A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

Barco, R. A.; Garrity, G. M.; Scott, J. J.; Amend, J. P.; Nealson, K. H.; Emerson, D.; Giovannoni, ed., Stephen J.

doi:10.1128/mBio.02475-19

Title: A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

Journal Article · Tue Feb 25 00:00:00 EST 2020 · mBio

DOI:https://doi.org/10.1128/mBio.02475-19· OSTI ID:1582484

Barco, R. A. ^[1];

^[2]; Scott, J. J. ^[3]; Amend, J. P. ^[4]; Nealson, K. H. ^[4]; Emerson, D. ^[5]; Giovannoni, ed., Stephen J.

Department of Earth Sciences, University of Southern California, Los Angeles, California, USA, Department of Biological Sciences, University of Southern California, Los Angeles, California, USA, Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine, USA
Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USA
Smithsonian Tropical Research Institute, Panama, Republic of Panama
Department of Earth Sciences, University of Southern California, Los Angeles, California, USA, Department of Biological Sciences, University of Southern California, Los Angeles, California, USA
Bigelow Laboratory for Ocean Sciences, East Boothbay, Maine, USA

Genus assignment is fundamental in the characterization of microbes, yet there is currently no unambiguous way to demarcate genera solely using standard genomic relatedness indices. Here, we propose an approach to demarcate genera that relies on the combined use of the average nucleotide identity, genome alignment fraction, and the distinction between type- and non-type species. More than 3,500 genomes representing type strains of species from >850 genera of either bacterial or archaeal lineages were tested. Over 140 genera were analyzed in detail within the taxonomic context of order/family. Significant genomic differences between members of a genus and type species of other genera in the same order/family were conserved in 94% of the cases. Nearly 90% (92% if polyphyletic genera are excluded) of the type strains were classified in agreement with current taxonomy. The 448 type strains that need reclassification directly impact 33% of the genera analyzed in detail. The results provide a first line of evidence that the combination of genomic indices provides added resolution to effectively demarcate genera within the taxonomic framework that is currently based on the 16S rRNA gene. We also identify the emergence of natural breakpoints at the genome level that can further help in the circumscription of taxa, increasing the proportion of directly impacted genera to at least 43% and pointing at inaccuracies on the use of the 16S rRNA gene as a taxonomic marker, despite its precision. Altogether, these results suggest that genomic coherence is an emergent property of genera in Bacteria and Archaea.

View Journal Article

Cite

Export

Save

Research Organization:: NamesforLife, LLC, East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF); Gordon and Betty Moore Foundation; Smithsonian Tropical Research Institute; Center for Dark Energy Biosphere Investigations

Grant/Contract Number:: FG02-07ER86321; SC0006191; 1523639; GBMF5603; OCE-039564

OSTI ID:: 1582484

Alternate ID(s):: OSTI ID: 1626150

Journal Information:: mBio, Journal Name: mBio Vol. 11 Journal Issue: 1; ISSN 2161-2129

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 145 works

Citation information provided by
Web of Science

References (61)

Uncultivated microbes in need of their own taxonomy Konstantinidis, Konstantinos T.; Rosselló-Móra, Ramon; Amann, Rudolf The ISME Journal, Vol. 11, Issue 11 https://doi.org/10.1038/ismej.2017.113	journal	July 2017
Anvi’o: an advanced analysis and visualization platform for ‘omics data Eren, A. Murat; Esen, Özcan C.; Quince, Christopher PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1319	journal	January 2015
Revisiting the Evolution and Taxonomy of Clostridia, a Phylogenomic Update Cruz-Morales, Pablo; Orellana, Camila A.; Moutafis, George Genome Biology and Evolution, Vol. 11, Issue 7 https://doi.org/10.1093/gbe/evz096	journal	May 2019
Shifting the genomic gold standard for the prokaryotic species definition Richter, Michael; Rosselló-Móra, Ramon Proceedings of the National Academy of Sciences, Vol. 106, Issue 45 https://doi.org/10.1073/pnas.0906412106	journal	October 2009
Thiomicrospira thermophila sp. nov., a novel microaerobic, thermotolerant, sulfur-oxidizing chemolithomixotroph isolated from a deep-sea hydrothermal fumarole in the TOTO caldera, Mariana Arc, Western Pacific Takai, K. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 6 https://doi.org/10.1099/ijs.0.63284-0	journal	November 2004
Taxonomic Note: A Place for DNA-DNA Reassociation and 16S rRNA Sequence Analysis in the Present Species Definition in Bacteriology Stackebrandt, E.; Goebel, B. M. International Journal of Systematic and Evolutionary Microbiology, Vol. 44, Issue 4 https://doi.org/10.1099/00207713-44-4-846	journal	October 1994
The Entomopathogenic Bacterial Endosymbionts Xenorhabdus and Photorhabdus: Convergent Lifestyles from Divergent Genomes Chaston, John M.; Suen, Garret; Tucker, Sarah L. PLoS ONE, Vol. 6, Issue 11 https://doi.org/10.1371/journal.pone.0027909	journal	November 2011
Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes Kim, M.; Oh, H. -S.; Park, S. -C. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 2 https://doi.org/10.1099/ijs.0.059774-0	journal	February 2014
Using MCL to Extract Clusters from Networks van Dongen, Stijn; Abreu-Goodger, Cei Bacterial Molecular Networks https://doi.org/10.1007/978-1-61779-361-5_15	book	October 2011
Inability of the Polyphasic Approach to Systematics To Determine the Relatedness of the Genera Xenorhabdus and Photorhabdus Rainey, F. A.; Ehlers, R. -U.; Stackebrandt, E. International Journal of Systematic Bacteriology, Vol. 45, Issue 2 https://doi.org/10.1099/00207713-45-2-379	journal	April 1995
1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life Mukherjee, Supratim; Seshadri, Rekha; Varghese, Neha J. Nature Biotechnology, Vol. 35, Issue 7 https://doi.org/10.1038/nbt.3886	journal	June 2017
Priority of the genus name Clostridium Prazmowski 1880 (Approved Lists 1980) vs Sarcina Goodsir 1842 (Approved Lists 1980) and the creation of the illegitimate combinations Clostridium maximum (Lindner 1888) Lawson and Rainey 2016 and Clostridium ventriculi (Goodsir 1842) Lawson and Rainey 2016 that may not be used Tindall, B. J. International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 11 https://doi.org/10.1099/ijsem.0.001361	journal	November 2016
Anoxybacillus pushchinensis gen. nov., sp. nov., a novel anaerobic, alkaliphilic, moderately thermophilic bacterium from manure, and description of Anoxybacillus flavithermus comb. nov Pikuta, E.; Lysenko, A.; Chuvilskaya, N. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 50, Issue 6 https://doi.org/10.1099/00207713-50-6-2109	journal	November 2000
A Non-luminescent Strain of Xenorhabdus luminescens (Enterobacteriaceae) Akhurst, R. J.; Boemare, N. E. Microbiology, Vol. 132, Issue 7 https://doi.org/10.1099/00221287-132-7-1917	journal	July 1986
Towards a Genome-Based Reclassification of the Genus Lactobacillus Wittouck, Stijn; Wuyts, Sander; Lebeer, Sarah Applied and Environmental Microbiology, Vol. 85, Issue 3 https://doi.org/10.1128/AEM.02155-18	journal	January 2019
Approved Lists of Bacterial Names Sneath, P. H. A.; McGOWAN, Vicki; Skerman, V. B. D. International Journal of Systematic and Evolutionary Microbiology, Vol. 30, Issue 1 https://doi.org/10.1099/00207713-30-1-225	journal	January 1980
Genomic patterns of recombination, clonal divergence and environment in marine microbial populations Konstantinidis, Konstantinos T.; DeLong, Edward F. The ISME Journal, Vol. 2, Issue 10 https://doi.org/10.1038/ismej.2008.62	journal	June 2008
Ten Years of Maintaining and Expanding a Microbial Genome and Metagenome Analysis System Markowitz, Victor M.; Chen, I-Min A.; Chu, Ken Trends in Microbiology, Vol. 23, Issue 11 https://doi.org/10.1016/j.tim.2015.07.012	journal	November 2015
Prokaryotic species are sui generis evolutionary units Palmer, Marike; Venter, Stephanus N.; Coetzee, Martin P. A. Systematic and Applied Microbiology, Vol. 42, Issue 2 https://doi.org/10.1016/j.syapm.2018.10.002	journal	March 2019
Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar Nature Reviews Microbiology, Vol. 12, Issue 9 https://doi.org/10.1038/nrmicro3330	journal	August 2014
Genome sequence-based species delimitation with confidence intervals and improved distance functions Meier-Kolthoff, Jan P.; Auch, Alexander F.; Klenk, Hans-Peter BMC Bioinformatics, Vol. 14, Issue 1 https://doi.org/10.1186/1471-2105-14-60	journal	January 2013
Characterization and optimization of Bacillus subtilis ATCC 6051 as an expression host Kabisch, Johannes; Thürmer, Andrea; Hübel, Tanno Journal of Biotechnology, Vol. 163, Issue 2 https://doi.org/10.1016/j.jbiotec.2012.06.034	journal	January 2013
Prodigal: prokaryotic gene recognition and translation initiation site identification Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F. BMC Bioinformatics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2105-11-119	journal	March 2010
Microbial species delineation using whole genome sequences Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia Nucleic Acids Research, Vol. 43, Issue 14 https://doi.org/10.1093/nar/gkv657	journal	July 2015
A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life Parks, Donovan H.; Chuvochina, Maria; Waite, David W. Nature Biotechnology, Vol. 36, Issue 10 https://doi.org/10.1038/nbt.4229	journal	August 2018
Bypassing Cultivation To Identify Bacterial Species: Culture-independent genomic approaches identify credibly distinct clusters, avoid cultivation bias, and provide true insights into microbial species Rodriguez-R, Luis M.; Konstantinidis, Konstantinos T. Microbe Magazine, Vol. 9, Issue 3 https://doi.org/10.1128/microbe.9.111.1	journal	March 2014
Genome sequences as the type material for taxonomic descriptions of prokaryotes Whitman, William B. Systematic and Applied Microbiology, Vol. 38, Issue 4 https://doi.org/10.1016/j.syapm.2015.02.003	journal	June 2015
The Global Catalogue of Microorganisms (GCM) 10K type strain sequencing project: providing services to taxonomists for standard genome sequencing and annotation Wu, Linhuan; Ma, Juncai International Journal of Systematic and Evolutionary Microbiology, Vol. 69, Issue 4 https://doi.org/10.1099/ijsem.0.003276	journal	April 2019
A Genomic View of Lactobacilli and Pediococci Demonstrates that Phylogeny Matches Ecology and Physiology Zheng, Jinshui; Ruan, Lifang; Sun, Ming Applied and Environmental Microbiology, Vol. 81, Issue 20 https://doi.org/10.1128/AEM.02116-15	journal	August 2015
A Proposed Genus Boundary for the Prokaryotes Based on Genomic Insights Qin, Q. -L.; Xie, B. -B.; Zhang, X. -Y. Journal of Bacteriology, Vol. 196, Issue 12 https://doi.org/10.1128/JB.01688-14	journal	April 2014
Composite Metagenome-Assembled Genomes Reduce the Quality of Public Genome Repositories Shaiber, Alon; Eren, A. Murat mBio, Vol. 10, Issue 3 https://doi.org/10.1128/mBio.00725-19	journal	June 2019
Prokaryotic taxonomy and phylogeny in the genomic era: advancements and challenges ahead Konstantinidis, Konstantinos T.; Tiedje, James M. Current Opinion in Microbiology, Vol. 10, Issue 5 https://doi.org/10.1016/j.mib.2007.08.006	journal	October 2007
Intragenomic Heterogeneity and Intergenomic Recombination among Haloarchaeal rRNA Genes Boucher, Y.; Douady, C. J.; Sharma, A. K. Journal of Bacteriology, Vol. 186, Issue 12 https://doi.org/10.1128/JB.186.12.3980-3990.2004	journal	June 2004
Expanding the biotechnology potential of lactobacilli through comparative genomics of 213 strains and associated genera Sun, Zhihong; Harris, Hugh M. B.; McCann, Angela Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9322	journal	September 2015
The SILVA ribosomal RNA gene database project: improved data processing and web-based tools Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1219	journal	November 2012
SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes Pruesse, Elmar; Peplies, Jörg; Glöckner, Frank Oliver Bioinformatics, Vol. 28, Issue 14 https://doi.org/10.1093/bioinformatics/bts252	journal	May 2012
Single-amino acid variants reveal evolutionary processes that shape the biogeography of a global SAR11 subclade Delmont, Tom O.; Kiefl, Evan; Kilinc, Ozsel eLife, Vol. 8 https://doi.org/10.7554/eLife.46497	journal	September 2019
The Sorcerer II Global Ocean Sampling Expedition: Northwest Atlantic through Eastern Tropical Pacific Rusch, Douglas B.; Halpern, Aaron L.; Sutton, Granger PLoS Biology, Vol. 5, Issue 3 https://doi.org/10.1371/journal.pbio.0050077	journal	March 2007
Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. Ahmed, I.; Yokota, A.; Yamazoe, A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 57, Issue 5 https://doi.org/10.1099/ijs.0.63867-0	journal	May 2007
Linking pangenomes and metagenomes: the Prochlorococcus metapangenome Delmont, Tom O.; Eren, A. Murat PeerJ, Vol. 6 https://doi.org/10.7717/peerj.4320	journal	January 2018
Accelerated Profile HMM Searches Eddy, Sean R. PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002195	journal	October 2011
Intragenomic Heterogeneity of 16S rRNA Genes Causes Overestimation of Prokaryotic Diversity Sun, Dong-Lei; Jiang, Xuan; Wu, Qinglong L. Applied and Environmental Microbiology, Vol. 79, Issue 19 https://doi.org/10.1128/AEM.01282-13	journal	July 2013
Towards a Genome-Based Taxonomy for Prokaryotes Konstantinidis, K. T.; Tiedje, J. M. Journal of Bacteriology, Vol. 187, Issue 18 https://doi.org/10.1128/JB.187.18.6258-6264.2005	journal	September 2005
Phylogeny of Photorhabdus and Xenorhabdus Species and Strains as Determined by Comparison of Partial 16S rRNA Gene Sequences Liu, J.; Berry, R.; Poinar, G. International Journal of Systematic Bacteriology, Vol. 47, Issue 4 https://doi.org/10.1099/00207713-47-4-948	journal	October 1997
Lactobacillus equicursoris sp. nov., isolated from the faeces of a thoroughbred racehorse Morita, H.; Shimazu, M.; Shiono, H. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 60, Issue 1 https://doi.org/10.1099/ijs.0.009290-0	journal	July 2009
The Genome of Deep-Sea Vent Chemolithoautotroph Thiomicrospira crunogena XCL-2 Scott, Kathleen M.; Sievert, Stefan M.; Abril, Fereniki N. PLoS Biology, Vol. 4, Issue 12 https://doi.org/10.1371/journal.pbio.0040383	journal	November 2006
DNA Relatedness between Xenorhabdus spp. (Enterobacteriaceae), Symbiotic Bacteria of Entomopathogenic Nematodes, and a Proposal To Transfer Xenorhabdus luminescens to a New Genus, Photorhabdus gen. nov. Boemare, N. E.; Akhurst, R. J.; Mourant, R. G. International Journal of Systematic Bacteriology, Vol. 43, Issue 2 https://doi.org/10.1099/00207713-43-2-249	journal	April 1993
Identifying and Overcoming Threats to Reproducibility, Replicability, Robustness, and Generalizability in Microbiome Research Schloss, Patrick D. mBio, Vol. 9, Issue 3 https://doi.org/10.1128/mBio.00525-18	journal	June 2018
Occurrence, phylogeny and evolution of ribulose-1,5-bisphosphate carboxylase/oxygenase genes in obligately chemolithoautotrophic sulfur-oxidizing bacteria of the genera Thiomicrospira and Thioalkalimicrobium Tourova, T. P. Microbiology, Vol. 152, Issue 7 https://doi.org/10.1099/mic.0.28699-0	journal	July 2006
High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M. Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-07641-9	journal	November 2018
Notes on the characterization of prokaryote strains for taxonomic purposes Busse, H. -J.; Tindall, B. J.; Ludwig, W. International Journal of Systematic and Evolutionary Microbiology, Vol. 60, Issue 1 https://doi.org/10.1099/ijs.0.016949-0	journal	January 2010
Thiomicrospira halophila sp. nov., a moderately halophilic, obligately chemolithoautotrophic, sulfur-oxidizing bacterium from hypersaline lakes Sorokin, D. Yu. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 10 https://doi.org/10.1099/ijs.0.64445-0	journal	October 2006
Xenorhabdus gen. nov., a Genus of Entomopathogenic, Nematophilic Bacteria of the Family Enterobacteriaceae Thomas, G. M.; Poinar, G. O. International Journal of Systematic Bacteriology, Vol. 29, Issue 4 https://doi.org/10.1099/00207713-29-4-352	journal	October 1979
Genomes of ubiquitous marine and hypersaline Hydrogenovibrio , Thiomicrorhabdus and Thiomicrospira spp. encode a diversity of mechanisms to sustain chemolithoautotrophy in heterogeneous environments : Hydrogenovibrio, Thiomicrorhabdus, Thiomicrospira Scott, Kathleen M.; Williams, John; Porter, Cody M. B. Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14090	journal	April 2018
Genomic insights that advance the species definition for prokaryotes Konstantinidis, K. T.; Tiedje, J. M. Proceedings of the National Academy of Sciences, Vol. 102, Issue 7 https://doi.org/10.1073/pnas.0409727102	journal	February 2005
Draft Genome Sequences of 24 Lactococcus lactis Strains Backus, Lennart; Wels, Michiel; Boekhorst, Jos Genome Announcements, Vol. 5, Issue 13 https://doi.org/10.1128/genomeA.01737-16	journal	March 2017
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood Guindon, Stéphane; Gascuel, Olivier Systematic Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10635150390235520	journal	October 2003
DNA–DNA hybridization values and their relationship to whole-genome sequence similarities Klappenbach, Joel A.; Goris, Johan; Vandamme, Peter International Journal of Systematic and Evolutionary Microbiology, Vol. 57, Issue 1 https://doi.org/10.1099/ijs.0.64483-0	journal	January 2007
A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea Wu, Dongying; Hugenholtz, Philip; Mavromatis, Konstantinos Nature, Vol. 462, Issue 7276 https://doi.org/10.1038/nature08656	journal	December 2009
Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies Yoon, Seok-Hwan; Ha, Sung-Min; Kwon, Soonjae International Journal of Systematic and Evolutionary Microbiology, Vol. 67, Issue 5, p. 1613-1617 https://doi.org/10.1099/ijsem.0.001755	journal	May 2017
Bacterial species may exist, metagenomics reveal: Bacterial species may exist Caro-Quintero, Alejandro; Konstantinidis, Konstantinos T. Environmental Microbiology, Vol. 14, Issue 2 https://doi.org/10.1111/j.1462-2920.2011.02668.x	journal	December 2011

Similar Records

Genome sequence of the thermophilic fresh-water bacterium Spirochaeta caldaria type strain (H1^T), reclassification of Spirochaeta caldaria, Spirochaeta stenostrepta, and Spirochaeta zuelzerae in the genus Treponema as Treponema caldaria comb. nov., Treponema stenostrepta comb. nov., and Treponema zuelzerae comb. nov., and emendation of the genus Treponema

Journal Article · Mon Apr 15 00:00:00 EDT 2013 · Standards in Genomic Sciences · OSTI ID:1582484

Abt, Birte; Göker, Markus; Scheuner, Carmen; +35 more

Zwartia hollandica gen. nov., sp. nov., Jezberella montanilacus gen. nov., sp. nov. and Sheuella amnicola gen. nov., comb. nov., representing the environmental GKS98 (betIII) cluster

Journal Article · Wed Sep 07 00:00:00 EDT 2022 · International Journal of Systematic and Evolutionary Microbiology · OSTI ID:1582484

Hahn, Martin W.; Pitt, Alexandra; Schmidt, Johanna; +5 more

Genome sequence of the mud-dwelling archaeon Methanoplanus limicola type strain (DSM 2279^T), reclassification of Methanoplanus petrolearius as Methanolacinia petrolearia and emended descriptions of the genera Methanoplanus and Methanolacinia

Journal Article · Sun Jun 15 00:00:00 EDT 2014 · Standards in Genomic Sciences · OSTI ID:1582484

Goker, Markus; Lu, Megan; Fiebig, Anne; +31 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
microbiology
ANI
Bacillus
Clostridium
Lactobacillus
Photorhabdus
Pseudomonas
Xenorhabdus
delineation
demarcation
genus
systematics
taxonomy

Title: A Genus Definition for Bacteria and Archaea Based on a Standard Genome Relatedness Index

Citation Formats

References (61)

Similar Records

Related Subjects