Microbial species delineation using whole genome sequences

Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia; Konstantinidis, Konstantinos T.; Mavrommatis, Kostas; Kyrpides, Nikos C.; Pati, Amrita

doi:10.1093/nar/gkv657

Microbial species delineation using whole genome sequences

Journal Article · Mon Jul 06 00:00:00 EDT 2015 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkv657· OSTI ID:1625546

Varghese, Neha J. ^[1]; Mukherjee, Supratim ^[2]; Ivanova, Natalia ^[2]; Konstantinidis, Konstantinos T. ^[3]; Mavrommatis, Kostas ^[4]; Kyrpides, Nikos C. ^[2]; Pati, Amrita ^[2]

USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States). Microbial and Metagenome Superprogram; DOE/OSTI
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States). Microbial and Metagenome Superprogram
Georgia Inst. of Technology, Atlanta, GA (United States). Dept. of Civil and Environmental Engineering
Celgene Corp., San Francisco, CA (United States)

Increased sequencing of microbial genomes has revealed that prevailing prokaryotic species assignments can be inconsistent with whole genome information for a significant number of species. The long-standing need for a systematic and scalable species assignment technique can be met by the genome-wide Average Nucleotide Identity (gANI) metric, which is widely acknowledged as a robust measure of genomic relatedness. In this work, we demonstrate that the combination of gANI and the alignment fraction (AF) between two genomes accurately reflects their genomic relatedness. We introduce an efficient implementation of AF,gANI and discuss its successful application to 86.5M genome pairs between 13,151 prokaryotic genomes assigned to 3032 species. Subsequently, by comparing the genome clusters obtained from complete linkage clustering of these pairs to existing taxonomy, we observed that nearly 18% of all prokaryotic species suffer from anomalies in species definition. Our results can be used to explore central questions such as whether microorganisms form a continuum of genetic diversity or distinct species represented by distinct genetic signatures. We propose that this precise and objective AF,gANI-based species definition: the MiSI (Microbial Species Identifier) method, be used to address previous inconsistencies in species classification and as the primary guide for new taxonomic species assignment, supplemented by the traditional polyphasic approach, as required.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625546

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 14 Vol. 43; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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CMY-1/MOX-family AmpC β-lactamases MOX-1, MOX-2 and MOX-9 were mobilized independently from three Aeromonas species Ebmeyer, Stefan; Kristiansson, Erik; Larsson, D. G. Joakim Journal of Antimicrobial Chemotherapy, Vol. 74, Issue 5 https://doi.org/10.1093/jac/dkz025	journal	February 2019
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Transfer of the potato plant isolates of Pectobacterium wasabiae to Pectobacterium parmentieri sp. nov. Khayi, Slimane; Cigna, Jérémy; Chong, Teik Min International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 12 https://doi.org/10.1099/ijsem.0.001524	journal	December 2016
Phylogenomic analysis of the family Peptostreptococcaceae (Clostridium cluster XI) and proposal for reclassification of Clostridium litorale (Fendrich et al. 1991) and Eubacterium acidaminophilum (Zindel et al. 1989) as Peptoclostridium litorale gen. nov. comb. nov. and Peptoclostridium acidaminophilum comb. nov. Galperin, Michael Y.; Brover, Vyacheslav; Tolstoy, Igor International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 12 https://doi.org/10.1099/ijsem.0.001548	journal	December 2016
Lactobacillus micheneri sp. nov., Lactobacillus timberlakei sp. nov. and Lactobacillus quenuiae sp. nov., lactic acid bacteria isolated from wild bees and flowers McFrederick, Quinn S.; Vuong, Hoang Q.; Rothman, Jason A. International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 6 https://doi.org/10.1099/ijsem.0.002758	journal	June 2018
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Sphingobacterium haloxyli sp. nov., an endophytic bacterium isolated from Haloxylon ammodendron stems in Kumtag desert Liu, Lei; Hui, Nan; Liang, Li-xiong International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 10 https://doi.org/10.1099/ijsem.0.002982	journal	October 2018
Pectobacterium punjabense sp. nov., isolated from blackleg symptoms of potato plants in Pakistan Sarfraz, Sohaib; Riaz, Kashif; Oulghazi, Saïd International Journal of Systematic and Evolutionary Microbiology, Vol. 68, Issue 11 https://doi.org/10.1099/ijsem.0.003029	journal	November 2018
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Minimal standards for the description of new genera and species of rhizobia and agrobacteria de Lajudie, Philippe M.; Andrews, Mitchell; Ardley, Julie International Journal of Systematic and Evolutionary Microbiology, Vol. 69, Issue 7 https://doi.org/10.1099/ijsem.0.003426	journal	July 2019
Reclassification of Ochrobactrum lupini as a later heterotypic synonym of Ochrobactrum anthropi based on whole-genome sequence analysis Gazolla Volpiano, Camila; Hayashi Sant'Anna, Fernando; Ambrosini, Adriana International Journal of Systematic and Evolutionary Microbiology, Vol. 69, Issue 8 https://doi.org/10.1099/ijsem.0.003465	journal	August 2019
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Elioraea thermophila sp. nov., a thermophilic bacterium from hot spring of the class Alphaproteobacteria, emended description of the genus Elioraea and proposal of Elioraeaceae fam. nov. Habib, Neeli; Khan, Inam Ullah; Xiao, Min International Journal of Systematic and Evolutionary Microbiology, Vol. 70, Issue 2 https://doi.org/10.1099/ijsem.0.003915	journal	February 2020
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High-throughput ANI Analysis of 90K Prokaryotic Genomes Reveals Clear Species Boundaries Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M. https://doi.org/10.1101/225342	posted_content	October 2017
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The anaerobic digestion microbiome: a collection of 1600 metagenome-assembled genomes shows high species diversity related to methane production Campanaro, Stefano; Treu, Laura; Rodriguez-R, Luis M. https://doi.org/10.1101/680553	posted_content	June 2019
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Metabolic potential and in situ transcriptomic profiles of previously uncharacterized key microbial groups involved in coupled carbon, nitrogen and sulfur cycling in anoxic marine zones: Single-cell genomes of anoxic-marine-zone microbes Plominsky, Alvaro M.; Trefault, Nicole; Podell, Sheila Environmental Microbiology, Vol. 20, Issue 8 https://doi.org/10.1111/1462-2920.14109	journal	April 2018
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Complete Genome Sequence of Micrococcus luteus Strain SGAir0127, Isolated from Indoor Air Samples from Singapore Kutmutia, Shruti Ketan; Drautz-Moses, Daniela I.; Uchida, Akira Microbiology Resource Announcements, Vol. 8, Issue 41 https://doi.org/10.1128/mra.00646-19	journal	October 2019
Complete Genome Sequence of Curtobacterium sp. Strain SGAir0471, Isolated from Singapore Air Samples Hlaing, Phu Pwint Thin; Junqueira, Ana Carolina M.; Uchida, Akira Microbiology Resource Announcements, Vol. 8, Issue 47 https://doi.org/10.1128/mra.00960-19	journal	November 2019
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The Phylogenomic Diversity of Herbivore-Associated Fibrobacter spp. Is Correlated to Lignocellulose-Degrading Potential Neumann, Anthony P.; Suen, Garret mSphere, Vol. 3, Issue 6 https://doi.org/10.1128/msphere.00593-18	journal	December 2018
To Dereplicate or Not To Dereplicate? Evans, Jacob T.; Denef, Vincent J. mSphere, Vol. 5, Issue 3 https://doi.org/10.1128/msphere.00971-19	journal	June 2020
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Comparative genomics of cocci-shaped Sporosarcina strains with diverse spatial isolation Oliver, Andrew; Kay, Matthew; Cooper, Kerry K. BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4635-8	journal	May 2018
Comparative analysis of Faecalibacterium prausnitzii genomes shows a high level of genome plasticity and warrants separation into new species-level taxa Fitzgerald, Cormac Brian; Shkoporov, Andrey N.; Sutton, Thomas D. S. BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-5313-6	journal	December 2018
Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil Klonowska, Agnieszka; Moulin, Lionel; Ardley, Julie Kaye BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-6623-z	journal	March 2020
Genome-resolved metagenomics analysis provides insights into the ecological role of Thaumarchaeota in the Amazon River and its plume Pinto, Otávio H. B.; Silva, Thais F.; Vizzotto, Carla S. BMC Microbiology, Vol. 20, Issue 1 https://doi.org/10.1186/s12866-020-1698-x	journal	January 2020
Genome-centric metatranscriptomes and ecological roles of the active microbial populations during cellulosic biomass anaerobic digestion Jia, Yangyang; Ng, Siu-Kin; Lu, Hongyuan Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1121-0	journal	April 2018
Domestication of the novel alcohologenic acetogen Clostridium sp. AWRP: from isolation to characterization for syngas fermentation Lee, Joungmin; Lee, Jin Woo; Chae, Cheol Gi Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1570-0	journal	September 2019
Carbapenemases on the move: it’s good to be on ICEs Botelho, João; Roberts, Adam P.; León-Sampedro, Ricardo Mobile DNA, Vol. 9, Issue 1 https://doi.org/10.1186/s13100-018-0141-4	journal	December 2018
Genomes from uncultivated prokaryotes: a comparison of metagenome-assembled and single-amplified genomes Alneberg, Johannes; Karlsson, Christofer M. G.; Divne, Anna-Maria Microbiome, Vol. 6, Issue 1 https://doi.org/10.1186/s40168-018-0550-0	journal	September 2018
CAMISIM: simulating metagenomes and microbial communities Fritz, Adrian; Hofmann, Peter; Majda, Stephan Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0633-6	journal	February 2019
Complete genome sequence and whole-genome phylogeny of Kosmotoga pacifica type strain SLHLJ1T from an East Pacific hydrothermal sediment Jiang, Lijing; L’Haridon, Stéphane; Jebbar, Mohamed Standards in Genomic Sciences, Vol. 12, Issue 1 https://doi.org/10.1186/s40793-016-0214-2	journal	January 2017
Draft genome sequence of type strain HBR26T and description of Rhizobium aethiopicum sp. nov. Aserse, Aregu Amsalu; Woyke, Tanja; Kyrpides, Nikos C. Standards in Genomic Sciences, Vol. 12, Issue 1 https://doi.org/10.1186/s40793-017-0220-z	journal	January 2017
High-quality genome sequence of the radioresistant bacterium Deinococcus ficus KS 0460 Matrosova, Vera Y.; Gaidamakova, Elena K.; Makarova, Kira S. Standards in Genomic Sciences, Vol. 12, Issue 1 https://doi.org/10.1186/s40793-017-0258-y	journal	July 2017
High-quality draft genome sequence of Ensifer meliloti Mlalz-1, a microsymbiont of Medicago laciniata (L.) miller collected in Lanzarote, Canary Islands, Spain Osman, Wan Adnawani Meor; van Berkum, Peter; León-Barrios, Milagros Standards in Genomic Sciences, Vol. 12, Issue 1 https://doi.org/10.1186/s40793-017-0270-2	journal	September 2017
Insights into the draft genome sequence of bioactives-producing Bacillus thuringiensis DNG9 isolated from Algerian soil-oil slough Daas, Mohamed Seghir; Rosana, Albert Remus R.; Acedo, Jeella Z. Standards in Genomic Sciences, Vol. 13, Issue 1 https://doi.org/10.1186/s40793-018-0331-1	journal	October 2018
Enterobacter hormaechei subsp. hoffmannii subsp. nov., Enterobacter hormaechei subsp. xiangfangensis comb. nov., Enterobacter roggenkampii sp. nov., and Enterobacter muelleri is a later heterotypic synonym of Enterobacter asburiae based on computational analysis of sequenced Enterobacter genomes. Sutton, Granger G.; Brinkac, Lauren M.; Clarke, Thomas H. F1000Research, Vol. 7 https://doi.org/10.12688/f1000research.14566.1	journal	January 2018
Typing and classification of non-tuberculous mycobacteria isolates Clarke, Thomas; Brinkac, Lauren; Manoranjan, Joanna F1000Research, Vol. 9 https://doi.org/10.12688/f1000research.22620.1	journal	January 2020
Typing and classification of non-tuberculous mycobacteria isolates Clarke, Thomas; Brinkac, Lauren; Manoranjan, Joanna F1000Research, Vol. 9 https://doi.org/10.12688/f1000research.22620.2	journal	January 2020
Genomic features of bacterial adaptation to plants Sarah, Lebeis,; Bryan, Rangel Alvarez,; Freddy, Monteiro, The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/z1ym-1m42	text	January 2018
Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil Klonowska, Agnieszka; Moulin, Lionel; Ardley, Julie Research Square [preprints] https://doi.org/10.21203/rs.2.15865/v3	posted_content	March 2020
Novel heavy metal resistance gene clusters are present in the genome of Cupriavidus neocaledonicus STM 6070, a new species of Mimosa pudica microsymbiont isolated from heavy-metal-rich mining site soil Klonowska, Agnieszka; Moulin, Lionel; Ardley, Julie Kaye Research Square [preprints] https://doi.org/10.21203/rs.2.15865/v5	posted_content	March 2020
New insights from the biogas microbiome by comprehensive genome-resolved metagenomics of nearly 1600 species originating from multiple anaerobic digesters Campanaro, Stefano; Treu, Laura; Rodriguez-Rojas, Luis M. https://doi.org/10.21203/rs.2.18473/v1	preprint	February 2020
Genome Sequence of Pseudomonas koreensis CRS05-R5, an Antagonistic Bacterium Isolated from Rice Paddy Field Lin, Haiyan; Hu, Shikai; Liu, Ruifang Frontiers in Microbiology, Vol. 7 https://doi.org/10.3389/fmicb.2016.01756	journal	November 2016
Cultivation and Genomic Analysis of “Candidatus Nitrosocaldus islandicus,” an Obligately Thermophilic, Ammonia-Oxidizing Thaumarchaeon from a Hot Spring Biofilm in Graendalur Valley, Iceland Daebeler, Anne; Herbold, Craig W.; Vierheilig, Julia Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00193	journal	February 2018
Genomic Insights Into the Mycobacterium kansasii Complex: An Update Jagielski, Tomasz; Borówka, Paulina; Bakuła, Zofia Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.02918	journal	January 2020
The Distribution of Tryptophan-Dependent Indole-3-Acetic Acid Synthesis Pathways in Bacteria Unraveled by Large-Scale Genomic Analysis Zhang, Pengfan; Jin, Tao; Kumar Sahu, Sunil Molecules, Vol. 24, Issue 7 https://doi.org/10.3390/molecules24071411	journal	April 2019
Genome Mining and Comparative Pathogenomic Analysis of An Endemic Methicillin-Resistant Staphylococcus Aureus (MRSA) Clone, ST612-CC8-t1257-SCCmec_IVd(2B), Isolated in South Africa Amoako, Daniel Gyamfi; Somboro, Anou M.; Abia, Akebe Luther King Pathogens, Vol. 8, Issue 4 https://doi.org/10.3390/pathogens8040166	journal	September 2019
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

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