A standardized archaeal taxonomy for the Genome Taxonomy Database.
Journal
Nature microbiology
ISSN: 2058-5276
Titre abrégé: Nat Microbiol
Pays: England
ID NLM: 101674869
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
10
03
2020
accepted:
10
05
2021
pubmed:
23
6
2021
medline:
21
9
2021
entrez:
22
6
2021
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 34155373
doi: 10.1038/s41564-021-00918-8
pii: 10.1038/s41564-021-00918-8
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
946-959Références
Woese, C. R. & Fox, G. E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc. Natl Acad. Sci. USA 74, 5088–5090 (1977).
pubmed: 270744
pmcid: 432104
doi: 10.1073/pnas.74.11.5088
Gribaldo, S. & Brochier-Armanet, C. The origin and evolution of Archaea: a state of the art. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1007–1022 (2006).
pubmed: 16754611
pmcid: 1578729
doi: 10.1098/rstb.2006.1841
Zuo, G., Xu, Z. & Hao, B. Phylogeny and taxonomy of Archaea: a comparison of the whole-genome-based CVTree approach with 16S rRNA sequence analysis. Life 5, 949–968 (2015).
pubmed: 25789552
pmcid: 4390887
doi: 10.3390/life5010949
Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576–4579 (1990).
pubmed: 2112744
pmcid: 54159
doi: 10.1073/pnas.87.12.4576
Adam, P. S., Borrel, G., Brochier-Armanet, C. & Gribaldo, S. The growing tree of Archaea: new perspectives on their diversity, evolution and ecology. ISME J. https://doi.org/10.1038/ismej.2017.122 (2017).
Baker, B. J. et al. Diversity, ecology and evolution of Archaea. Nat. Microbiol. 5, 887–900 (2020).
pubmed: 32367054
doi: 10.1038/s41564-020-0715-z
Spang, A., Caceres, E. F. & Ettema, T. J. G. Genomic exploration of the diversity, ecology, and evolution of the archaeal domain of life. Science 357, eaaf3883 (2017).
pubmed: 28798101
doi: 10.1126/science.aaf3883
Barns, S. M., Delwiche, C. F., Palmer, J. D. & Pace, N. R. Perspectives on archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc. Natl Acad. Sci. USA 93, 9188–9193 (1996).
pubmed: 8799176
pmcid: 38617
doi: 10.1073/pnas.93.17.9188
Huber, H. et al. A new phylum of Archaea represented by a nanosized hyperthermophilic symbiont. Nature 417, 63–67 (2002).
pubmed: 11986665
doi: 10.1038/417063a
Hallam, S. J. et al. Genomic analysis of the uncultivated marine crenarchaeote Cenarchaeum symbiosum. Proc. Natl Acad. Sci. USA 103, 18296–18301 (2006).
pubmed: 17114289
pmcid: 1643844
doi: 10.1073/pnas.0608549103
Brochier-Armanet, C., Boussau, B., Gribaldo, S. & Forterre, P. Mesophilic crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat. Rev. Microbiol. 6, 245–252 (2008).
pubmed: 18274537
doi: 10.1038/nrmicro1852
Nunoura, T. et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res. 39, 3204–3223 (2011).
pubmed: 21169198
doi: 10.1093/nar/gkq1228
Kozubal, M. A. et al. Geoarchaeota: a new candidate phylum in the Archaea from high-temperature acidic iron mats in Yellowstone National Park. ISME J. 7, 622–634 (2013).
pubmed: 23151644
doi: 10.1038/ismej.2012.132
Meng, J. et al. Genetic and functional properties of uncultivated MCG Archaea assessed by metagenome and gene expression analyses. ISME J. 8, 650–659 (2014).
pubmed: 24108328
doi: 10.1038/ismej.2013.174
Guy, L., Spang, A., Saw, J. H. & Ettema, T. J. G. ‘Geoarchaeote NAG1’ is a deeply rooting lineage of the archaeal order Thermoproteales rather than a new phylum. ISME J. 8, 1353–1357 (2014).
pubmed: 24522265
pmcid: 4069404
doi: 10.1038/ismej.2014.6
Guy, L. & Ettema, T. J. G. The archaeal ‘TACK’ superphylum and the origin of eukaryotes. Trends Microbiol. 19, 580–587 (2011).
pubmed: 22018741
doi: 10.1016/j.tim.2011.09.002
Vanwonterghem, I. et al. Methylotrophic methanogenesis discovered in the archaeal phylum Verstraetearchaeota. Nat. Microbiol. 1, 16170 (2016).
pubmed: 27694807
doi: 10.1038/nmicrobiol.2016.170
Rinke, C. et al. Insights into the phylogeny and coding potential of microbial dark matter. Nature 499, 431–437 (2013).
Zaremba-Niedzwiedzka, K. et al. Asgard Archaea illuminate the origin of eukaryotic cellular complexity. Nature 541, 353–358 (2017).
pubmed: 28077874
doi: 10.1038/nature21031
Baker, B. J. et al. Enigmatic, ultrasmall, uncultivated Archaea. Proc. Natl Acad. Sci. USA 107, 8806–8811 (2010).
pubmed: 20421484
pmcid: 2889320
doi: 10.1073/pnas.0914470107
Castelle, C. J. et al. Genomic expansion of domain Archaea highlights roles for organisms from new phyla in anaerobic carbon cycling. Curr. Biol. 16, 690–701 (2015).
doi: 10.1016/j.cub.2015.01.014
Probst, A. J. et al. Differential depth distribution of microbial function and putative symbionts through sediment-hosted aquifers in the deep terrestrial subsurface. Nat. Microbiol. 3, 328–336 (2018).
pubmed: 29379208
pmcid: 6792436
doi: 10.1038/s41564-017-0098-y
Probst, A. J. et al. Biology of a widespread uncultivated archaeon that contributes to carbon fixation in the subsurface. Nat. Commun. 5, 5497 (2014).
pubmed: 25425419
doi: 10.1038/ncomms6497
Seitz, K. W., Lazar, C. S., Hinrichs, K.-U., Teske, A. P. & Baker, B. J. Genomic reconstruction of a novel, deeply branched sediment archaeal phylum with pathways for acetogenesis and sulfur reduction. ISME J. 10, 1696–1705 (2016).
pubmed: 26824177
pmcid: 4918440
doi: 10.1038/ismej.2015.233
Spang, A. et al. Complex Archaea that bridge the gap between prokaryotes and eukaryotes. Nature 521, 173–179 (2015).
pubmed: 25945739
pmcid: 4444528
doi: 10.1038/nature14447
Seitz, K. W. et al. Asgard Archaea capable of anaerobic hydrocarbon cycling. Nat. Commun. 10, 1822 (2019).
pubmed: 31015394
pmcid: 6478937
doi: 10.1038/s41467-019-09364-x
Petitjean, C., Deschamps, P., López-García, P. & Moreira, D. Rooting the domain Archaea by phylogenomic analysis supports the foundation of the new kingdom Proteoarchaeota. Genome Biol. Evol. 7, 191–204 (2014).
pubmed: 25527841
pmcid: 4316627
doi: 10.1093/gbe/evu274
Petitjean, C., Deschamps, P., López-García, P., Moreira, D. & Brochier-Armanet, C. Extending the conserved phylogenetic core of Archaea disentangles the evolution of the third domain of life. Mol. Biol. Evol. 32, 1242–1254 (2015).
pubmed: 25660375
doi: 10.1093/molbev/msv015
Parker, C. T., Tindall, B. J. & Garrity, G. M. International Code of Nomenclature of Prokaryotes. Int. J. Syst. Evol. Microbiol. 69, S1–S111 (2019).
doi: 10.1099/ijsem.0.000778
Oren, A. et al. Proposal to include the rank of phylum in the International Code of Nomenclature of Prokaryotes. Int. J. Syst. Evol. Microbiol. 65, 4284–4287 (2015).
pubmed: 26654112
doi: 10.1099/ijsem.0.000664
Whitman, W. B. Modest proposals to expand the type material for naming of prokaryotes. Int. J. Syst. Evol. Microbiol. 66, 2108–2112 (2016).
pubmed: 26902077
doi: 10.1099/ijsem.0.000980
Chuvochina, M. et al. The importance of designating type material for uncultured taxa. Syst. Appl. Microbiol. 42, 15–21 (2019).
pubmed: 30098831
doi: 10.1016/j.syapm.2018.07.003
Murray, R. G. E. & Stackebrandt, E. Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int. J. Syst. Evol. Microbiol. 45, 186–187 (1995).
Oren, A. A plea for linguistic accuracy—also for Candidatus taxa. Int. J. Syst. Evolut. Microbiol. 67, 1085–1094 (2017).
doi: 10.1099/ijsem.0.001715
Parks, D. H. et al. A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life. Nat. Biotechnol. 36, 996–1004 (2018).
pubmed: 30148503
doi: 10.1038/nbt.4229
Parks, D. H. et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat. Biotechnol. 38, 1079–1086 (2020).
pubmed: 32341564
doi: 10.1038/s41587-020-0501-8
Haft, D. H. et al. RefSeq: an update on prokaryotic genome annotation and curation. Nucleic Acids Res. 46, D851–D860 (2018).
pubmed: 29112715
doi: 10.1093/nar/gkx1068
Parks, D. H. et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat. Biotechnol. 38, 1079–1086 (2020).
Parks, D. H. et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat. Microbiol. 2, 1533–1542 (2017).
pubmed: 28894102
doi: 10.1038/s41564-017-0012-7
Wang, H.-C., Minh, B. Q., Susko, E. & Roger, A. J. Modeling site heterogeneity with posterior mean site frequency profiles accelerates accurate phylogenomic estimation. Syst. Biol. 67, 216–235 (2018).
pubmed: 28950365
doi: 10.1093/sysbio/syx068
Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).
pubmed: 25371430
doi: 10.1093/molbev/msu300
Federhen, S. The NCBI Taxonomy database. Nucleic Acids Res. 40, D136–D143 (2012).
pubmed: 22139910
doi: 10.1093/nar/gkr1178
Marin, J., Battistuzzi, F. U., Brown, A. C. & Hedges, S. B. The timetree of prokaryotes: new insights into their evolution and speciation. Mol. Biol. Evol. 34, 437–446 (2017).
pubmed: 27965376
Sieber, C. M. K. et al. Recovery of genomes from metagenomes via a dereplication, aggregation and scoring strategy. Nat. Microbiol. 3, 836–843 (2018).
pubmed: 29807988
pmcid: 6786971
doi: 10.1038/s41564-018-0171-1
Hug, L. A. et al. A new view of the tree of life. Nat. Microbiol. 1, 16048 (2016).
pubmed: 27572647
doi: 10.1038/nmicrobiol.2016.48
Dombrowski, N. et al. Undinarchaeota illuminate DPANN phylogeny and the impact of gene transfer on archaeal evolution. Nat. Commun. 11, 3939 (2020).
pubmed: 32770105
pmcid: 7414124
doi: 10.1038/s41467-020-17408-w
Galtier, N. & Lobry, J. R. Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. J. Mol. Evol. 44, 632–636 (1997).
pubmed: 9169555
doi: 10.1007/PL00006186
Segata, N., Börnigen, D., Morgan, X. C. & Huttenhower, C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat. Commun. 4, 2304 (2013).
pubmed: 23942190
doi: 10.1038/ncomms3304
Ali, R. H., Bogusz, M. & Whelan, S. Identifying clusters of high confidence homologies in multiple sequence alignments. Mol. Biol. Evol. 36, 2340–2351 (2019).
pubmed: 31209473
pmcid: 6933875
doi: 10.1093/molbev/msz142
Criscuolo, A. & Gribaldo, S. BMGE (block mapping and gathering with entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010).
pubmed: 20626897
pmcid: 3017758
doi: 10.1186/1471-2148-10-210
Raymann, K., Brochier-Armanet, C. & Gribaldo, S. The two-domain tree of life is linked to a new root for the Archaea. Proc. Natl Acad. Sci. USA 112, 6670–6675 (2015).
pubmed: 25964353
pmcid: 4450401
doi: 10.1073/pnas.1420858112
Williams, T. A. et al. Integrative modeling of gene and genome evolution roots the archaeal tree of life. Proc. Natl Acad. Sci. USA 114, E4602–E4611 (2017).
pubmed: 28533395
pmcid: 5468678
doi: 10.1073/pnas.1618463114
Whitman, W. B. et al. Proposal of the suffix –ota to denote phyla. Addendum to ‘Proposal to include the rank of phylum in the International Code of Nomenclature of Prokaryotes’. Int. J. Syst. Evol. Microbiol. 68, 967–969 (2018).
pubmed: 29458499
doi: 10.1099/ijsem.0.002593
Jungbluth, S. P., Amend, J. P. & Rappé, M. S. Metagenome sequencing and 98 microbial genomes from Juan de Fuca Ridge flank subsurface fluids. Sci. Data 4, sdata201737 (2017).
Reysenbach, A.-L. Class I. Thermoprotei class. nov. in Bergey’s Manual of Systematic Bacteriology Volume 1: The Archaea and the Deeply Branching and Phototrophic Bacteria (eds Garrity, G. et al.) 169–210 (Springer Verlag, 2001).
Stieglmeier, M. et al. Nitrososphaera viennensis gen. nov., sp. nov., an aerobic and mesophilic, ammonia-oxidizing archaeon from soil and a member of the archaeal phylum Thaumarchaeota. Int. J. Syst. Evol. Microbiol. 64, 2738–2752 (2014).
pubmed: 24907263
pmcid: 4129164
doi: 10.1099/ijs.0.063172-0
Elkins, J. G. et al. A korarchaeal genome reveals insights into the evolution of the Archaea. Proc. Natl Acad. Sci. USA 105, 8102–8107 (2008).
pubmed: 18535141
pmcid: 2430366
doi: 10.1073/pnas.0801980105
Oren, A., Garrity, G. M., Parker, C. T., Chuvochina, M. & Trujillo, M. E. Lists of names of prokaryotic Candidatus taxa. Int. J. Syst. Evol. Microbiol. https://doi.org/10.1099/ijsem.0.003789 (2020).
Imachi, H. et al. Isolation of an archaeon at the prokaryote–eukaryote interface. Nature 577, 519–525 (2020).
pubmed: 31942073
pmcid: 7015854
doi: 10.1038/s41586-019-1916-6
Fuchs, T., Huber, H., Burggraf, S. & Stetter, K. O. 16S rDNA-based phylogeny of the archaeal order Sulfolobales and reclassification of Desulfurolobus ambivalens as Acidianus ambivalens comb. nov. Syst. Appl. Microbiol. 19, 56–60 (1996).
doi: 10.1016/S0723-2020(96)80009-9
Quehenberger, J., Shen, L., Albers, S.-V., Siebers, B. & Spadiut, O. Sulfolobus—a potential key organism in future biotechnology. Front. Microbiol 8, 2474 (2017).
pubmed: 29312184
pmcid: 5733018
doi: 10.3389/fmicb.2017.02474
Minegishi, H. et al. Further refinement of the phylogeny of the Halobacteriaceae based on the full-length RNA polymerase subunit B′ (rpoB′) gene. Int. J. Syst. Evol. Microbiol. 60, 2398–2408 (2010).
pubmed: 19946058
doi: 10.1099/ijs.0.017160-0
Sorokin, D. Y. et al. Natronolimnobius sulfurireducens sp. nov. and Halalkaliarchaeum desulfuricum gen. nov., sp. nov., the first sulfur-respiring alkaliphilic Haloarchaea from hypersaline alkaline lakes. Int. J. Syst. Evol. Microbiol. 69, 2662–2673 (2019).
pubmed: 31166158
doi: 10.1099/ijsem.0.003506
Sorokin, D. Y. et al. Sulfur respiration in a group of facultatively anaerobic natronoarchaea ubiquitous in hypersaline soda lakes. Front. Microbiol. 9, 2359 (2018).
pubmed: 30333814
pmcid: 6176080
doi: 10.3389/fmicb.2018.02359
Mendler, K. et al. AnnoTree: visualization and exploration of a functionally annotated microbial tree of life. Nucleic Acids Res. https://doi.org/10.1093/nar/gkz246 (2019).
Chaumeil, P.-A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics https://doi.org/10.1093/bioinformatics/btz848 (2019).
Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).
pubmed: 25977477
pmcid: 4484387
doi: 10.1101/gr.186072.114
McDonald, D. et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of Bacteria and Archaea. ISME J. 6, 610–618 (2012).
pubmed: 22134646
doi: 10.1038/ismej.2011.139
Wheeler, T. J. & Eddy, S. R. nhmmer: DNA homology search with profile HMMs. Bioinformatics 29, 2487–2489 (2013).
pubmed: 23842809
pmcid: 3777106
doi: 10.1093/bioinformatics/btt403
Kalvari, I. et al. Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families. Nucleic Acids Res. 46, D335–D342 (2018).
pubmed: 29112718
doi: 10.1093/nar/gkx1038
Nawrocki, E. Structural RNA Homology Search and Alignment Using Covariance Models PhD thesis, Washington Univ. St Louis (2009).
Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree 2—approximately maximum-likelihood trees for large alignments. PLoS ONE 5, e9490 (2010).
pubmed: 20224823
pmcid: 2835736
doi: 10.1371/journal.pone.0009490
Kozlov, A. M., Aberer, A. J. & Stamatakis, A. ExaML version 3: a tool for phylogenomic analyses on supercomputers. Bioinformatics 31, 2577–2579 (2015).
pubmed: 25819675
pmcid: 4514929
doi: 10.1093/bioinformatics/btv184
Lartillot, N. & Philippe, H. A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process. Mol. Biol. Evol. 21, 1095–1109 (2004).
pubmed: 15014145
doi: 10.1093/molbev/msh112
Zhou, X., Shen, X.-X., Hittinger, C. T. & Rokas, A. Evaluating fast maximum likelihood-based phylogenetic programs using empirical phylogenomic data sets. Mol. Biol. Evol. 35, 486–503 (2018).
pubmed: 29177474
doi: 10.1093/molbev/msx302
Quang, L. S., Gascuel, O. & Lartillot, N. Empirical profile mixture models for phylogenetic reconstruction. Bioinformatics 24, 2317–2323 (2008).
doi: 10.1093/bioinformatics/btn445
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
pubmed: 23329690
pmcid: 3603318
doi: 10.1093/molbev/mst010
Robinson, D. F. & Foulds, L. R. Comparison of phylogenetic trees. Math. Biosci. 53, 131–147 (1981).
doi: 10.1016/0025-5564(81)90043-2
Kupczok, A., Schmidt, H. A. & von Haeseler, A. Accuracy of phylogeny reconstruction methods combining overlapping gene data sets. Algorithms Mol. Biol. 5, 37 (2010).
pubmed: 21134245
pmcid: 3022592
doi: 10.1186/1748-7188-5-37
Letunic, I. & Bork, P. Interactive tree of life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256–W259 (2019).
pubmed: 30931475
pmcid: 6602468
doi: 10.1093/nar/gkz239