 165]. This compound is currently in the late-stage of a world-wide phase III clinical trial for anticancer therapy of non-small cell lung cancer and for the reduction of chemotherapy-induced neutropenia [ 166]. Despite the research efforts towards marine fungi, most studies are focused only on the description of new natural compounds with in vitro biological activities. A simplified representation of the fungal marine natural product drug discovery pipeline is shown in Figure 6. Therefore, after the drug discovery process, efficient approaches to produce enough quantities of the interest compound for clinical trials need to be implemented. Silber et al. [ 162] already listed different biotechnological approaches in all stages of the discovery-to-development of antibiotics from marine fungi.

4.1. Metabolomics Approaches

Omics (genomic, transcriptomic, proteomic, and metabolomic approaches) have become popular due to the advances in high-throughput sequencing technologies, bioinformatic tools and mass spectrometry techniques. Metabolomic approaches have embraced the discovery of natural products [ 34]. Mass spectrometry (MS) is a highly sensitive analytical tool used for the identification and quantification of metabolites [ 167]. Analytical techniques (e.g., nuclear magnetic resonance (NMR)) and several types of mass analyzers are used for metabolomic studies, such as capillary electrophoresis mass spectrometry (CE-MS), gas chromatography mass spectrometry (GC-MS), liquid chromatography mass spectrometry (LC-MS), and matrix-assisted laser desorption/ionization mass spectrometry (MALDI-MS).

Mass spectrometry has a significantly higher sensitivity and resolution than NMR [ 168], that requires a relatively simple sample preparation step and generates large amounts of data that remain challenging to handle. Despite MS-based approaches being able to quantify the metabolic profile in different sample matrices, the metabolites' capacity to ionize in a particular analyzer deeply influences data. MS-based approaches have become popular both in targeted and untargeted studies, due to their potential to identify an array of diverse metabolites by an organism [ 169, 170]. On the other hand, NMR-based approaches have advantages compared to MS. NMR is quantitative, highly reproducible, and has the possibility of not using standards to elucidate the compounds [ 168]. NMR is also a non-destructive technique, which allows MS-based approaches to be used as complementary. The use of these two approaches is information-rich, becoming more popular for the discovery of new metabolites. Table 2 sums up the recent studies of marine fungi's metabolome using different techniques. The most used techniques are GC-MS and LC-MS [ 171]. GC-MS separates a mixture of compounds according to their compound's volatility/molecular weight, while LC-MS separates according to compound polarity or hydrophobicity for example. However, LC-MS represents the most versatile approach for profiling extracts [ 172].

Metabolomics has become an essential analytical tool for the drug discovery process. Nonetheless, as metabolomics of marine fungi is still in its infancy, the identification of marine natural products, remains challenging [ 160]. Untargeted metabolomics generate massive data sets. However, analysis is time consuming, due to the lack of user-friendly bioinformatic annotation pipeline tools and open access data repositories. Furthermore, the prediction of biological activity of the secondary metabolites identified is a challenging task-if not impossible-because small structural differences in the molecules may lead to different bioactivities [ 34].

Recently, Rotter et al. [ 173] listed an overview of databases useful for the marine biotechnology pipelines. Briefly, the major MS/MS data organization tool and open access is the Global Natural Products Social (GNPS) Molecular Networking. However, most of the specific databases that already contain some marine natural products from fungi, such as Marine Lit and Dictionary of Natural Products, are not open access. Recently, Van Santen et al. [ 174] developed the Natural Products Atlas, an open access database for microbial natural products discovery. In any case, at our knowledge, there is no marine fungi-specific database combining mass spectra data.

Table 2. Different MS techniques used on marine fungi metabolomics.

4.2. Genomic Approaches

Marine fungal genomes' sequencing adds more in-depth information to search for natural products from these microorganisms. The increasing number of fungal genomes sequenced has revealed that fungi contain an enormous potential for secondary metabolite production. Biosynthetic gene clusters (BGCs) can be involved in different biosynthetic pathways, resulting in a variety of possible final products [ 117]. However, most of these BGCs have not been linked to their corresponding natural products [ 34]. So far, only approximately 4000 fungal species have completed or ongoing genome projects [ 196], with more than 8000 genomes available. The shortage of marine fungal genomes in public databases, such as Genome-NCBI (National Center for Biotechnology Information) ( https://www.ncbi.nlm.nih.gov/ (accessed on 9 January 2022) [ 197]) and JGI Genome Portal (Joint Genome Institute) ( https://genome.jgi.doe.gov/portal/ (accessed on 9 January 2022) [ 198]), impairs the fast identification of BGCs, thus hampering the discovery of natural products from these microorganisms. Table 3 shows an overview of the marine fungal genomes sequenced that are deposited at Genome-NCBI and at JGI databases. Ascomycota is the phylum that contains more sequenced marine fungal genomes (21 isolates of 12 different families).

The 'unculturable' fungal species represent one of the major problems and challenges for marine mycology. Isolation into pure culture remains the gold standard for the identification, description, and genome sequencing of new marine fungal species. Another challenge for marine natural products identification is, as mentioned before, that BGCs may remain silent under laboratory culture conditions. To overcome this, different methods have been developed to 'awaken' or stimulate the expression of silent genes. Among these methods to induce the production of BGC coded compounds, we can highlight: (1) the use of epigenetic modifiers of natural or chemical elicitors (microbial cells components, microbial lysates, or non-biological origin compounds) and (2) the co-cultivation with other species [ 199]. These strategies are known as OSMAC (One Strain Many Compounds) approach [ 200]. OSMAC makes use of altering cultivation parameters or adding elicitors to activate silent and poorly expressed BGCs in microorganisms to induce the expression of more natural products [ 201].

5. Conclusions and Prospects

Marine fungi have been studied since the first record of a marine species. However, despite their widespread distribution and abundance, marine fungi have been largely neglected. Since isolation into pure culture remains the gold standard for discovery and description of novel taxa, the use of different methods for isolation, culture media, incubation temperatures, and damp/moist chamber incubation, may contribute for the increase of fungal diversity. Environmental alterations, such as the seasonality could also yield different diversity. However, climate changes can also have a major impact on the food web dynamics in the marine fungal communities as well as alter their structure causing unpredictable consequences. It is widely accepted that the climate is changing at a global level, and it is also essential to understand these impacts on marine fungi dynamics.

It is recognized that marine fungi represent a potential source of secondary metabolites for drug discovery. Although genome-wide sequencing allows the detection of BGCs involved in different biosynthetic pathways in marine fungi, there is still limited of genomes available. Therefore, it is crucial to broaden this field of investigation into underexplored marine taxa, to infer about the lifestyles, ecological roles, evolutionary history, and regulatory mechanisms.

Despite the research motivation, a holistic and integrated approach is necessary to ensure the success of any conservation management strategy or economic use of marine fungi. Therefore, all fungal species recorded in each study should be isolated and preserved in reference culture collections to provide the authentic biological material. This material will not only increase the accuracy of the taxonomic assignments but will also be useful for further biotechnological purposes.

Author Contributions

Conceptualization: M.F.M.G., A.C.E. and A.A.; Data curation: M.F.M.G.; Funding acquisition: A.A.; Methodology: M.F.M.G., A.C.E. and A.A.; Supervision: A.A. and A.C.E. Writing-original draft: M.F.M.G. Writing-review and editing: M.F.M.G., A.C.E. and A.A. All authors have read and agreed to the published version of the manuscript.

Funding

We acknowledge financial support of Portuguese Foundation for Science and Technology (FCT) through national funds to CESAM (UIDP/50017/2020+UIDB/50017/2020+LA/P/0094/2020) and to M. Gonçalves (SFRH/BD/129020/2017).

Institutional Review Board Statement

Informed Consent Statement

Conflicts of Interest

The authors declare no conflict of interest.

Entry Link on the Encyclopedia Platform

References

1. Johnson, T.W.; Sparrow, F.K. Fungi in Oceans and Estuaries; J. Cramer: Weinheim, Germany, 1961; p. 685. [Google Scholar]

2. Kohlmeyer, J.; Kohlmeyer, E. Marine Mycology: The Higher Fungi; Academic Press: London, UK, 1979; p. 704. [Google Scholar]

3. Jensen, P.R.; Fenical, W. Secondary metabolites from marine fungi. In Fungi in Marine Environments; Hyde, K.D., Ed.; Fungal Diversity Research Series; Fungal Diversity Press: Hong Kong, China, 2002; Volume 7, pp. 293-315. [Google Scholar]

4. Sarma, V.V. Marine fungal diversity: Present status and future perspectives. In Microbial Diversity in Ecosystem Sustainability and Biotechnological Applications; Springer: Singapore, 2019; pp. 267-291. [Google Scholar]

5. An Online Resource for Marine Fungi. Available online: https://www.marinefungi.org (accessed on 5 January 2022).

6. Raghukumar, S. Fungi in Coastal and Oceanic Marine Ecosystems; Springer: New York, NY, USA, 2017; p. 364. [Google Scholar]

7. BioRender. Available online: https://biorender.com (accessed on 25 September 2021).

8. Poli, A.; Bovio, E.; Ranieri, L.; Varese, G.C.; Prigione, V. Fungal diversity in the Neptune forest: Comparison of the Mycobiota of Posidonia oceanica, Flabellia omycote, and Padina pavonica. Front. Microbiol. 2020, 11, 933. [Google Scholar] [CrossRef] [PubMed]

9. Devadatha, B.; Sarma, V.V. Pontoporeia mangrovei sp. nov, a new marine fungus from an Indian mangrove along with a new geographical and host record of Falciformispora lignatilis. Curr. Res. Environ. Appl. 2018, 8, 238-246. [Google Scholar]

10. Gonçalves, M.F.M.; Aleixo, A.; Vicente, T.F.L.; Esteves, A.C.; Alves, A. Three new species of Neocamarosporium isolated from saline environments: N. aestuarinum sp. nov., N. endophyticum sp. nov. and N. halimiones sp. nov. Mycosphere 2019, 10, 608-621. [Google Scholar] [CrossRef]

11. Abdel-Wahab, M.; Bahkali, A.H.; El-Gorban, A.M.; Jones, G. Metagenomics Study of Fungi and Fungi-like Organisms Associated with the Seagrass Halophila stipulacea (Forssk.) Asch. from Al-Leith Mangroves, Saudi Arabia; Research Square: Durham, NC, USA, 2021; pp. 1-19. [Google Scholar]

12. Baral, H.O.; Rämä, T. Morphological update on Calycina marina (Pezizellaceae, Helotiales, Leotiomycetes), a new combination for Laetinaevia marina. Bot. Mar. 2015, 58, 523-534. [Google Scholar] [CrossRef]

13. Kwon, S.L.; Park, M.S.; Jang, S.; Lee, Y.M.; Heo, Y.M.; Hong, J.H.; Lee, H.; Jang, Y.; Park, J.H.; Kim, C.; et al. The genus Arthrinium (Ascomycota, Sordariomycetes, Apiosporaceae) from marine habitats from Korea, with eight new species. IMA Fungus 2021, 12, 1-26. [Google Scholar] [CrossRef] [PubMed]

14. Vohník, M.; Borovec, O.; Kolaříková, Z.; Sudová, R.; Réblová, M. Extensive sampling and high-throughput sequencing reveal Posidoniomyces atricolor gen. et sp. nov. (Aigialaceae, Pleosporales) as the dominant root mycobiont of the dominant Mediterranean seagrass Posidonia oceanica. MycoKeys 2019, 55, 59. [Google Scholar] [CrossRef]

15. De Menezes, G.; Câmara, P.; Pinto, O.; Convey, P.; Carvalho-Silva, M.; Simões, J.; Rosa, C.; Rosa, L. Fungi in the Antarctic Cryosphere: Using DNA Metabarcoding to Reveal Fungal Diversity in Glacial Ice from the Antarctic Peninsula Region; Research Square: Durham, NC, USA, 2021; pp. 1-18. [Google Scholar]

16. Carroll, A.R.; Copp, B.R.; Davis, R.A.; Keyzers, R.A.; Prinsep, M.R. Marine natural products. In Natural Product Reports; Royal Society of Chemistry: London, UK, 2019; pp. 122-173. [Google Scholar]

17. Abd El-Hady, F.K.; Abdel-Aziz, M.S.; Shaker, K.H.; El-Shahid, Z.A.; Ibrahim, L.S. Antioxidant, acetylcholinesterase and α-Glucosidase potentials of metabolites from the marine fungus Aspergillus unguis RSPG_204 associated with the sponge (Agelas sp.). Int. J. Pharm. Sci. Rev. Res. 2015, 30, 272-278. [Google Scholar]

18. National Center for Biotechnology Information. Available online: https://www.ncbi.nlm.nih.gov (accessed on 28 October 2021).

19. JGI Genome Portal. Available online: https://genome.jgi.doe.gov/portal/ (accessed on 28 October 2021).

Gonçalves MFM, Esteves AC, Alves A. Marine Fungi: Opportunities and Challenges. Encyclopedia. 2022; 2(1):559-577. https://doi.org/10.3390/encyclopedia2010037

Chicago/Turabian Style

Gonçalves, Micael F. M., Ana C. Esteves, and Artur Alves. 2022. "Marine Fungi: Opportunities and Challenges" Encyclopedia 2, no. 1: 559-577. https://doi.org/10.3390/encyclopedia2010037

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Marine Fungi: Opportunities and Challenges

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Marine fungi play a crucial role in energy flow and nutrient recycling, mediating the cycling of dissolved organic matter in marine environments. However, despite being a prolific group of organisms, marine fungi have been largely neglected for a long time. Besides their importance in the marine food web, marine fungi represent an active source of natural products.

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Fungi are widespread throughout marine habitats. Most marine fungi are microscopic, either microfungi, yeasts, or swimming zoospore‐producing groups such as the Chytridiomycota ('the chytrids'). The macroscopic exceptions are the marine lichens along coastlines. Marine mushrooms are yet to be discovered. The functional roles of marine fungi include parasites (e.g., infecting phytoplankton; Hassett & Gradinger, ), saprotrophs recycling organic matter (e.g., degrading phytoplankton‐produced polysaccharides; Cunliffe et al., ) and in symbiosis with other marine life (e.g., seaweeds; Bonthond et al., ). Here, I briefly summarize my perspective of marine fungi with an emphasis on identity. Looking into the crystal ball, I see a possible near future for marine mycology highlighting some conceptual and technical developments.

The first marine fungus was described in the middle of the 19th century and subsequently for several decades, early pioneers (e.g., Sparrow, ; Sutherland, ) extended a list of new species. The first proposal of a definition to identify marine fungi came in the mid‐20th century and was simply based around the physiological ability to grow in seawater (Barghoorn & Linder, ). Earlier studies had already shown that some fungi collected from the marine environment are the same or at least similar to non‐marine taxa (Sparrow, ), and an updated definition of marine fungi was made to separate the obligate marine fungi (i.e., fungi that only grow and sporulate in the marine environment) from facultative marine fungi (i.e., fungi that are from the non‐marine ecosystems that are still able to grow and sporulate in the marine environment) (Kohlmeyer & Kohlmeyer, ). The definition of a marine fungus was further developed to identify any fungus able to grow and/or sporulate in the marine environment or adapt and evolve or be metabolically active in the marine environment or form symbiotic relationships with other marine organisms (Pang et al., ). From the first described marine fungus, the legacy of collecting, characterizing, and cataloguing continues with an expanding compendium of marine fungal diversity (Jones et al., , ). All this work is made possible through collecting samples, observing fungi living on substrates, stimulating spore production, growing fungi and/or cultivation on artificial media, with taxonomy from morphology and more recently in combination with DNA barcoding of phylogenetic marker genes. Jan Kohlmeyer with Brigitte Volkmann‐Kohlmeyer need to be acknowledged here because they were some of the most prolific collectors and identifiers of marine fungi in the 20th and early 21st century with their herbarium of more than 25,000 specimens now held at the New York Botanical Garden. Cultivation‐based approaches to identify would‐be marine fungi are of course not perfect, and proof that the isolated fungus is active in the marine environment is important. Such information will help to distinguish the genuine marine fungi from cultured contaminants washed in from non‐marine ecosystems that are present but not active (Kohlmeyer & Kohlmeyer, ).

As with many topics in environmental microbiology, the advent and subsequent application of DNA‐based molecular ecology tools in the late 20th century offered a panacea to some limitations of culture‐based approaches and yet opened a Pandora's Box of issues likely to vex any typical 'Reviewer 2'. From early clone libraries and other now apparently obsolete techniques (e.g., my personal favourite was denaturing gradient gel electrophoresis), through to the current importunate production of high‐throughput next‐generation metabarcode libraries, we have an almost overwhelming bounty of apparent marine fungal diversity studies to peruse. These data‐dense DNA surveys have allowed a new interpretation of marine fungal diversity that is different to the 'Kohlmeyer‐type' view, including congruent spatial surveys that in some cases traverse entire ocean basins (e.g., Hassett et al., ) and temporal analysis from multiyear time‐series (e.g., Taylor & Cunliffe, ). With adequate resources that are available to many researchers but not all, these DNA‐based approaches are relatively quick and easy to conduct, and provide access to the field for those without the training or patience needed for identification covered in the previous paragraph.

Writing with the perspective of an eternal optimist, my gaze into the crystal ball is more of a wish list for the near future of marine mycological research, including a call for the wider inclusion of marine fungi in contemporary marine microbial and general marine science. As a general observation, there needs to be improved integration of fungi into wider understanding of the structure and function of marine ecosystems. Fungi still seem lacking from a consensus view of marine ecosystems at all levels. For example, I checked current editions of marine microbiology textbooks I use for undergraduate teaching and found marine fungi are included in some (Munn, ) but not others (Gasol & Kirchman, ). Who is responsible for this improved integration and how could this be achieved? Perhaps in part, this could be delivered with truly holistic whole system level approaches in marine science in which entire ecosystems are considered together, with fungi included alongside the usual suspects (bacteria, phytoplankton, etc.) in marine ecosystem functioning. Historic biases, including those associated with sampling approaches and assessment tools, can now be overcome to some extent with contemporary and inclusive methodologies à la Tara Ocean, for example.

We need a more realistic view of the identity of marine fungi that considers and combines both the culture dependent and independent approaches. Many of the marine fungi identified with culture‐independent DNA‐based tools are not on lists of 'obligate marine fungi' but are instead currently taxa more familiar to non‐marine habitats and potentially fall into Kohlmeyer's category of 'facultative marine fungi'. The relatively short DNA sequences from metabarcoding and choice of phylogenetic marker genes [normally the internal transcribed spacer (ITS) DNA between small‐subunit ribosomal RNA (rRNA) and large‐subunit rRNA genes or part of the small‐subunit rRNA gene] means at best only genera are typically resolved with other studies having coarser taxonomic resolution that is difficult to fully interpret. Overcoming the limitations of interpreting the typical short sequences that constrain most metabarcoding surveys would be worthwhile. More sequence data could improve taxonomic resolution of marine fungi and therefore progress our understanding of the phylogeny of taxa that are similar but still different and currently not differentiated. Longer read metabarcoding is promising because it captures entire and multiple phylogenetic marker genes. How long read metabarcoding needs to be to distinguish the closely related marine and non‐marine relatives should be assessed. Phylogenetic placement of the recently discovered marine fungus Emericellopsis atlantica in a clade of other marine relatives versus other species in the same genus and other non‐marine clades required catenated six‐gene analysis (Hagestad et al., ). The level of resolution needed to distinguish marine fungi across all major groups needs exploring.

'Nothing in biology makes sense except in the light of evolution' Theodosius Dobzhansky. As well as improving DNA‐based taxonomic resolution, developing a better understanding of the identity of marine fungi would also be supported by a clearer view of their evolution and therefore systematics. This includes improved insight into terrestrial and freshwater‐to‐marine transition events, which are critical in determining marine fungal evolutionary history and contemporary diversity. Compared to other microbial eukaryotes, terrestrial/freshwater to marine transition events have occurred many more times with fungi and often only 'recently' in an evolutionary sense (Jamy et al., ). Why and how did these transition events specifically occur in the fungi? The why could include the regular transport of terrestrial and freshwater fungi to marine ecosystems via estuaries into coastal waters or fungi living in dynamic marginal habitats and ecotones at the land‐sea coastal fringe such as on intertidal seaweeds and mangroves. The how is likely, in part, related to the incredible adaptive capabilities of fungi underpinning their ability to conquer distinct niches and general resilience/plasticity. An impact of these rapid and recent transitions to marine is that there is not much change in the phylogenetic marker genes currently used (Jamy et al., ). This could account for why many marine fungi in short read metabarcode studies appear the same or similar to terrestrial/freshwater fungi.

Identity and functional biology are frequently overlapping concepts in environmental microbiology. The two‐component research question ' who is doing what?' is probably a key aspect of many of our endeavours. More knowledge of the functional biology of marine fungi is also required. Think about nitrogen fixation in the marine environment and you might also be thinking about the marine diazotrophic cyanobacterium genus Trichodesmium. Oil degradation and the hydrocarbonoclastic genera Alcanivorax or Cycloclasticus. Marine primary production and the diatoms ( Chaetoceros, Skeletonema, etc.). Comparable levels of established understanding of the links between functional biology and identify of marine fungi are yet to be widely considered, with some groups such as the marine chytrids especially poorly studied (Laundon & Cunliffe, ). Here is an example to illustrate potential. The widespread yeast Malassezia was initially a surprising member of the marine mycobiome with close non‐marine relatives typically found living on skin (Amend, ); however, assimilation of ¹³C‐labelled diatom‐produced organic matter in stable isotope probing (SIP) experiments have shown that marine Malassezia are active saprotrophs in coastal waters (Cunliffe et al., ) and the open ocean (Orsi et al., ).

Insightfully, Kohlmeyer and Kohlmeyer () outlined what they called 'unsolved major problems' in marine mycology, which included the need for the quantification of biomass, abundance and activity. Some progress has been made since 1979 to address their concerns, but more work is needed. Only very few studies have quantified marine fungal biomass and abundance (e.g., Gutiérrez et al., ; Priest et al., ), certainly much less than other marine microbial groups. Marine fungal activity has been determined now in several different ways. Seeing is believing and some marine fungi are conspicuous in their activity, such as marine chytrids that are observed infecting diatoms in sea ice (Hassett & Gradinger, ) and the open ocean (Gutiérrez et al., ). With new 'single spore' DNA barcode techniques developed for freshwater chytrid parasites (Kagami et al., ), the identity of the marine chytrid parasites in action is possible. The lichens are perhaps the most obvious marine fungi in their activity, we see them living along coastlines with their symbionts (Chrismas et al., ). Activity has been shown through ¹³ C assimilation in SIP‐type experiments with examples already mentioned (Cunliffe et al., ; Orsi et al., ). RNA‐based studies of marine fungi have also been conducted, such as metatranscriptome indications of functional biology in the open ocean (Chrismas & Cunliffe, ). This work is still only a handful of studies from a small number of researchers, especially when compared to other marine microbial groups such as bacteria and protists. Greater exploration of marine fungal abundance, biomass (including production and turnover), and activity across all marine habitats and under changing conditions could be the ammunition needed to convince the wider marine microbiological and broader marine science community to include fungi in their view of the marine world.

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Fungi are widespread throughout marine habitats. Most marine fungi are microscopic, either microfungi, yeasts, or swimming zoospore‐producing groups such as the Chytridiomycota ('the chytrids'). The macroscopic exceptions are the marine lichens along coastlines. Marine mushrooms are yet to be discovered.

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Author links open overlay panelAmy S. Gladfelter 1 2, Timothy Y. James 3, Anthony S. Amend 4

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Fungi play a dominant role in terrestrial environments where they thrive in symbiotic associations with plants and animals and are integral to nutrien…

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After weeks of drenching rain, it's hard to miss the happy explosion happening around Sonoma County: emerging mushrooms.

With abundant water, varieties are popping up in wild assortments of otherworldly shapes and colors, much to the delight of local hikers and foragers.

But for many mycologists - people who study fungi - their appearance also offers an short-lived opportunity. An estimated 90% of fungal species on Earth have yet to be discovered, according to experts.

And, mycologists say, we're only just starting to learn how critically important the fungi among us are. Without them, life as we know it could not exist.

The mushrooms we see are just the visible fruiting bodies of microscopic filamentary creatures collectively known as fungi. To reproduce, the fungi produce mushrooms that release tiny spores, which spread in the air until they land in a habitat suitable to start a new colony. The spores are small enough that hundreds would fit on the head of a pin.

They're an extremely ancient form of life. The first fungi appeared long before the dinosaurs, long before there were plants. Fossil remains of fungi have been found that are 1,000,000,000 years old.

Since then, fungi have branched, multiplied and diversified into more than 1,000,000 species. As other types of life have evolved and appeared on the scene, the fungi have adapted and formed intimate relationships with them.

As a result, fungi are quite literally everywhere today. They're busy inside our bodies, in plants and soil and in habitats across the planet. They perform a variety of incredibly useful tasks, from breaking down organic matter and wood and supporting the roots of forests to fermenting our wine and making our bread rise.

Even so, it's estimated that science has only identified 10% or so of the species of all the fungi that exist.

Forest health

A Sebastopol-based project, FunDIS, is leading a new effort to find and catalog some of the world's "missing" fungi, before they're lost to climate change, pollution or human development. Gabriela D'Elia is the director of the FunDIS Fungal Diversity Study.

"Science is currently experiencing a 'fungal awakening,'" she said.

"Fungi predate plants," she explained. "In fact, they helped plants first move onto land. Today they're found in virtually all environments: ocean sediments, frozen valleys, on the walls of Chernobyl, our bodies' orifices, where they help us maintain a healthy balance."

Fungi are particularly important, D'Elia said, because they connect things.

For example, delicate networks of fungal filaments, known as mycelia, associate with plant roots. Underground, those fungal mycelia form extensive, highly interconnected webs, called mycorrhizal networks.

These networks have been found connecting the roots of pine and fir trees in forests, for example.

And they're critically important to forest health: Because the fungi can reach much farther through soil than individual tree roots, they can gather and transport water and nutrients to the trees, which they do in exchange for sugars the trees produce.

It's estimated that 95% of all plants rely on mycorrhizal networks like these, D'Elia said. Without their fungi, the kingdom of plants could not survive.

Fungi are also key to organic recycling in nature. No other organism we know of can break down lignin, the tough material in wood cells and bark.

"Without fungi, D'Elia explained, "the world would be deep in undecayed wood and plant matter, debris everywhere, towering above us.

"Fungi are incredibly useful, and likely in ways we haven't even yet discovered. They're essential for making wine and beer, chocolate, all fermentation - yeast is a fungus - and fungal enzymes are now used everywhere in industrial food production."

Scientists have discovered fungi with anti-bacterial and antiviral properties, and it's unknown what other beneficial features might be discovered, she said. But that will only be possible if science can explore the fungi kingdom before species are lost.

Extinction

Like other creatures, fungi have preferred habitats. Unfortunately, many of those habitats are under threat or disappearing, , D'Elia said. And we stand to lose species before we've even discovered they're there.

"Species are undoubtedly going extinct faster than we can catalog and map them" she said.

According to FunDIS, of an estimated two to 12 million species of fungi, less than 5% have been named.

The primary goal of FunDIS, D' Elia said, is to equip citizen scientists and professionals with tools to discover and document fungi and their habitats across North America. After signing up, participants can use the phone app iNaturalist or other available programs to record their finds.

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Local project leading effort to find, catalog world's mushrooms

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After weeks of drenching rain, it's hard to miss the happy explosion happening around Sonoma County: emerging mushrooms. With abundant water, varieties are popping up in wild assortments of otherworldly shapes and colors, much to the delight of local hikers and foragers.

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* How do plants and fungi interact, and why does it matter? Dr. Kabir Peay, Associate Professor of Biology at Stanford, digs into how mycorrhizal fungi shape the distribution of trees across the planet, and how they’ll play a role in forest resiliency in the face of climate change.

* Buried deep below farms are intricate networks of symbiotic fungi that provide a myriad of benefits to agricultural crops. Dr. Aidee Guzman, a postdoctoral fellow at UC Irvine, talks about the opportunities to harness these fungi for healthy soils—and healthy plants.

* While it’s widely known that mammals help disperse truffle spores, little is known about how birds play a role. But in the rainforests of southern Chile, they do: Dr. Marcos Vinicius Caiafa Sepulveda, a fungal ecologist at UC Riverside, is exploring how the truffle diet of certain bird species is boosting the health of their forest home.

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What kind of microscope do I need, and where do I get it?
You'll need a pretty good microscope. The many microscopes in people's basements and closets-forgotten gifts to 12-year-olds whose enthusiasm dwindled a few weeks after Christmas-are usually toys, great for looking at hair follicles and the like, but usually not powerful enough to get you very far with mushrooms. Some of the larger microscopic structures of mushrooms can sometimes be seen with these "garage-sale microscopes," however, and if you'd like to whet your appetite I recommend trying to view the asci and spores of morels, which have particularly large microscopic features, by slicing a thin section of the spore-bearing surface and using a tap-water mount (equipment required: garage-sale microscope; slide; cover slip; sharp razor blade; tap water; morel).

But if you want to go beyond having a little fun just seeing some or the larger microscopic features of mushrooms, you will need a microscope with an oil immersion lens, capable of magnifying things about 1,000 times-and the eyepiece of the microscope will need to have an ocular micrometer in it so that you can measure things. You will want an electric light source, controls to move the stage (the platform that holds the slide) mechanically, and a fine-focus knob (not just a single, coarse-focus knob).

You could buy a new microscope, of course. You can probably find new microscopes online that meet the requirements above for under $400 at the time of this writing (2019). However, and this is a big however, you cannot find a good new microscope for that price. With microscopes it is all about the lenses, and there are many knock-off, substandard lenses and microscopes out there. If you're going to make this investment, I recommend you get good lenses. Nikon. Olympus. Zeiss. Leica. We're not talking about handbags, where the reasons for getting the real Luis Vuitton as opposed to the "Luis Vuitton" the guy in the parking lot at the Leaning Tower of Pisa wanted to sell you are mostly social and legal. We're talking about the quality of your views of mushrooms.

. . . which probably means, if you're like me, that you can't afford a new microscope, since the good ones are much more than $400. It's a good thing, then, that a used microscope will work perfectly well, assuming it's in good condition. Good used microscopes can be found online, but I suspect that your best bet is to contact someone in one of the life science departments at a local university or community college. Former Biology 101 microscopes are not too hard to get hold of, and are often relatively cheap.
Calibrating a Microscope
The little ruler in the eyepiece of your microscope is divided up evenly into units-but those units do not necessarily correspond to anything in particular. You will need to compare the units on your microscope to the units on a special slide (called a "stage micrometer") that has known values on it. Most microscopic mushroom measurements are expressed in "micrometers," also called "microns." One micrometer is equal to 0.001 millimeter; the symbol for a micrometer is µm.

"Calibrating" your microscope is simply the process of comparing your yard-stick's units to the predetermined units on a special slide. Borrow the stage micrometer slide, if possible; you probably won't need to calibrate your microscope more than once. Once you have a conversion basis, you may need to do a little math every time you measure something. For example, if each unit on your yardstick equals 1.07 µm when you're using the highest magnification, a structure that measures 10 units long is 10.7 µm (roughly 11 µm) long. Or, if you're lucky, you may find that your highest magnification conversion is 1:1, in which case the math may not be needed (however, you will still need to calibrate your other lenses).
What other equipment will I need?
The obvious microscope things: slides, coverslips, extra bulbs, lens paper, and immersion oil. You will also need some very sharp razor blades, and some chemicals (see below).

Slides and coverslips are available from many sources, online and in brick-and-mortar stores. Your experience and preferences will dictate what kind of slides and cover slips you need. Glass cover slips are wonderful, but more expensive and easily broken. Plastic, disposable coverslips are much cheaper, but the view through them is inferior.

You will need lens paper to clean your oil immersion lens after each use. There are many online suppliers; also try your local camera shop, or your optometrist. Immersion oil can be purchased online, as well.
Chemicals, Reagents, and Stains
While water can be used to mount mycological specimens, features are often difficult to see without using stains and/or reagents that mycologists use. The bad news is, some of these chemicals can be very difficult to obtain (even for mycologists). At a minimum, you will probably need the chemicals below.

KOH (potassium hydroxide) is a strong base often used to study mushrooms. Although it is sometimes difficult to obtain, KOH can usually be purchased without too much difficulty. Several major online vendors have it available. KOH is used in a 2 percent aqueous solution as a mounting medium for microscopic examination of mushrooms. As a medium it often does a good job of clarifying mounts and making tissues and structures visible. It has its drawbacks (for example it tends to swell some structures) but it has been used for so long by mycologists that using it is necessary if one wants to compare data with their work.

Phloxine is a red stain, particularly good for making structures more visible. Phloxine is readily available from online retailers.

Melzer's reagent is an iodine-based stain regularly used in mycological microscope work to better see tissues and to determine whether spores and tissues are amyloid, inamyloid, or dextrinoid. It is unfortunately extremely difficult to obtain. Melzer's contains water, iodine, and potassium iodide, all of which are fairly easy to get hold of-but it also contains chloral hydrate, which is a controlled substance. Thus, you won't be able to buy it easily. Virtually your only option is to beg it from a professional mycologist. Even mycologists have difficulty obtaining Melzer's, however, and if the mycologist you know can't afford to provide you with some of her precious supply (or if you cannot find a mycologist), your last resort is to try explaining your situation to your doctor and getting a prescription for chloral hydrate (not likely; it's a date-rape drug) or for Melzer's reagent itself, which a compounding pharmacist could mix according to the formula below, and which your doctor would need to write on the prescription (still not very likely, but not unheard of).

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Using a Microscope to Study Mushrooms (MushroomExpert.Com)

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What kind of microscope do I need, and where do I get it? You'll need a pretty good microscope.