Deep divergence and rapid evolutionary rates in gut-associated Acetobacteraceae of ants
Symbiotic associations between gut microbiota and their animal hosts shape the evolutionary trajectories of both partners. The genomic consequences of these relationships are significantly influenced by a variety of factors, including niche localization, interaction potential, and symbiont transmiss...
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| description | Symbiotic associations between gut microbiota and their animal hosts shape the evolutionary trajectories of both partners. The genomic consequences of these relationships are significantly influenced by a variety of factors, including niche localization, interaction potential, and symbiont transmission mode. In eusocial insect hosts, socially transmitted gut microbiota may represent an intermediate point between free living or environmentally acquired bacteria and those with strict host association and maternal transmission.
We characterized the bacterial communities associated with an abundant ant species, Camponotus chromaiodes. While many bacteria had sporadic distributions, some taxa were abundant and persistent within and across ant colonies. Specially, two Acetobacteraceae operational taxonomic units (OTUs; referred to as AAB1 and AAB2) were abundant and widespread across host samples. Dissection experiments confirmed that AAB1 and AAB2 occur in C. chromaiodes gut tracts. We explored the distribution and evolution of these Acetobacteraceae OTUs in more depth. We found that Camponotus hosts representing different species and geographical regions possess close relatives of the Acetobacteraceae OTUs detected in C. chromaiodes. Phylogenetic analysis revealed that AAB1 and AAB2 join other ant associates in a monophyletic clade. This clade consists of Acetobacteraceae from three ant tribes, including a third, basal lineage associated with Attine ants. This ant-specific AAB clade exhibits a significant acceleration of substitution rates at the 16S rDNA gene and elevated AT content. Substitutions along 16S rRNA in AAB1 and AAB2 result in ~10 % reduction in the predicted rRNA stability.
Combined, these patterns in Camponotus-associated Acetobacteraceae resemble those found in cospeciating gut associates that are both socially and maternally transmitted. These associates may represent an intermediate point along an evolutionary trajectory manifest most extremely in symbionts with strict maternal transmission. Collectively, these results suggest that Acetobacteraceae may be a frequent and persistent gut associate in Camponotus species and perhaps other ant groups, and that its evolution is strongly impacted by this host association. |
| doi_str_mv | 10.1186/s12866-016-0721-8 |
| format | Article |
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We characterized the bacterial communities associated with an abundant ant species, Camponotus chromaiodes. While many bacteria had sporadic distributions, some taxa were abundant and persistent within and across ant colonies. Specially, two Acetobacteraceae operational taxonomic units (OTUs; referred to as AAB1 and AAB2) were abundant and widespread across host samples. Dissection experiments confirmed that AAB1 and AAB2 occur in C. chromaiodes gut tracts. We explored the distribution and evolution of these Acetobacteraceae OTUs in more depth. We found that Camponotus hosts representing different species and geographical regions possess close relatives of the Acetobacteraceae OTUs detected in C. chromaiodes. Phylogenetic analysis revealed that AAB1 and AAB2 join other ant associates in a monophyletic clade. This clade consists of Acetobacteraceae from three ant tribes, including a third, basal lineage associated with Attine ants. This ant-specific AAB clade exhibits a significant acceleration of substitution rates at the 16S rDNA gene and elevated AT content. Substitutions along 16S rRNA in AAB1 and AAB2 result in ~10 % reduction in the predicted rRNA stability.
Combined, these patterns in Camponotus-associated Acetobacteraceae resemble those found in cospeciating gut associates that are both socially and maternally transmitted. These associates may represent an intermediate point along an evolutionary trajectory manifest most extremely in symbionts with strict maternal transmission. Collectively, these results suggest that Acetobacteraceae may be a frequent and persistent gut associate in Camponotus species and perhaps other ant groups, and that its evolution is strongly impacted by this host association.</description><identifier>ISSN: 1471-2180</identifier><identifier>EISSN: 1471-2180</identifier><identifier>DOI: 10.1186/s12866-016-0721-8</identifier><identifier>PMID: 27400652</identifier><language>eng</language><publisher>England: BioMed Central Ltd</publisher><subject>Acetobacteraceae - genetics ; Acetobacteraceae - isolation & purification ; Acetobacteraceae - physiology ; Adaptation (Biology) ; Analysis ; Animals ; Ants - classification ; Ants - microbiology ; Bacteria ; Base Sequence ; Biodiversity ; Biological Evolution ; Cladistic analysis ; DNA, Bacterial - genetics ; DNA, Ribosomal - genetics ; Evolution, Molecular ; Gastrointestinal Microbiome ; Genes, Bacterial ; Genomes ; Host Specificity ; Microbial Consortia ; Microbiota ; Pathogens ; Phylogeny ; RNA, Ribosomal, 16S - genetics ; Sequence Alignment ; Sequence Analysis, DNA ; Symbiosis</subject><ispartof>BMC microbiology, 2016-07, Vol.16 (1), p.140-140, Article 140</ispartof><rights>COPYRIGHT 2016 BioMed Central Ltd.</rights><rights>Copyright BioMed Central 2016</rights><rights>The Author(s). 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c455t-2486d13c0b2b801199b9950506387ba2907590cb54b062b14c935e1642079f743</citedby><cites>FETCH-LOGICAL-c455t-2486d13c0b2b801199b9950506387ba2907590cb54b062b14c935e1642079f743</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4939635/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4939635/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27400652$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Brown, Bryan P</creatorcontrib><creatorcontrib>Wernegreen, Jennifer J</creatorcontrib><title>Deep divergence and rapid evolutionary rates in gut-associated Acetobacteraceae of ants</title><title>BMC microbiology</title><addtitle>BMC Microbiol</addtitle><description>Symbiotic associations between gut microbiota and their animal hosts shape the evolutionary trajectories of both partners. The genomic consequences of these relationships are significantly influenced by a variety of factors, including niche localization, interaction potential, and symbiont transmission mode. In eusocial insect hosts, socially transmitted gut microbiota may represent an intermediate point between free living or environmentally acquired bacteria and those with strict host association and maternal transmission.
We characterized the bacterial communities associated with an abundant ant species, Camponotus chromaiodes. While many bacteria had sporadic distributions, some taxa were abundant and persistent within and across ant colonies. Specially, two Acetobacteraceae operational taxonomic units (OTUs; referred to as AAB1 and AAB2) were abundant and widespread across host samples. Dissection experiments confirmed that AAB1 and AAB2 occur in C. chromaiodes gut tracts. We explored the distribution and evolution of these Acetobacteraceae OTUs in more depth. We found that Camponotus hosts representing different species and geographical regions possess close relatives of the Acetobacteraceae OTUs detected in C. chromaiodes. Phylogenetic analysis revealed that AAB1 and AAB2 join other ant associates in a monophyletic clade. This clade consists of Acetobacteraceae from three ant tribes, including a third, basal lineage associated with Attine ants. This ant-specific AAB clade exhibits a significant acceleration of substitution rates at the 16S rDNA gene and elevated AT content. Substitutions along 16S rRNA in AAB1 and AAB2 result in ~10 % reduction in the predicted rRNA stability.
Combined, these patterns in Camponotus-associated Acetobacteraceae resemble those found in cospeciating gut associates that are both socially and maternally transmitted. These associates may represent an intermediate point along an evolutionary trajectory manifest most extremely in symbionts with strict maternal transmission. Collectively, these results suggest that Acetobacteraceae may be a frequent and persistent gut associate in Camponotus species and perhaps other ant groups, and that its evolution is strongly impacted by this host association.</description><subject>Acetobacteraceae - genetics</subject><subject>Acetobacteraceae - isolation & purification</subject><subject>Acetobacteraceae - physiology</subject><subject>Adaptation (Biology)</subject><subject>Analysis</subject><subject>Animals</subject><subject>Ants - classification</subject><subject>Ants - microbiology</subject><subject>Bacteria</subject><subject>Base Sequence</subject><subject>Biodiversity</subject><subject>Biological Evolution</subject><subject>Cladistic analysis</subject><subject>DNA, Bacterial - genetics</subject><subject>DNA, Ribosomal - genetics</subject><subject>Evolution, Molecular</subject><subject>Gastrointestinal Microbiome</subject><subject>Genes, Bacterial</subject><subject>Genomes</subject><subject>Host Specificity</subject><subject>Microbial Consortia</subject><subject>Microbiota</subject><subject>Pathogens</subject><subject>Phylogeny</subject><subject>RNA, Ribosomal, 16S - genetics</subject><subject>Sequence Alignment</subject><subject>Sequence Analysis, DNA</subject><subject>Symbiosis</subject><issn>1471-2180</issn><issn>1471-2180</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNpdkV1rFDEUhoNYbK3-AG9kwBtvxub740ZYWr-g0BvFy5Bkzqwps5M1ySz475th61IlhIST97znnDwIvSH4AyFaXhVCtZQ9Jm0rSnr9DF0QrkhPicbPn9zP0ctS7jEmSjP1Ap1TxTGWgl6gnzcA-26IB8hbmAN0bh667PZx6OCQpqXGNLv8p4UqlC7O3XapvSslhdgiQ7cJUJN3oUJ2ARx0aWwWtbxCZ6ObCrx-PC_Rj8-fvl9_7W_vvny73tz2gQtRe8q1HAgL2FOvMSHGeGMEFlgyrbyjBithcPCCeyypJzwYJoBITrEyo-LsEn08-u4Xv4MhwFyzm-w-x11r2yYX7b8vc_xlt-lguWFGMtEM3j8a5PR7gVLtLpYA0-RmSEux7feYMm2xJn33n_Q-LXlu460qpRWXzfKk2roJbJzH1OqG1dRuuNC4IcNrWXJUhZxKyTCeWibYrnDtEa5tcO0K1-qW8_bprKeMvzTZA3tRnZ8</recordid><startdate>20160711</startdate><enddate>20160711</enddate><creator>Brown, Bryan P</creator><creator>Wernegreen, Jennifer J</creator><general>BioMed Central Ltd</general><general>BioMed Central</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>3V.</scope><scope>7QL</scope><scope>7T7</scope><scope>7U9</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>AEUYN</scope><scope>AFKRA</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>H94</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>PHGZM</scope><scope>PHGZT</scope><scope>PIMPY</scope><scope>PJZUB</scope><scope>PKEHL</scope><scope>PPXIY</scope><scope>PQEST</scope><scope>PQGLB</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20160711</creationdate><title>Deep divergence and rapid evolutionary rates in gut-associated Acetobacteraceae of ants</title><author>Brown, Bryan P ; Wernegreen, Jennifer J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c455t-2486d13c0b2b801199b9950506387ba2907590cb54b062b14c935e1642079f743</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Acetobacteraceae - genetics</topic><topic>Acetobacteraceae - isolation & purification</topic><topic>Acetobacteraceae - physiology</topic><topic>Adaptation (Biology)</topic><topic>Analysis</topic><topic>Animals</topic><topic>Ants - classification</topic><topic>Ants - microbiology</topic><topic>Bacteria</topic><topic>Base Sequence</topic><topic>Biodiversity</topic><topic>Biological Evolution</topic><topic>Cladistic analysis</topic><topic>DNA, Bacterial - genetics</topic><topic>DNA, Ribosomal - genetics</topic><topic>Evolution, Molecular</topic><topic>Gastrointestinal Microbiome</topic><topic>Genes, Bacterial</topic><topic>Genomes</topic><topic>Host Specificity</topic><topic>Microbial Consortia</topic><topic>Microbiota</topic><topic>Pathogens</topic><topic>Phylogeny</topic><topic>RNA, Ribosomal, 16S - genetics</topic><topic>Sequence Alignment</topic><topic>Sequence Analysis, DNA</topic><topic>Symbiosis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brown, Bryan P</creatorcontrib><creatorcontrib>Wernegreen, Jennifer J</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 Central (Corporate)</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Virology and AIDS Abstracts</collection><collection>Health & 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 One Sustainability</collection><collection>ProQuest Central UK/Ireland</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>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & 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>ProQuest Central (New)</collection><collection>ProQuest One Academic (New)</collection><collection>Publicly Available Content Database</collection><collection>ProQuest Health & Medical Research Collection</collection><collection>ProQuest One Academic Middle East (New)</collection><collection>ProQuest One Health & Nursing</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Applied & Life Sciences</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>BMC microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brown, Bryan P</au><au>Wernegreen, Jennifer J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Deep divergence and rapid evolutionary rates in gut-associated Acetobacteraceae of ants</atitle><jtitle>BMC microbiology</jtitle><addtitle>BMC Microbiol</addtitle><date>2016-07-11</date><risdate>2016</risdate><volume>16</volume><issue>1</issue><spage>140</spage><epage>140</epage><pages>140-140</pages><artnum>140</artnum><issn>1471-2180</issn><eissn>1471-2180</eissn><abstract>Symbiotic associations between gut microbiota and their animal hosts shape the evolutionary trajectories of both partners. The genomic consequences of these relationships are significantly influenced by a variety of factors, including niche localization, interaction potential, and symbiont transmission mode. In eusocial insect hosts, socially transmitted gut microbiota may represent an intermediate point between free living or environmentally acquired bacteria and those with strict host association and maternal transmission.
We characterized the bacterial communities associated with an abundant ant species, Camponotus chromaiodes. While many bacteria had sporadic distributions, some taxa were abundant and persistent within and across ant colonies. Specially, two Acetobacteraceae operational taxonomic units (OTUs; referred to as AAB1 and AAB2) were abundant and widespread across host samples. Dissection experiments confirmed that AAB1 and AAB2 occur in C. chromaiodes gut tracts. We explored the distribution and evolution of these Acetobacteraceae OTUs in more depth. We found that Camponotus hosts representing different species and geographical regions possess close relatives of the Acetobacteraceae OTUs detected in C. chromaiodes. Phylogenetic analysis revealed that AAB1 and AAB2 join other ant associates in a monophyletic clade. This clade consists of Acetobacteraceae from three ant tribes, including a third, basal lineage associated with Attine ants. This ant-specific AAB clade exhibits a significant acceleration of substitution rates at the 16S rDNA gene and elevated AT content. Substitutions along 16S rRNA in AAB1 and AAB2 result in ~10 % reduction in the predicted rRNA stability.
Combined, these patterns in Camponotus-associated Acetobacteraceae resemble those found in cospeciating gut associates that are both socially and maternally transmitted. These associates may represent an intermediate point along an evolutionary trajectory manifest most extremely in symbionts with strict maternal transmission. Collectively, these results suggest that Acetobacteraceae may be a frequent and persistent gut associate in Camponotus species and perhaps other ant groups, and that its evolution is strongly impacted by this host association.</abstract><cop>England</cop><pub>BioMed Central Ltd</pub><pmid>27400652</pmid><doi>10.1186/s12866-016-0721-8</doi><tpages>1</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Acetobacteraceae - genetics Acetobacteraceae - isolation & purification Acetobacteraceae - physiology Adaptation (Biology) Analysis Animals Ants - classification Ants - microbiology Bacteria Base Sequence Biodiversity Biological Evolution Cladistic analysis DNA, Bacterial - genetics DNA, Ribosomal - genetics Evolution, Molecular Gastrointestinal Microbiome Genes, Bacterial Genomes Host Specificity Microbial Consortia Microbiota Pathogens Phylogeny RNA, Ribosomal, 16S - genetics Sequence Alignment Sequence Analysis, DNA Symbiosis |
| title | Deep divergence and rapid evolutionary rates in gut-associated Acetobacteraceae of ants |
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