k-mer Similarity, Networks of Microbial Genomes, and Taxonomic Rank
Identifieur interne : 001255 ( Pmc/Curation ); précédent : 001254; suivant : 001256k-mer Similarity, Networks of Microbial Genomes, and Taxonomic Rank
Auteurs : Guillaume Bernard [Australie] ; Paul Greenfield [Australie] ; Mark A. Ragan [Australie] ; Cheong Xin Chan [Australie]Source :
- mSystems [ 2379-5077 ] ; 2018.
Abstract
Genome evolution of microbes involves parent-to-offspring descent, and lateral genetic transfer that convolutes the phylogenomic signal. This study investigated phylogenomic signals among thousands of microbial genomes based on short subsequences without using multiple-sequence alignment. The signal from ribosomal RNAs is strong across all taxa, and the signal of plasmids is strong only in closely related groups, particularly
Url:
DOI: 10.1128/mSystems.00257-18
PubMed: 30505941
PubMed Central: 6247013
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en"><italic>k</italic>-mer Similarity, Networks of Microbial Genomes, and Taxonomic Rank</title><author><name sortKey="Bernard, Guillaume" sort="Bernard, Guillaume" uniqKey="Bernard G" first="Guillaume" last="Bernard">Guillaume Bernard</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation></author><author><name sortKey="Greenfield, Paul" sort="Greenfield, Paul" uniqKey="Greenfield P" first="Paul" last="Greenfield">Paul Greenfield</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Commonwealth Scientific and Industrial Research Organisation (CSIRO), North Ryde, NSW, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Commonwealth Scientific and Industrial Research Organisation (CSIRO), North Ryde, NSW</wicri:regionArea></affiliation></author><author><name sortKey="Ragan, Mark A" sort="Ragan, Mark A" uniqKey="Ragan M" first="Mark A." last="Ragan">Mark A. Ragan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation></author><author><name sortKey="Chan, Cheong Xin" sort="Chan, Cheong Xin" uniqKey="Chan C" first="Cheong Xin" last="Chan">Cheong Xin Chan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">30505941</idno><idno type="pmc">6247013</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6247013</idno><idno type="RBID">PMC:6247013</idno><idno type="doi">10.1128/mSystems.00257-18</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">001255</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001255</idno><idno type="wicri:Area/Pmc/Curation">001255</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">001255</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main"><italic>k</italic>-mer Similarity, Networks of Microbial Genomes, and Taxonomic Rank</title><author><name sortKey="Bernard, Guillaume" sort="Bernard, Guillaume" uniqKey="Bernard G" first="Guillaume" last="Bernard">Guillaume Bernard</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation></author><author><name sortKey="Greenfield, Paul" sort="Greenfield, Paul" uniqKey="Greenfield P" first="Paul" last="Greenfield">Paul Greenfield</name><affiliation wicri:level="1"><nlm:aff id="aff2"><addr-line>Commonwealth Scientific and Industrial Research Organisation (CSIRO), North Ryde, NSW, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Commonwealth Scientific and Industrial Research Organisation (CSIRO), North Ryde, NSW</wicri:regionArea></affiliation></author><author><name sortKey="Ragan, Mark A" sort="Ragan, Mark A" uniqKey="Ragan M" first="Mark A." last="Ragan">Mark A. Ragan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation></author><author><name sortKey="Chan, Cheong Xin" sort="Chan, Cheong Xin" uniqKey="Chan C" first="Cheong Xin" last="Chan">Cheong Xin Chan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><addr-line>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia</addr-line></nlm:aff><country xml:lang="fr">Australie</country><wicri:regionArea>School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation></author></analytic><series><title level="j">mSystems</title><idno type="eISSN">2379-5077</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Genome evolution of microbes involves parent-to-offspring descent, and lateral genetic transfer that convolutes the phylogenomic signal. This study investigated phylogenomic signals among thousands of microbial genomes based on short subsequences without using multiple-sequence alignment. The signal from ribosomal RNAs is strong across all taxa, and the signal of plasmids is strong only in closely related groups, particularly <italic>Proteobacteria</italic>. However, the signal from other chromosomal regions (∼99% of the genomes) is remarkably restricted in breadth. The similarity of subsequences is found to correlate with taxonomic rank and informs on conserved and differential core functions relative to niche specialization and evolutionary diversification of microbes. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">mSystems</journal-id><journal-id journal-id-type="iso-abbrev">mSystems</journal-id><journal-id journal-id-type="hwp">msys</journal-id><journal-id journal-id-type="pmc">msys</journal-id><journal-id journal-id-type="publisher-id">mSystems</journal-id><journal-title-group><journal-title>mSystems</journal-title></journal-title-group><issn pub-type="epub">2379-5077</issn><publisher><publisher-name>American Society for Microbiology</publisher-name><publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30505941</article-id><article-id pub-id-type="pmc">6247013</article-id><article-id pub-id-type="publisher-id">mSystems00257-18</article-id><article-id pub-id-type="doi">10.1128/mSystems.00257-18</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="overline"><subject>Ecological and Evolutionary Science</subject></subj-group></article-categories><title-group><article-title><italic>k</italic>-mer Similarity, Networks of Microbial Genomes, and Taxonomic Rank</article-title><alt-title alt-title-type="running-head"><italic>k-</italic>mer Phylogenomics of Microbes</alt-title><alt-title alt-title-type="short-authors">Bernard et al.</alt-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-6251-9500</contrib-id><name><surname>Bernard</surname><given-names>Guillaume</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1">*</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-4028-9243</contrib-id><name><surname>Greenfield</surname><given-names>Paul</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-1672-7020</contrib-id><name><surname>Ragan</surname><given-names>Mark A.</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0002-3729-8176</contrib-id><name><surname>Chan</surname><given-names>Cheong Xin</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><aff id="aff1"><label>a</label><addr-line>Institute for Molecular Bioscience, The University of Queensland, Brisbane, QLD, Australia</addr-line></aff><aff id="aff2"><label>b</label><addr-line>Commonwealth Scientific and Industrial Research Organisation (CSIRO), North Ryde, NSW, Australia</addr-line></aff><aff id="aff3"><label>c</label><addr-line>School of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD, Australia</addr-line></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Claesson</surname><given-names>Marcus J.</given-names></name><role>Editor</role><aff>University College Cork</aff></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Cheong Xin Chan, <email>c.chan1@uq.edu.au</email>.</corresp><fn id="fn1" fn-type="present-address"><label>*</label><p>Present address: Guillaume Bernard, Sorbonne Universités, UPMC Université Paris 06, Institut de Biologie Paris-Seine (IBPS), Paris, France.</p></fn><fn fn-type="other"><p><bold>Citation</bold> Bernard G, Greenfield P, Ragan MA, Chan CX. 2018. <italic>k</italic>-mer similarity, networks of microbial genomes, and taxonomic rank. mSystems 3:e00257-18. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/mSystems.00257-18">https://doi.org/10.1128/mSystems.00257-18</ext-link>.</p></fn></author-notes><pub-date pub-type="epub"><day>20</day><month>11</month><year>2018</year></pub-date><pub-date pub-type="collection"><season>Nov-Dec</season><year>2018</year></pub-date><volume>3</volume><issue>6</issue><elocation-id>e00257-18</elocation-id><history><date date-type="received"><day>12</day><month>10</month><year>2018</year></date><date date-type="accepted"><day>2</day><month>11</month><year>2018</year></date></history><permissions><copyright-statement>Copyright © 2018 Bernard et al.</copyright-statement><copyright-year>2018</copyright-year><copyright-holder>Bernard et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="sys006182296001.pdf"></self-uri><abstract abstract-type="precis"><p>Genome evolution of microbes involves parent-to-offspring descent, and lateral genetic transfer that convolutes the phylogenomic signal. This study investigated phylogenomic signals among thousands of microbial genomes based on short subsequences without using multiple-sequence alignment. The signal from ribosomal RNAs is strong across all taxa, and the signal of plasmids is strong only in closely related groups, particularly <italic>Proteobacteria</italic>. However, the signal from other chromosomal regions (∼99% of the genomes) is remarkably restricted in breadth. The similarity of subsequences is found to correlate with taxonomic rank and informs on conserved and differential core functions relative to niche specialization and evolutionary diversification of microbes. These results provide a comprehensive, alignment-free view of microbial genome evolution as a network, beyond a tree-like structure.</p></abstract><abstract><title>ABSTRACT</title><p>Microbial genomes have been shaped by parent-to-offspring (vertical) descent and lateral genetic transfer. These processes can be distinguished by alignment-based inference and comparison of phylogenetic trees for individual gene families, but this approach is not scalable to whole-genome sequences, and a tree-like structure does not adequately capture how these processes impact microbial physiology. Here we adopted alignment-free approaches based on <italic>k</italic>-mer statistics to infer phylogenomic networks involving 2,783 completely sequenced bacterial and archaeal genomes and compared the contributions of rRNA, protein-coding, and plasmid sequences to these networks. Our results show that the phylogenomic signal arising from ribosomal RNAs is strong and extends broadly across all taxa, whereas that from plasmids is strong but restricted to closely related groups, particularly <italic>Proteobacteria</italic>. However, the signal from the other chromosomal regions is restricted in breadth. We show that mean <italic>k</italic>-mer similarity can correlate with taxonomic rank. We also link the implicated <italic>k</italic>-mers to genome annotation (thus, functions) and define core <italic>k</italic>-mers (thus, core functions) in specific phyletic groups. Highly conserved functions in most phyla include amino acid metabolism and transport as well as energy production and conversion. Intracellular trafficking and secretion are the most prominent core functions among <italic>Spirochaetes</italic>, whereas energy production and conversion are not highly conserved among the largely parasitic or commensal <italic>Tenericutes</italic>. These observations suggest that differential conservation of functions relates to niche specialization and evolutionary diversification of microbes. Our results demonstrate that <italic>k</italic>-mer approaches can be used to efficiently identify phylogenomic signals and conserved core functions at the multigenome scale.</p><p><bold>IMPORTANCE</bold> Genome evolution of microbes involves parent-to-offspring descent, and lateral genetic transfer that convolutes the phylogenomic signal. This study investigated phylogenomic signals among thousands of microbial genomes based on short subsequences without using multiple-sequence alignment. The signal from ribosomal RNAs is strong across all taxa, and the signal of plasmids is strong only in closely related groups, particularly <italic>Proteobacteria</italic>. However, the signal from other chromosomal regions (∼99% of the genomes) is remarkably restricted in breadth. The similarity of subsequences is found to correlate with taxonomic rank and informs on conserved and differential core functions relative to niche specialization and evolutionary diversification of microbes. These results provide a comprehensive, alignment-free view of microbial genome evolution as a network, beyond a tree-like structure.</p></abstract><kwd-group><title>KEYWORDS</title><kwd>core functions</kwd><kwd><italic>k</italic>-mers</kwd><kwd>networks</kwd><kwd>phylogenetic analysis</kwd><kwd>phylogenomics</kwd></kwd-group><funding-group><award-group id="award1"><funding-source><institution-wrap><institution>James S. McDonnell Foundation (JSMF)</institution><institution-id>https://doi.org/10.13039/100000913</institution-id></institution-wrap></funding-source><principal-award-recipient><name><surname>Ragan</surname><given-names>Mark A.</given-names></name></principal-award-recipient></award-group><award-group id="award2"><funding-source><institution-wrap><institution>Department of Education and Training | Australian Research Council (ARC)</institution><institution-id>https://doi.org/10.13039/501100000923</institution-id></institution-wrap></funding-source><award-id>DP150101875</award-id><principal-award-recipient><name><surname>Chan</surname><given-names>Cheong Xin</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Ragan</surname><given-names>Mark A.</given-names></name></principal-award-recipient></award-group></funding-group><counts><count count="10" count-type="supplementary-material"></count><fig-count count="7"></fig-count><table-count count="3"></table-count><equation-count count="21"></equation-count><ref-count count="57"></ref-count><page-count count="16"></page-count><word-count count="9632"></word-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>November/December 2018</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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