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Learn about how the tree of life is organized and how it has changed over the years.

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Letter | Open

Nature Microbiology 1, Article number: 16048 (2016)

doi:10.1038/nmicrobiol.2016.48

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Early approaches to describe the tree of life distinguished organisms based on their physical characteristics and metabolic features. Molecular methods dramatically broadened the diversity that could be included in the tree because they circumvented the need for direct observation and experimentation by relying on sequenced genes as markers for lineages. Gene surveys, typically using the small subunit ribosomal RNA (SSU rRNA) gene, provided a remarkable and novel view of the biological world, but questions about the structure and extent of diversity remain. Organisms from novel lineages have eluded surveys, because many are invisible to these methods due to sequence divergence relative to the primers commonly used for gene amplification. Furthermore, unusual sequences, including those with unexpected insertions, may be discarded as artefacts.

Whole genome reconstruction was first accomplished in 1995 (ref. 12), with a near-exponential increase in the number of draft genomes reported each subsequent year. There are 30,437 genomes from all three domains of life-Bacteria, Archaea and Eukarya-which are currently available in the Joint Genome Institute's Integrated Microbial Genomes database (accessed 24 September 2015). Contributing to this expansion in genome numbers are single cell genomics and metagenomics studies. Metagenomics is a shotgun sequencing-based method in which DNA isolated directly from the environment is sequenced, and the reconstructed genome fragments are assigned to draft genomes. New bioinformatics methods yield complete and near-complete genome sequences, without a reliance on cultivation or reference genomes. These genome- (rather than gene) based approaches provide information about metabolic potential and a variety of phylogenetically informative sequences that can be used to classify organisms. Here, we have constructed a tree of life by making use of genomes from public databases and 1,011 newly reconstructed genomes that we recovered from a variety of environments (see Methods).

To render this tree of life, we aligned and concatenated a set of 16 ribosomal protein sequences from each organism. This approach yields a higher-resolution tree than is obtained from a single gene, such as the widely used 16S rRNA gene. The use of ribosomal proteins avoids artefacts that would arise from phylogenies constructed using genes with unrelated functions and subject to different evolutionary processes. Another important advantage of the chosen ribosomal proteins is that they tend to be syntenic and co-located in a small genomic region in Bacteria and Archaea, reducing binning errors that could substantially perturb the geometry of the tree. Included in this tree is one representative per genus for all genera for which high-quality draft and complete genomes exist (3,083 organisms in total).

Despite the methodological challenges, we have included representatives of all three domains of life. Our primary focus relates to the status of Bacteria and Archaea, as these organisms have been most difficult to profile using macroscopic approaches, and substantial progress has been made recently with acquisition of new genome sequences. The placement of Eukarya relative to Bacteria and Archaea is controversial. Eukaryotes are believed to be evolutionary chimaeras that arose via endosymbiotic fusion, probably involving bacterial and archaeal cells. Here, we do not attempt to confidently resolve the placement of the Eukarya. We position them using sequences of a subset of their nuclear-encoded ribosomal proteins, an approach that classifies them based on the inheritance of their information systems as opposed to lipid or other cellular structures.

Figure 1 presents a new view of the tree of life. This is one of a relatively small number of three-domain trees constructed from molecular information so far, and the first comprehensive tree to be published since the development of genome-resolved metagenomics. We highlight all major lineages with genomic representation, most of which are phylum-level branches (see Supplementary Fig. 1 for full bootstrap support values). However, we separately identify the Classes of the Proteobacteria, because the phylum is not monophyletic (for example, the Deltaproteobacteria branch away from the other Proteobacteria, as previously reported).

Figure 1: A current view of the tree of life, encompassing the total diversity represented by sequenced genomes.

The tree includes 92 named bacterial phyla, 26 archaeal phyla and all five of the Eukaryotic supergroups. Major lineages are assigned arbitrary colours and named, with well-characterized lineage names, in italics. Lineages lacking an isolated representative are highlighted with non-italicized names and red dots. For details on taxon sampling and tree inference, see Methods. The names Tenericutes and Thermodesulfobacteria are bracketed to indicate that these lineages branch within the Firmicutes and the Deltaproteobacteria, respectively. Eukaryotic supergroups are noted, but not otherwise delineated due to the low resolution of these lineages. The CPR phyla are assigned a single colour as they are composed entirely of organisms without isolated representatives, and are still in the process of definition at lower taxonomic levels. The complete ribosomal protein tree is available in rectangular format with full bootstrap values as Supplementary Fig. 1 and in Newick format in Supplementary Dataset 2.

The tree in Fig. 1 recapitulates expected organism groupings at most taxonomic levels and is largely congruent with the tree calculated using traditional SSU rRNA gene sequence information ( Supplementary Fig. 2). The support values for taxonomic groups are strong at the Species through Class levels (>85%), with moderate-to-strong support for Phyla (>75% in most cases), but the branching order of the deepest branches cannot be confidently resolved ( Supplementary Fig. 1). The lower support for deep branch placements is a consequence of our prioritization of taxon sampling over number of genes used for tree construction. As proposed recently, the Eukarya, a group that includes protists, fungi, plants and animals, branches within the Archaea, specifically within the TACK superphylum and sibling to the Lokiarchaeota. Interestingly, this placement is not evident in the SSU rRNA tree, which has the three-domain topology proposed by Woese and co-workers in 1990 ( Supplementary Fig. 2). The two-domain Eocyte tree and the three-domain tree are competing hypotheses for the origin of Eukarya; further analyses to resolve these and other deep relationships will be strengthened with the availability of genomes for a greater diversity of organisms. Important advantages of the ribosomal protein tree compared with the SSU rRNA gene tree are that it includes organisms with incomplete or unavailable SSU rRNA gene sequences and more strongly resolves the deeper radiations. Ribosomal proteins have been shown to contain compositional biases across the three domains, driven by thermophilic, mesophilic and halophilic lifestyles as well as by a primitive genetic code. Continued expansion of the number of genome sequences for non-extremophile Archaea, such as the DPANN lineages, may allow clarification of these compositional biases.

A striking feature of this tree is the large number of major lineages without isolated representatives (red dots in Fig. 1). Many of these lineages are clustered together into discrete regions of the tree. Of particular note is the Candidate Phyla Radiation (CPR), highlighted in purple in Fig. 1. Based on information available from hundreds of genomes from genome-resolved metagenomics and single-cell genomics methods to date, all members have relatively small genomes and most have somewhat (if not highly) restricted metabolic capacities. Many are inferred (and some have been shown) to be symbionts. Thus far, all cells lack complete citric acid cycles and respiratory chains and most have limited or no ability to synthesize nucleotides and amino acids. It remains unclear whether these reduced metabolisms are a consequence of superphylum-wide loss of capacities or if these are inherited characteristics that hint at an early metabolic platform for life. If inherited, then adoption of symbiotic lifestyles may have been a later innovation by these organisms once more complex organisms appeared.

Figure 2 presents another perspective, where the major lineages of the tree are defined using evolutionary distance, so that the main groups become apparent without bias arising from historical naming conventions. This depiction uses the same inferred tree as in Fig. 1, but with groups defined on the basis of average branch length to the leaf taxa. We chose an average branch length that best recapitulated the current taxonomy (smaller values fragmented many currently accepted phyla and larger values collapsed accepted phyla into very few lineages, see Methods). Evident in Fig. 2 is the enormous extent of evolution that has occurred within the CPR. The diversity within the CPR could be a result of the early emergence of this group and/or a consequence of rapid evolution related to symbiotic lifestyles. The CPR is early-emerging on the ribosomal protein tree ( Fig. 1), but not in the SSU rRNA tree ( Supplementary Fig. 2). Regardless of branching order, the CPR, in combination with other lineages that lack isolated representatives (red dots in Fig. 2), clearly comprises the majority of life's current diversity.

Figure 2: A reformatted view of the tree in Fig. 1in which each major lineage represents the same amount of evolutionary distance.

The threshold for groups (coloured wedges) was an average branch length of <0.65 substitutions per site. Notably, some well-accepted phyla become single groups and others are split into multiple distinct groups. We undertook this analysis to provide perspective on the structure of the tree, and do not propose the resulting groups to have special taxonomic status. The massive scale of diversity in the CPR and the large fraction of major lineages that lack isolated representatives (red dots) are apparent from this analysis. Bootstrap support values are indicated by circles on nodes-black for support of 85% and above, grey for support from 50 to 84%. The complete ribosomal protein tree is available in rectangular format with full bootstrap values as Supplementary Fig. 1 and in Newick format in Supplementary Dataset 2.

Domain Bacteria includes more major lineages of organisms than the other Domains. We do not attribute the smaller scope of the Archaea relative to Bacteria to sampling bias because metagenomics and single-cell genomics methods detect members of both domains equally well. Consistent with this view, Archaea are less prominent and less diverse in many ecosystems (for example, seawater, hydrothermal vents, the terrestrial subsurface and human-associated microbiomes). The lower apparent phylogenetic diversity of Eukarya is fully expected, based on their comparatively recent evolution.

The tree of life as we know it has dramatically expanded due to new genomic sampling of previously enigmatic or unknown microbial lineages. This depiction of the tree captures the current genomic sampling of life, illustrating the progress that has been made in the last two decades following the first published genome. What emerges from analysis of this tree is the depth of evolutionary history that is contained within the Bacteria, in part due to the CPR, which appears to subdivide the domain. Most importantly, the analysis highlights the large fraction of diversity that is currently only accessible via cultivation-independent genome-resolved approaches.

This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

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An update to the 'tree of life' has revealed a dominance of bacterial diversity in many ecosystems and extensive evolution in some branches of the tree. It also highlights how few organisms we have been able to cultivate for further investigation.

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