Chance and necessity in the genome evolution of endosymbiotic bacteria of insects

An open question in evolutionary biology is how does the selection–drift balance determine the fates of biological interactions. We searched for signatures of selection and drift in genomes of five endosymbiotic bacterial groups known to evolve under strong genetic drift. Although most genes in endo...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:The ISME Journal 2017-06, Vol.11 (6), p.1291-1304
Hauptverfasser: Sabater-Muñoz, Beatriz, Toft, Christina, Alvarez-Ponce, David, Fares, Mario A
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 1304
container_issue 6
container_start_page 1291
container_title The ISME Journal
container_volume 11
creator Sabater-Muñoz, Beatriz
Toft, Christina
Alvarez-Ponce, David
Fares, Mario A
description An open question in evolutionary biology is how does the selection–drift balance determine the fates of biological interactions. We searched for signatures of selection and drift in genomes of five endosymbiotic bacterial groups known to evolve under strong genetic drift. Although most genes in endosymbiotic bacteria showed evidence of relaxed purifying selection, many genes in these bacteria exhibited stronger selective constraints than their orthologs in free-living bacterial relatives. Remarkably, most of these highly constrained genes had no role in the host–symbiont interactions but were involved in either buffering the deleterious consequences of drift or other host-unrelated functions, suggesting that they have either acquired new roles or their role became more central in endosymbiotic bacteria. Experimental evolution of Escherichia coli under strong genetic drift revealed remarkable similarities in the mutational spectrum, genome reduction patterns and gene losses to endosymbiotic bacteria of insects. Interestingly, the transcriptome of the experimentally evolved lines showed a generalized deregulation of the genome that affected genes encoding proteins involved in mutational buffering, regulation and amino acid biosynthesis, patterns identical to those found in endosymbiotic bacteria. Our results indicate that drift has shaped endosymbiotic associations through a change in the functional landscape of bacterial genes and that the host had only a small role in such a shift.
doi_str_mv 10.1038/ismej.2017.18
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5437351</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1917965582</sourcerecordid><originalsourceid>FETCH-LOGICAL-c454t-65f05e5d62f92734fb387c76ea1d0e55f219ae89a2979b9acbf22a2ce8089d2c3</originalsourceid><addsrcrecordid>eNptkUtrGzEURkVpaV5dZhsE3XQzrh7WSNoUimmbQKAUmrXQaO7YMjNSKmkC_veR69QkJStd-A7n6vIhdEnJghKuPvs8wXbBCJULqt6gUyoFbSSX5O1xbtkJOst5S4iQbSvfoxOmOONM0VP0a7WxwQG2occBHOTsyw77gMsG8BpCnADDQxzn4mPAccAQ-ph3U-dj8Q531hVI3u4THzK4ki_Qu8GOGT48vefo7vu336vr5vbnj5vV19vGLcWyNK0YiADRt2zQTPLl0HElnWzB0p6AEAOj2oLSlmmpO21dNzBmmQNFlO6Z4-foy8F7P3cT9A5CSXY098lPNu1MtN68TILfmHV8MGLJJRe0Cj49CVL8M0MuZvLZwTjaAHHOhiqp25ZqTir68T90G-cU6nmGaloxIRSrVHOgXIo5JxiOn6HE7Msyf8sy-7KqvfJXzy840v_aqcDiAOQahTWkZ2tfNT4Cay-hig</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1917965582</pqid></control><display><type>article</type><title>Chance and necessity in the genome evolution of endosymbiotic bacteria of insects</title><source>MEDLINE</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Oxford Journals Open Access Collection</source><source>PubMed Central</source><creator>Sabater-Muñoz, Beatriz ; Toft, Christina ; Alvarez-Ponce, David ; Fares, Mario A</creator><creatorcontrib>Sabater-Muñoz, Beatriz ; Toft, Christina ; Alvarez-Ponce, David ; Fares, Mario A</creatorcontrib><description>An open question in evolutionary biology is how does the selection–drift balance determine the fates of biological interactions. We searched for signatures of selection and drift in genomes of five endosymbiotic bacterial groups known to evolve under strong genetic drift. Although most genes in endosymbiotic bacteria showed evidence of relaxed purifying selection, many genes in these bacteria exhibited stronger selective constraints than their orthologs in free-living bacterial relatives. Remarkably, most of these highly constrained genes had no role in the host–symbiont interactions but were involved in either buffering the deleterious consequences of drift or other host-unrelated functions, suggesting that they have either acquired new roles or their role became more central in endosymbiotic bacteria. Experimental evolution of Escherichia coli under strong genetic drift revealed remarkable similarities in the mutational spectrum, genome reduction patterns and gene losses to endosymbiotic bacteria of insects. Interestingly, the transcriptome of the experimentally evolved lines showed a generalized deregulation of the genome that affected genes encoding proteins involved in mutational buffering, regulation and amino acid biosynthesis, patterns identical to those found in endosymbiotic bacteria. Our results indicate that drift has shaped endosymbiotic associations through a change in the functional landscape of bacterial genes and that the host had only a small role in such a shift.</description><identifier>ISSN: 1751-7362</identifier><identifier>EISSN: 1751-7370</identifier><identifier>DOI: 10.1038/ismej.2017.18</identifier><identifier>PMID: 28323281</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>45/91 ; 631/181/735 ; 631/326/325/2482 ; Amino acids ; Animals ; Arthropods ; Bacteria ; Bacteria - genetics ; Biological evolution ; Biomedical and Life Sciences ; Biosynthesis ; Buffers ; Deregulation ; E coli ; Ecology ; Evolution ; Evolution, Molecular ; Evolutionary Biology ; Gene expression ; Genes ; Genetic Drift ; Genome, Bacterial ; Genomes ; Insecta - microbiology ; Insects ; Invertebrates ; Life Sciences ; Microbial Ecology ; Microbial Genetics and Genomics ; Microbiology ; Mutation ; Original ; original-article ; Proteins ; Selection, Genetic ; Symbiosis - genetics</subject><ispartof>The ISME Journal, 2017-06, Vol.11 (6), p.1291-1304</ispartof><rights>The Author(s) 2017</rights><rights>Copyright Nature Publishing Group Jun 2017</rights><rights>Copyright © 2017 International Society for Microbial Ecology 2017 International Society for Microbial Ecology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c454t-65f05e5d62f92734fb387c76ea1d0e55f219ae89a2979b9acbf22a2ce8089d2c3</citedby><cites>FETCH-LOGICAL-c454t-65f05e5d62f92734fb387c76ea1d0e55f219ae89a2979b9acbf22a2ce8089d2c3</cites><orcidid>0000-0002-4345-3013</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5437351/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5437351/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28323281$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sabater-Muñoz, Beatriz</creatorcontrib><creatorcontrib>Toft, Christina</creatorcontrib><creatorcontrib>Alvarez-Ponce, David</creatorcontrib><creatorcontrib>Fares, Mario A</creatorcontrib><title>Chance and necessity in the genome evolution of endosymbiotic bacteria of insects</title><title>The ISME Journal</title><addtitle>ISME J</addtitle><addtitle>ISME J</addtitle><description>An open question in evolutionary biology is how does the selection–drift balance determine the fates of biological interactions. We searched for signatures of selection and drift in genomes of five endosymbiotic bacterial groups known to evolve under strong genetic drift. Although most genes in endosymbiotic bacteria showed evidence of relaxed purifying selection, many genes in these bacteria exhibited stronger selective constraints than their orthologs in free-living bacterial relatives. Remarkably, most of these highly constrained genes had no role in the host–symbiont interactions but were involved in either buffering the deleterious consequences of drift or other host-unrelated functions, suggesting that they have either acquired new roles or their role became more central in endosymbiotic bacteria. Experimental evolution of Escherichia coli under strong genetic drift revealed remarkable similarities in the mutational spectrum, genome reduction patterns and gene losses to endosymbiotic bacteria of insects. Interestingly, the transcriptome of the experimentally evolved lines showed a generalized deregulation of the genome that affected genes encoding proteins involved in mutational buffering, regulation and amino acid biosynthesis, patterns identical to those found in endosymbiotic bacteria. Our results indicate that drift has shaped endosymbiotic associations through a change in the functional landscape of bacterial genes and that the host had only a small role in such a shift.</description><subject>45/91</subject><subject>631/181/735</subject><subject>631/326/325/2482</subject><subject>Amino acids</subject><subject>Animals</subject><subject>Arthropods</subject><subject>Bacteria</subject><subject>Bacteria - genetics</subject><subject>Biological evolution</subject><subject>Biomedical and Life Sciences</subject><subject>Biosynthesis</subject><subject>Buffers</subject><subject>Deregulation</subject><subject>E coli</subject><subject>Ecology</subject><subject>Evolution</subject><subject>Evolution, Molecular</subject><subject>Evolutionary Biology</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic Drift</subject><subject>Genome, Bacterial</subject><subject>Genomes</subject><subject>Insecta - microbiology</subject><subject>Insects</subject><subject>Invertebrates</subject><subject>Life Sciences</subject><subject>Microbial Ecology</subject><subject>Microbial Genetics and Genomics</subject><subject>Microbiology</subject><subject>Mutation</subject><subject>Original</subject><subject>original-article</subject><subject>Proteins</subject><subject>Selection, Genetic</subject><subject>Symbiosis - genetics</subject><issn>1751-7362</issn><issn>1751-7370</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>C6C</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNptkUtrGzEURkVpaV5dZhsE3XQzrh7WSNoUimmbQKAUmrXQaO7YMjNSKmkC_veR69QkJStd-A7n6vIhdEnJghKuPvs8wXbBCJULqt6gUyoFbSSX5O1xbtkJOst5S4iQbSvfoxOmOONM0VP0a7WxwQG2occBHOTsyw77gMsG8BpCnADDQxzn4mPAccAQ-ph3U-dj8Q531hVI3u4THzK4ki_Qu8GOGT48vefo7vu336vr5vbnj5vV19vGLcWyNK0YiADRt2zQTPLl0HElnWzB0p6AEAOj2oLSlmmpO21dNzBmmQNFlO6Z4-foy8F7P3cT9A5CSXY098lPNu1MtN68TILfmHV8MGLJJRe0Cj49CVL8M0MuZvLZwTjaAHHOhiqp25ZqTir68T90G-cU6nmGaloxIRSrVHOgXIo5JxiOn6HE7Msyf8sy-7KqvfJXzy840v_aqcDiAOQahTWkZ2tfNT4Cay-hig</recordid><startdate>20170601</startdate><enddate>20170601</enddate><creator>Sabater-Muñoz, Beatriz</creator><creator>Toft, Christina</creator><creator>Alvarez-Ponce, David</creator><creator>Fares, Mario A</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</general><scope>C6C</scope><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>3V.</scope><scope>7QL</scope><scope>7SN</scope><scope>7ST</scope><scope>7T7</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>P64</scope><scope>PATMY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PYCSY</scope><scope>SOI</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4345-3013</orcidid></search><sort><creationdate>20170601</creationdate><title>Chance and necessity in the genome evolution of endosymbiotic bacteria of insects</title><author>Sabater-Muñoz, Beatriz ; Toft, Christina ; Alvarez-Ponce, David ; Fares, Mario A</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c454t-65f05e5d62f92734fb387c76ea1d0e55f219ae89a2979b9acbf22a2ce8089d2c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>45/91</topic><topic>631/181/735</topic><topic>631/326/325/2482</topic><topic>Amino acids</topic><topic>Animals</topic><topic>Arthropods</topic><topic>Bacteria</topic><topic>Bacteria - genetics</topic><topic>Biological evolution</topic><topic>Biomedical and Life Sciences</topic><topic>Biosynthesis</topic><topic>Buffers</topic><topic>Deregulation</topic><topic>E coli</topic><topic>Ecology</topic><topic>Evolution</topic><topic>Evolution, Molecular</topic><topic>Evolutionary Biology</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genetic Drift</topic><topic>Genome, Bacterial</topic><topic>Genomes</topic><topic>Insecta - microbiology</topic><topic>Insects</topic><topic>Invertebrates</topic><topic>Life Sciences</topic><topic>Microbial Ecology</topic><topic>Microbial Genetics and Genomics</topic><topic>Microbiology</topic><topic>Mutation</topic><topic>Original</topic><topic>original-article</topic><topic>Proteins</topic><topic>Selection, Genetic</topic><topic>Symbiosis - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sabater-Muñoz, Beatriz</creatorcontrib><creatorcontrib>Toft, Christina</creatorcontrib><creatorcontrib>Alvarez-Ponce, David</creatorcontrib><creatorcontrib>Fares, Mario A</creatorcontrib><collection>Springer Nature OA Free Journals</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Ecology Abstracts</collection><collection>Environment Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Agricultural &amp; Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>Environmental Science Collection</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The ISME Journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sabater-Muñoz, Beatriz</au><au>Toft, Christina</au><au>Alvarez-Ponce, David</au><au>Fares, Mario A</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Chance and necessity in the genome evolution of endosymbiotic bacteria of insects</atitle><jtitle>The ISME Journal</jtitle><stitle>ISME J</stitle><addtitle>ISME J</addtitle><date>2017-06-01</date><risdate>2017</risdate><volume>11</volume><issue>6</issue><spage>1291</spage><epage>1304</epage><pages>1291-1304</pages><issn>1751-7362</issn><eissn>1751-7370</eissn><abstract>An open question in evolutionary biology is how does the selection–drift balance determine the fates of biological interactions. We searched for signatures of selection and drift in genomes of five endosymbiotic bacterial groups known to evolve under strong genetic drift. Although most genes in endosymbiotic bacteria showed evidence of relaxed purifying selection, many genes in these bacteria exhibited stronger selective constraints than their orthologs in free-living bacterial relatives. Remarkably, most of these highly constrained genes had no role in the host–symbiont interactions but were involved in either buffering the deleterious consequences of drift or other host-unrelated functions, suggesting that they have either acquired new roles or their role became more central in endosymbiotic bacteria. Experimental evolution of Escherichia coli under strong genetic drift revealed remarkable similarities in the mutational spectrum, genome reduction patterns and gene losses to endosymbiotic bacteria of insects. Interestingly, the transcriptome of the experimentally evolved lines showed a generalized deregulation of the genome that affected genes encoding proteins involved in mutational buffering, regulation and amino acid biosynthesis, patterns identical to those found in endosymbiotic bacteria. Our results indicate that drift has shaped endosymbiotic associations through a change in the functional landscape of bacterial genes and that the host had only a small role in such a shift.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>28323281</pmid><doi>10.1038/ismej.2017.18</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-4345-3013</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1751-7362
ispartof The ISME Journal, 2017-06, Vol.11 (6), p.1291-1304
issn 1751-7362
1751-7370
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_5437351
source MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Oxford Journals Open Access Collection; PubMed Central
subjects 45/91
631/181/735
631/326/325/2482
Amino acids
Animals
Arthropods
Bacteria
Bacteria - genetics
Biological evolution
Biomedical and Life Sciences
Biosynthesis
Buffers
Deregulation
E coli
Ecology
Evolution
Evolution, Molecular
Evolutionary Biology
Gene expression
Genes
Genetic Drift
Genome, Bacterial
Genomes
Insecta - microbiology
Insects
Invertebrates
Life Sciences
Microbial Ecology
Microbial Genetics and Genomics
Microbiology
Mutation
Original
original-article
Proteins
Selection, Genetic
Symbiosis - genetics
title Chance and necessity in the genome evolution of endosymbiotic bacteria of insects
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-23T05%3A42%3A45IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Chance%20and%20necessity%20in%20the%20genome%20evolution%20of%20endosymbiotic%20bacteria%20of%20insects&rft.jtitle=The%20ISME%20Journal&rft.au=Sabater-Mu%C3%B1oz,%20Beatriz&rft.date=2017-06-01&rft.volume=11&rft.issue=6&rft.spage=1291&rft.epage=1304&rft.pages=1291-1304&rft.issn=1751-7362&rft.eissn=1751-7370&rft_id=info:doi/10.1038/ismej.2017.18&rft_dat=%3Cproquest_pubme%3E1917965582%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1917965582&rft_id=info:pmid/28323281&rfr_iscdi=true