A Bayesian Method for Analyzing Lateral Gene Transfer
Lateral gene transfer (LGT)—which transfers DNA between two non-vertically related individuals belonging to the same or different species—is recognized as a major force in prokaryotic evolution, and evidence of its impact on eukaryotic evolution is ever increasing. LGT has attracted much public atte...
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Veröffentlicht in: | Systematic biology 2014-05, Vol.63 (3), p.409-420 |
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description | Lateral gene transfer (LGT)—which transfers DNA between two non-vertically related individuals belonging to the same or different species—is recognized as a major force in prokaryotic evolution, and evidence of its impact on eukaryotic evolution is ever increasing. LGT has attracted much public attention for its potential to transfer pathogenic elements and antibiotic resistance in bacteria, and to transfer pesticide resistance from genetically modified crops to other plants. In a wider perspective, there is a growing body of studies highlighting the role of LGT in enabling organisms to occupy new niches or adapt to environmental changes. The challenge LGT poses to the standard tree-based conception of evolution is also being debated. Studies of LGT have, however, been severely limited by a lack of computational tools. The best currently available LGT algorithms are parsimony-based phylogenetic methods, which require a pre-computed gene tree and cannot choose between sometimes wildly differing most parsimonious solutions. Moreover, in many studies, simple heuristics are applied that can only handle putative orthologs and completely disregard gene duplications (GDs). Consequently, proposed LGT among specific gene families, and the rate of LGT in general, remain debated. We present a Bayesian Markov-chain Monte Carlo-based method that integrates GD, gene loss, LGT, and sequence evolution, and apply the method in a genome-wide analysis of two groups of bacteria: Mollicutes and Cyanobacteria. Our analyses show that although the LGT rate between distant species is high, the net combined rate of duplication and close-species LGT is on average higher. We also show that the common practice of disregarding reconcilability in gene tree inference overestimates the number of LGT and duplication events. |
doi_str_mv | 10.1093/sysbio/syu007 |
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LGT has attracted much public attention for its potential to transfer pathogenic elements and antibiotic resistance in bacteria, and to transfer pesticide resistance from genetically modified crops to other plants. In a wider perspective, there is a growing body of studies highlighting the role of LGT in enabling organisms to occupy new niches or adapt to environmental changes. The challenge LGT poses to the standard tree-based conception of evolution is also being debated. Studies of LGT have, however, been severely limited by a lack of computational tools. The best currently available LGT algorithms are parsimony-based phylogenetic methods, which require a pre-computed gene tree and cannot choose between sometimes wildly differing most parsimonious solutions. Moreover, in many studies, simple heuristics are applied that can only handle putative orthologs and completely disregard gene duplications (GDs). Consequently, proposed LGT among specific gene families, and the rate of LGT in general, remain debated. We present a Bayesian Markov-chain Monte Carlo-based method that integrates GD, gene loss, LGT, and sequence evolution, and apply the method in a genome-wide analysis of two groups of bacteria: Mollicutes and Cyanobacteria. Our analyses show that although the LGT rate between distant species is high, the net combined rate of duplication and close-species LGT is on average higher. We also show that the common practice of disregarding reconcilability in gene tree inference overestimates the number of LGT and duplication events.</description><identifier>ISSN: 1063-5157</identifier><identifier>ISSN: 1076-836X</identifier><identifier>EISSN: 1076-836X</identifier><identifier>DOI: 10.1093/sysbio/syu007</identifier><identifier>PMID: 24562812</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Bayes Theorem ; Bayesian ; Bayesian analysis ; Biodiversity ; Bioinformatics ; Biological taxonomies ; Classification - methods ; Computer Science ; Cyanobacteria ; Cyanobacteria - classification ; Cyanobacteria - genetics ; datalogi ; Environmental Sciences ; Evolution ; Evolution, Molecular ; gene duplication ; gene loss ; Gene Transfer, Horizontal ; Genes ; Genetics ; Horizontal gene transfer ; lateral gene transfer ; Life Sciences ; Markov analysis ; MCMC ; Medicin och hälsovetenskap ; Models, Theoretical ; Mollicutes ; Monte Carlo simulation ; Parsimony ; Phylogenetics ; Phylogeny ; Reconciliation ; Systematic biology ; Systematics, Phylogenetics and taxonomy ; Tenericutes - classification ; Tenericutes - genetics ; Vertices</subject><ispartof>Systematic biology, 2014-05, Vol.63 (3), p.409-420</ispartof><rights>Copyright © 2014 Society of Systematic Biologists</rights><rights>The Author(s) 2014. Published by Oxford University Press, on behalf of the Society of Systematic Biologists. All rights reserved. For Permissions, please email: journals.permissions@oup.com 2014</rights><rights>Copyright Oxford University Press, UK May 2014</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c612t-6635f9692c04b3565b3b340e8cac98363b15bbdec770b605f171de90e10951883</citedby><cites>FETCH-LOGICAL-c612t-6635f9692c04b3565b3b340e8cac98363b15bbdec770b605f171de90e10951883</cites><orcidid>0000-0001-8269-9430</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/43699761$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/43699761$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,1584,27924,27925,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24562812$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01913945$$DView record in HAL$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:kth:diva-145578$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-104137$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:128771501$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Sjöstrand, Joel</creatorcontrib><creatorcontrib>Tofigh, Ali</creatorcontrib><creatorcontrib>Daubin, Vincent</creatorcontrib><creatorcontrib>Arvestad, Lars</creatorcontrib><creatorcontrib>Sennblad, Bengt</creatorcontrib><creatorcontrib>Lagergren, Jens</creatorcontrib><title>A Bayesian Method for Analyzing Lateral Gene Transfer</title><title>Systematic biology</title><addtitle>Syst Biol</addtitle><description>Lateral gene transfer (LGT)—which transfers DNA between two non-vertically related individuals belonging to the same or different species—is recognized as a major force in prokaryotic evolution, and evidence of its impact on eukaryotic evolution is ever increasing. LGT has attracted much public attention for its potential to transfer pathogenic elements and antibiotic resistance in bacteria, and to transfer pesticide resistance from genetically modified crops to other plants. In a wider perspective, there is a growing body of studies highlighting the role of LGT in enabling organisms to occupy new niches or adapt to environmental changes. The challenge LGT poses to the standard tree-based conception of evolution is also being debated. Studies of LGT have, however, been severely limited by a lack of computational tools. The best currently available LGT algorithms are parsimony-based phylogenetic methods, which require a pre-computed gene tree and cannot choose between sometimes wildly differing most parsimonious solutions. Moreover, in many studies, simple heuristics are applied that can only handle putative orthologs and completely disregard gene duplications (GDs). Consequently, proposed LGT among specific gene families, and the rate of LGT in general, remain debated. We present a Bayesian Markov-chain Monte Carlo-based method that integrates GD, gene loss, LGT, and sequence evolution, and apply the method in a genome-wide analysis of two groups of bacteria: Mollicutes and Cyanobacteria. Our analyses show that although the LGT rate between distant species is high, the net combined rate of duplication and close-species LGT is on average higher. We also show that the common practice of disregarding reconcilability in gene tree inference overestimates the number of LGT and duplication events.</description><subject>Bayes Theorem</subject><subject>Bayesian</subject><subject>Bayesian analysis</subject><subject>Biodiversity</subject><subject>Bioinformatics</subject><subject>Biological taxonomies</subject><subject>Classification - methods</subject><subject>Computer Science</subject><subject>Cyanobacteria</subject><subject>Cyanobacteria - classification</subject><subject>Cyanobacteria - genetics</subject><subject>datalogi</subject><subject>Environmental Sciences</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>gene duplication</subject><subject>gene loss</subject><subject>Gene Transfer, Horizontal</subject><subject>Genes</subject><subject>Genetics</subject><subject>Horizontal gene transfer</subject><subject>lateral gene transfer</subject><subject>Life Sciences</subject><subject>Markov analysis</subject><subject>MCMC</subject><subject>Medicin och hälsovetenskap</subject><subject>Models, Theoretical</subject><subject>Mollicutes</subject><subject>Monte Carlo simulation</subject><subject>Parsimony</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Reconciliation</subject><subject>Systematic biology</subject><subject>Systematics, Phylogenetics and taxonomy</subject><subject>Tenericutes - classification</subject><subject>Tenericutes - genetics</subject><subject>Vertices</subject><issn>1063-5157</issn><issn>1076-836X</issn><issn>1076-836X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkk1v1DAQhiMEoh9w5AiKxKVIBDx2xo6PoUCLtIhLQdwsO3G62WbjxU5Ay6_HIdtdgVQ4zWj0zOix_CbJEyCvgEj2OmyDaV0sIyHiXnIMRPCsYPzr_annLENAcZSchLAiBIAjPEyOaI6cFkCPEyzTN3prQ6v79KMdlq5OG-fTstfd9mfbX6cLPVivu_TC9ja98roPjfWPkgeN7oJ9vKunyef3767OL7PFp4sP5-UiqzjQIeOcYSO5pBXJDUOOhhmWE1tUupLRkRlAY2pbCUEMJ9iAgNpKYuPLEIqCnSbZfDf8sJvRqI1v19pvldOt2o1uYmcVUpbDxMs7-Y139WHpdhFoIQQggbj78s7dt-2XUjl_rcKogOTAxD_V9vjNsFSQI4pJ7cXML3X3B3xZLtQ0IyCByRy_TypnMxudv402DGrdhsp2ne6tG4MCBC4oo1xG9Plf6MqNPv7eb0oSLpHiQbbyLgRvm70BEDXFSM0xUnOMIv9sd3U0a1vv6dvcHAzduPnvraczugqD83s4Z1xKwYH9AnSI2o8</recordid><startdate>20140501</startdate><enddate>20140501</enddate><creator>Sjöstrand, Joel</creator><creator>Tofigh, Ali</creator><creator>Daubin, Vincent</creator><creator>Arvestad, Lars</creator><creator>Sennblad, Bengt</creator><creator>Lagergren, Jens</creator><general>Oxford University Press</general><general>Oxford University Press (OUP)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>K9.</scope><scope>7X8</scope><scope>1XC</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8V</scope><scope>DG7</scope><orcidid>https://orcid.org/0000-0001-8269-9430</orcidid></search><sort><creationdate>20140501</creationdate><title>A Bayesian Method for Analyzing Lateral Gene Transfer</title><author>Sjöstrand, Joel ; Tofigh, Ali ; Daubin, Vincent ; Arvestad, Lars ; Sennblad, Bengt ; Lagergren, Jens</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c612t-6635f9692c04b3565b3b340e8cac98363b15bbdec770b605f171de90e10951883</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Bayes Theorem</topic><topic>Bayesian</topic><topic>Bayesian analysis</topic><topic>Biodiversity</topic><topic>Bioinformatics</topic><topic>Biological taxonomies</topic><topic>Classification - methods</topic><topic>Computer Science</topic><topic>Cyanobacteria</topic><topic>Cyanobacteria - classification</topic><topic>Cyanobacteria - genetics</topic><topic>datalogi</topic><topic>Environmental Sciences</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>gene duplication</topic><topic>gene loss</topic><topic>Gene Transfer, Horizontal</topic><topic>Genes</topic><topic>Genetics</topic><topic>Horizontal gene transfer</topic><topic>lateral gene transfer</topic><topic>Life Sciences</topic><topic>Markov analysis</topic><topic>MCMC</topic><topic>Medicin och hälsovetenskap</topic><topic>Models, Theoretical</topic><topic>Mollicutes</topic><topic>Monte Carlo simulation</topic><topic>Parsimony</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Reconciliation</topic><topic>Systematic biology</topic><topic>Systematics, Phylogenetics and taxonomy</topic><topic>Tenericutes - classification</topic><topic>Tenericutes - genetics</topic><topic>Vertices</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sjöstrand, Joel</creatorcontrib><creatorcontrib>Tofigh, Ali</creatorcontrib><creatorcontrib>Daubin, Vincent</creatorcontrib><creatorcontrib>Arvestad, Lars</creatorcontrib><creatorcontrib>Sennblad, Bengt</creatorcontrib><creatorcontrib>Lagergren, Jens</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Kungliga Tekniska Högskolan</collection><collection>SWEPUB Stockholms universitet</collection><jtitle>Systematic biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sjöstrand, Joel</au><au>Tofigh, Ali</au><au>Daubin, Vincent</au><au>Arvestad, Lars</au><au>Sennblad, Bengt</au><au>Lagergren, Jens</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A Bayesian Method for Analyzing Lateral Gene Transfer</atitle><jtitle>Systematic biology</jtitle><addtitle>Syst Biol</addtitle><date>2014-05-01</date><risdate>2014</risdate><volume>63</volume><issue>3</issue><spage>409</spage><epage>420</epage><pages>409-420</pages><issn>1063-5157</issn><issn>1076-836X</issn><eissn>1076-836X</eissn><abstract>Lateral gene transfer (LGT)—which transfers DNA between two non-vertically related individuals belonging to the same or different species—is recognized as a major force in prokaryotic evolution, and evidence of its impact on eukaryotic evolution is ever increasing. LGT has attracted much public attention for its potential to transfer pathogenic elements and antibiotic resistance in bacteria, and to transfer pesticide resistance from genetically modified crops to other plants. In a wider perspective, there is a growing body of studies highlighting the role of LGT in enabling organisms to occupy new niches or adapt to environmental changes. The challenge LGT poses to the standard tree-based conception of evolution is also being debated. Studies of LGT have, however, been severely limited by a lack of computational tools. The best currently available LGT algorithms are parsimony-based phylogenetic methods, which require a pre-computed gene tree and cannot choose between sometimes wildly differing most parsimonious solutions. Moreover, in many studies, simple heuristics are applied that can only handle putative orthologs and completely disregard gene duplications (GDs). Consequently, proposed LGT among specific gene families, and the rate of LGT in general, remain debated. We present a Bayesian Markov-chain Monte Carlo-based method that integrates GD, gene loss, LGT, and sequence evolution, and apply the method in a genome-wide analysis of two groups of bacteria: Mollicutes and Cyanobacteria. Our analyses show that although the LGT rate between distant species is high, the net combined rate of duplication and close-species LGT is on average higher. We also show that the common practice of disregarding reconcilability in gene tree inference overestimates the number of LGT and duplication events.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>24562812</pmid><doi>10.1093/sysbio/syu007</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-8269-9430</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Bayes Theorem Bayesian Bayesian analysis Biodiversity Bioinformatics Biological taxonomies Classification - methods Computer Science Cyanobacteria Cyanobacteria - classification Cyanobacteria - genetics datalogi Environmental Sciences Evolution Evolution, Molecular gene duplication gene loss Gene Transfer, Horizontal Genes Genetics Horizontal gene transfer lateral gene transfer Life Sciences Markov analysis MCMC Medicin och hälsovetenskap Models, Theoretical Mollicutes Monte Carlo simulation Parsimony Phylogenetics Phylogeny Reconciliation Systematic biology Systematics, Phylogenetics and taxonomy Tenericutes - classification Tenericutes - genetics Vertices |
title | A Bayesian Method for Analyzing Lateral Gene Transfer |
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