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A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life

Nature Biotechnology volume 36, pages 996–1004 (2018)Cite this article

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Abstract

Taxonomy is an organizing principle of biology and is ideally based on evolutionary relationships among organisms. Development of a robust bacterial taxonomy has been hindered by an inability to obtain most bacteria in pure culture and, to a lesser extent, by the historical use of phenotypes to guide classification. Culture-independent sequencing technologies have matured sufficiently that a comprehensive genome-based taxonomy is now possible. We used a concatenated protein phylogeny as the basis for a bacterial taxonomy that conservatively removes polyphyletic groups and normalizes taxonomic ranks on the basis of relative evolutionary divergence. Under this approach, 58% of the 94,759 genomes comprising the Genome Taxonomy Database had changes to their existing taxonomy. This result includes the description of 99 phyla, including six major monophyletic units from the subdivision of the Proteobacteria, and amalgamation of the Candidate Phyla Radiation into a single phylum. Our taxonomy should enable improved classification of uncultured bacteria and provide a sound basis for ecological and evolutionary studies.

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Figure 1: Rank normalization through RED.
Figure 2: RED of NCBI and GTDB taxa in a genome tree inferred from 120 concatenated proteins.
Figure 3: RED and polyphyly of GTDB and NCBI taxa on trees inferred by using varying inference methods and marker sets.
Figure 4: Comparison of GTDB and NCBI taxonomies and naming status of GTDB taxa.
Figure 5: Comparisons of NCBI and GTDB classifications of genomes designated as Clostridia or Bacteroidetes in the GTDB taxonomy.

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Acknowledgements

We thank P. Yilmaz for helpful discussions on the proposed genome-based taxonomy; QFAB Bioinformatics for providing computational resources; and members of ACE for beta-testing GTDB. The project was primarily supported by an Australian Research Council Laureate Fellowship (FL150100038) awarded to P.H.

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  1. Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, Queensland, Australia

    Donovan H Parks, Maria Chuvochina, David W Waite, Christian Rinke, Adam Skarshewski, Pierre-Alain Chaumeil & Philip Hugenholtz

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  1. Donovan H Parks
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  2. Maria Chuvochina
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Contributions

D.H.P., D.W.W. and P.H. wrote the paper, and all other authors provided constructive suggestions. D.H.P. and P.H. designed the study. M.C. and P.H. performed the taxonomic curation. D.H.P., D.W.W., C.R., A.S., and P.-A.C. performed the bioinformatic analyses. P.-A.C. designed the website.

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Correspondence to Philip Hugenholtz.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Congruence of the GTDB taxonomy on a tree inferred with ExaML from the concatenation of 120 proteins (bac120) and species-dereplicated genome set.

Percentage of GTDB taxa at each rank which are monophyletic, operationally monophyletic, or polyphyletic within the ExaML tree. Results were calculated over all taxa comprised of >1 genomes and the number of taxa considered at each rank is shown in parentheses. (b) Percentage of the 10,462 genomes within the ExaML tree with identical, unresolved, or conflicting taxonomic assignments at each rank relative to the GTDB taxonomy when taxonomy is assigned based on their placement in the inferred tree. (c) RED of taxa with ≥2 immediate subordinate taxa in the ExaML tree, with the same coloring as used in panel a. The number of taxa plotted at each rank is given in parentheses.

Supplementary Figure 2 Congruence of the GTDB taxonomy on a tree inferred with FastTree from the concatenation of 16 ribosomal proteins (rp1).

(a) Percentage of GTDB taxa at each rank which are monophyletic, operationally monophyletic, or polyphyletic within the rp1 tree. Results were calculated over all taxa comprised of >1 genomes and the number of taxa considered at each rank is shown in parentheses. (b) Percentage of the 20,699 genomes within the rp1 tree with identical, unresolved, or conflicting taxonomic assignments at each rank relative to the GTDB taxonomy when taxonomy is assigned based on their placement in the inferred tree. (c) RED of taxa with ≥2 immediate subordinate taxa in the rp1 tree, with the same coloring as used in panel a. The number of taxa plotted at each rank is given in parentheses.

Supplementary Figure 3 Congruence of the GTDB taxonomy on a tree inferred with FastTree by using the 16S rRNA gene.

(a) Percentage of GTDB taxa at each rank which are monophyletic, operationally monophyletic, or polyphyletic within the 16S rRNA gene tree. Results were calculated over all taxa comprised of >1 genomes and the number of taxa considered at each rank is shown in parentheses. (b) Percentage of the 12,435 genomes within the 16S rRNA gene tree with identical, unresolved, or conflicting taxonomic assignments at each rank relative to the GTDB taxonomy when taxonomy is assigned based on their placement in the inferred gene tree. (c) RED of taxa with ≥2 immediate subordinate taxa in the 16S rRNA gene tree, with the same coloring as used in panel a. The number of taxa plotted at each rank is given in parentheses.

Supplementary Figure 4 Congruence of the NCBI taxonomy on a tree inferred with ExaML from the concatenation of 120 proteins (bac120) and species-dereplicated genome set.

(a) Percentage of NCBI taxa at each rank which are monophyletic, operationally monophyletic, or polyphyletic within the ExaML tree. Results were calculated over all taxa comprised of >1 genomes and the number of taxa considered at each rank is shown in parentheses. (b) Percentage of the 8,905 RefSeq/GenBank genomes within the ExaML tree with identical, unresolved, or conflicting taxonomic assignments at each rank relative to the NCBI taxonomy when taxonomy is assigned based on their placement in the inferred tree. (c) RED of taxa with ≥2 immediate subordinate taxa in the ExaML tree, with the same coloring as used in panel a. The number of taxa plotted at each rank is given in parentheses.

Supplementary Figure 5 Congruence of the NCBI taxonomy on a tree inferred with FastTree from the concatenation of 120 proteins (bac120).

(a) Percentage of NCBI taxa at each rank which are monophyletic, operationally monophyletic, or polyphyletic within the bac120 tree. Results were calculated over all taxa comprised of >1 genomes and the number of taxa considered at each rank is shown in parentheses. (b) Percentage of the 16,248 RefSeq/GenBank genomes within the bac120 tree with identical, unresolved, or conflicting taxonomic assignments at each rank relative to the NCBI taxonomy when taxonomy is assigned based on their placement in the inferred tree. (c) RED of taxa with ≥2 immediate subordinate taxa in the bac120 tree, with the same coloring as used in panel a. The number of taxa plotted at each rank is given in parentheses (note that this is a reproduction of Fig. 2a).

Supplementary Figure 6 Congruence of the NCBI taxonomy on a tree inferred with FastTree from the concatenation of 16 ribosomal proteins (rp1).

(a) Percentage of NCBI taxa at each rank which are monophyletic, operationally monophyletic, or polyphyletic within the rp1 tree. Results were calculated over all taxa comprised of >1 genomes and the number of taxa considered at each rank is shown in parentheses. (b) Percentage of the 16,306 RefSeq/GenBank genomes within the rp1 tree with identical, unresolved, or conflicting taxonomic assignments at each rank relative to the NCBI taxonomy when taxonomy is assigned based on their placement in the inferred tree. (c) RED of taxa with ≥2 immediate subordinate taxa in the rp1 tree, with the same coloring as used in panel a. The number of taxa plotted at each rank is given in parentheses.

Supplementary Figure 7 Congruence of the NCBI taxonomy on a tree inferred with FastTree by using the 16S rRNA gene.

(a) Percentage of NCBI taxa at each rank which are monophyletic, operationally monophyletic, or polyphyletic within the 16S rRNA gene tree. Results were calculated over all taxa comprised of >1 genomes and the number of taxa considered at each rank is shown in parentheses. (b) Percentage of the 12,174 RefSeq/GenBank genomes within the 16S rRNA gene tree with identical, unresolved, or conflicting taxonomic assignments at each rank relative to the NCBI taxonomy when taxonomy is assigned based on their placement in the inferred gene tree. (c) RED of taxa with ≥2 immediate subordinate taxa in the 16S rRNA gene tree, with the same coloring as used in panel a. The number of taxa plotted at each rank is given in parentheses.

Supplementary Figure 8 Comparison of GTDB and SILVA.

Comparison of GTDB and SILVA taxonomic assignments across 10,779 bacterial genomes from RefSeq/GenBank release 80. These genomes are part of the 21,943 dereplicated genomes for which a 16S rRNA gene could be reliably matched by sequence similarity to a 16S rRNA gene in SILVA release 128. For each rank, a taxon was classified as being unchanged if its name was identical in both taxonomies, passively changed if the GTDB taxonomy provided name information absent in the SILVA taxonomy, or actively changed if the name was different between the two taxonomies after adjusting the SILVA taxonomy for colloquial designations indicating of missing taxonomic information (see Methods). Changes between the GTDB and SILVA taxonomies are given in Supp. Table 9.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–8 (PDF 1124 kb)

Life Sciences Reporting Summary (PDF 89 kb)

Supplementary Table 1

Robustness of GTDB taxonomy under varying marker sets, maximum-likelihood tree inference software, subsets of taxa, and evolutionary models (XLSX 4427 kb)

Supplementary Table 2

16S rRNA-based taxa names adopted in the GTDB taxonomy and their associated rank and number of circumscribed genomes. (XLSX 12 kb)

Supplementary Table 3

Correspondence between standardly named NCBI and GTDB taxa ordered by degree of polyphyly. (XLSX 131 kb)

Supplementary Table 4

Taxa found to be polyphyletic in one or more of the trees inferred with FastTree, IQ-TREE, or ExaML on species- or genusdereplicated genome sets, or in trees inferred with FastTree using the ribosomal proteins (rp1) marker set or 16S rRNA gene. (XLSX 57 kb)

Supplementary Table 5

Genomes with conflicting or unresolved taxonomic assignments when applying the GTDB taxonomy to the species-dereplicated FastTree, IQ-TREE, or ExaML trees, or trees inferred from the concatenation of 16 ribosomal proteins (rp1) or the 16S rRNA gene. (XLSX 129 kb)

Supplementary Table 6

Pairwise comparison of trees inferred with varying inference methods and marker sets. (XLSX 13 kb)

Supplementary Table 7

Percentage of GTDB taxa at each taxonomic rank that are monophyletic, operationally monophyletic, or polyphyletic in each gene within the bac120 marker set. (XLSX 30 kb)

Supplementary Table 8

NCBI taxa that have been 'retired' in the GTDB taxonomy and brief explanations for their retirement. (XLSX 18 kb)

Supplementary Table 9

Correspondence between NCBI and SILVA taxa ordered by degree of polyphyly. (XLSX 59 kb)

Supplementary Table 10

Comparison of NCBI and GTDB genus and species classifications to those proposed by Beaz-Hidalgo et al. (2015), Kook et al. (2017), and Bobay & Ochman (2017). (XLSX 14 kb)

Supplementary Table 11

Comparison of clostridia classifications proposed by Yutin & Galperin (2013) to the GTDB taxonomy. (XLSX 20 kb)

Supplementary Table 12

Draft genomes with 16S rRNA genes that did not meet the selection criteria for inclusion in the 16S rRNA tree (Online Methods). (XLSX 33 kb)

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Parks, D., Chuvochina, M., Waite, D. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat Biotechnol 36, 996–1004 (2018). https://doi.org/10.1038/nbt.4229

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