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A standardized archaeal taxonomy for the Genome Taxonomy Database

Nature Microbiology volume 6, pages 946–959 (2021)Cite this article

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Abstract

The accrual of genomic data from both cultured and uncultured microorganisms provides new opportunities to develop systematic taxonomies based on evolutionary relationships. Previously, we established a bacterial taxonomy through the Genome Taxonomy Database. Here, we propose a standardized archaeal taxonomy that is derived from a 122-concatenated-protein phylogeny that resolves polyphyletic groups and normalizes ranks based on relative evolutionary divergence. The resulting archaeal taxonomy, which forms part of the Genome Taxonomy Database, is stable for a range of phylogenetic variables including marker gene selection, inference methods, corrections for rate heterogeneity and compositional bias, tree rooting scenarios and expansion of the genome database. Rank normalization is shown to robustly correct for substitution rates varying up to 30-fold using simulated datasets. Taxonomic curation follows the rules of the International Code of Nomenclature of Prokaryotes while taking into account proposals to formally recognize the rank of phylum and to use genome sequences as type material. This taxonomy is based on 2,392 archaeal genomes, 93.3% of which required one or more changes to their existing taxonomy, mainly owing to incomplete classification. We identify 16 archaeal phyla and reclassify 3 major monophyletic units from the former Euryarchaeota and one phylum that unites the Thaumarchaeota–Aigarchaeota–Crenarchaeota–Korarchaeota (TACK) superphylum into a single phylum.

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Fig. 1: Comparison of rank-normalized archaeal GTDB and NCBI taxonomies.
Fig. 2: Comparison of marker sets, inference methods and models.
Fig. 3: Impact of different rooting scenarios on RED intervals.
Fig. 4: Rank-normalized archaeal GTDB taxonomy.
Fig. 5: Reclassification of the Thaumarchaeota.

Data availability

The GTDB taxonomy is available at the GTDB website (https://gtdb.ecogenomic.org/), including the ar122.r89 tree and the GTDB and NCBI taxonomic assignments for all 2,392 archaeal genomes in GTDB 04-RS89. Genome assemblies are available from the NCBI Assembly database (BioProject: PRJNA593905). All GTDB decorated phylogenetic trees are provided as Newick files in Supplementary Data 1. The SR4 model used for data recoded inferences is provided in Supplementary Data 2. Source data are provided with this paper.

Code availability

The standalone tool GTDB-Tk, which enables researchers to classify their own genomes according to the GTDB taxonomy, is available from GitHub (https://github.com/Ecogenomics/GTDBTk/) and through KBase (https://kbase.us/applist/apps/kb_gtdbtk/run_kb_gtdbtk/release). Taxonomic assignment and rank standardization were carried out based on the RED calculated using PhyloRank v0.0.37, which is available from GitHub (https://github.com/dparks1134/PhyloRank/).

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Acknowledgements

We thank B. Kemish and D. Senanayake for system administration support, P. Yilmaz for stimulating discussions on archaeal taxonomy and the GTDB user community for their feedback. We also thank the Australian Centre for Ecogenomics (ACE) at The University of Queensland and the New Zealand eScience Infrastructure (NeSI) for providing high-performance computing facilities. The project was supported by an Australian Research Council (ARC) Future Fellowship (FT170100213) awarded to C.R. and by an Australian Research Council Laureate Fellowship (FL150100038) awarded to P.H. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information

Authors and Affiliations

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

    Christian Rinke, Maria Chuvochina, Aaron J. Mussig, Pierre-Alain Chaumeil, Adrián A. Davín, Donovan H. Parks & Philip Hugenholtz

  2. School of Biological Sciences, The University of Auckland, Auckland, New Zealand

    David W. Waite

  3. Department of Microbiology, University of Georgia, Athens, GA, USA

    William B. Whitman

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  1. Christian Rinke
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Contributions

P.H., C.R. and D.H.P. conceived the archaeal GTDB study and designed experiments. C.R., A.J.M., D.H.P. and D.W.W. performed phylogenetic inferences. D.H.P. and P.-A.C. calculated rank normalizations. D.H.P., P.-A.C. and A.J.M. created the GTDB web interface and underlying databases. M.C., C.R., P.H. and W.B.W. curated the GTDB taxonomy with input from all co-authors and the scientific community. A.A.D. performed the RED simulation analysis. C.R. and P.H. wrote the manuscript with contributions from all co-authors.

Corresponding authors

Correspondence to Christian Rinke or Philip Hugenholtz.

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The authors declare no competing interests.

Additional information

Peer review information Nature Microbiology thanks the anonymous reviewers for their contribution to the peer review of this work.

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Extended data

Extended Data Fig. 1 Implementing the shifting substitution rate model (SSR).

a, Timetree, that is a tree scaled to time. A grid has been overlayed on top of the tree to delineate the length of the individual branch segments. b, An array of substitution rate multipliers, ordered from lowest to highest. In this specific example, the slowest evolving lineage evolves 16 times more slowly than the fastest evolving lineage. c, The result of running the SSR model on the tree in a. Every circle represents a shift in the substitution rate, whereby the colour correlates to the substitution rates multipliers shown in c). At the start of the simulation the model starts with the grey circle. How quick the changes take place depend on the shifting substitution rate parameter. d, The result of taking the tree in a) and scaling it according to the active substitution rate multiplier in every branch at every branch segment. For instance, we can see that the single segment in dark red (x4) has the same length as the two prior segments in light red (x2) on the same branch.

Extended Data Fig. 2 Impact of variable evolutionary rates on the RED approach.

Each panel shows the true ranking of every inner node of the species tree (which we can directly obtain from the simulation) and the x-axis, and the inferred rankings of every node, resulting of modifying the branch lengths of the tree using the SSR model and subsequently applying the RED algorithm to recover an ultrametric tree, on the y-axis. The main diagonal corresponds therefore to the proportion of nodes for the ranking given by the column that has been correctly classified. In every panel we have the results of using a different shifting substitution rate, from 0.1 to 0.5, and 1 (events/speciation). These results show that, as expected, higher numbers of changes in the substitution rates impact the performance of the RED approach to a higher degree. However, the levels of accuracy remain high even for the most extreme cases.

Extended Data Fig. 3 Average number of monophyletic (green bars), operationally monophyletic (yellow bars) and polyphyletic (orange bars) taxa across higher ranks (phylum, class, and order) in percent.

Shown are GTDB taxonomy decorated phylogenetic trees inferred with different methods, from a range of markers, from alignments trimmed to reduce compositional bias and fast evolving sites, and from alignments created as part of the simulated database expansion. Note that only taxa with two or more genomes were included, and that the data set (order representatives) used for PhyloBayes restricts the analysis to the ranks of phylum and class. Details for each inferred tree are provided in Supplementary Table 10. Percentages for all ranks are shown in Supplementary Fig. 11. Monophyly and operational monophyly was determined based on the F measure of decorated internal nodes.

Extended Data Fig. 4 Higher rank GTDB lineages not resolved with alternative inference methods.

Shown are taxa that were not recovered as monophyletic or operational monophyletic (green) and hence were polyphyletic (red; F measure < 0.95) in at least one of the different alignments and inference methods. The bootstrap support for each taxon in the ar.122.r89 reference tree is given in the last column ‘BS in ar.122.r89 tree’.

Extended Data Fig. 5 Examples of application of names using the manual curation workflow.

Provided are five examples of taxon names that have been updated in GTDB following the manual curation workflow. Thereby, each example is shown in a distinct colour: Ca. Thaumarchaeota (red), Ca. Diapherotrites (blue), Ca. Bathyarchaeota (green), Ca. Verstraetearchaeota (purple), and Ca. Korarchaeota (orange). For example, Ca. Thaumarchaeota (red) has no designated nomenclature type and has no lower-ranking taxon based on the same stem as the taxon. Furthermore, it has been united with another taxon of the same rank in GTDB, which resulted in a name being chosen based on priority, in this case Thermoproteota. *Nomenclature type of the taxon (for ranks above genus) is defined as one of its subordinate taxa with which the name is permanently associated.

Supplementary information

Supplementary Information

Supplementary Figs. 1–21, Tables 13–18 and Notes 1–7.

Reporting Summary

Peer Review File

Supplementary Tables

Supplementary Tables 1–14 and 19–29.

Supplementary Data 1

Newick files of all GTDB decorated trees.

Supplementary Data 2

SR4 model used for data recoded inferences.

Source data

Source Data Fig. 1

Tab delimited table of the data used to create the plots.

Source Data Fig. 2

Tab delimited table of the data used to create the plots.

Source Data Fig. 3

Newick files of the phylogenetic trees.

Source Data Fig. 4

Newick file of the phylogenetic tree.

Source Data Fig. 5

Newick file of the phylogenetic tree.

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Rinke, C., Chuvochina, M., Mussig, A.J. et al. A standardized archaeal taxonomy for the Genome Taxonomy Database. Nat Microbiol 6, 946–959 (2021). https://doi.org/10.1038/s41564-021-00918-8

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