Host genetics and geography influence microbiome composition in the sponge Ircinia campana
Marine sponges are hosts to large, diverse communities of microorganisms. These microbiomes are distinct among sponge species and from seawater bacterial communities, indicating a key role of host identity in shaping its resident microbial community. However, the factors governing intraspecific micr...
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| Veröffentlicht in: | The Journal of animal ecology 2019-11, Vol.88 (11), p.1684-1695 |
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| container_title | The Journal of animal ecology |
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| creator | Griffiths, Sarah M. Antwis, Rachael E. Lenzi, Luca Lucaci, Anita Behringer, Donald C. Butler, Mark J. Preziosi, Richard F. Tate, Ann |
| description | Marine sponges are hosts to large, diverse communities of microorganisms. These microbiomes are distinct among sponge species and from seawater bacterial communities, indicating a key role of host identity in shaping its resident microbial community. However, the factors governing intraspecific microbiome variability are underexplored and may shed light on the evolutionary and ecological relationships between host and microbiome.
Here, we examined the influence of genetic variation and geographic location on the composition of the Ircinia campana microbiome.
We developed new microsatellite markers to genotype I. campana from two locations in the Florida Keys, USA, and characterized their microbiomes using V4 16S rRNA amplicon sequencing.
We show that microbial community composition and diversity is influenced by host genotype, with more genetically similar sponges hosting more similar microbial communities. We also found that although I. campana was not genetically differentiated between sites, microbiome composition differed by location.
Our results demonstrate that both host genetics and geography influence the composition of the sponge microbiome. Host genotypic influence on microbiome composition may be due to stable vertical transmission of the microbial community from parent to offspring, making microbiomes more similar by descent. Alternatively, sponge genotypic variation may reflect variation in functional traits that influence the acquisition of environmental microbes. This study reveals drivers of microbiome variation within and among locations, and shows the importance of intraspecific variability in mediating eco‐evolutionary dynamics of host‐associated microbiomes.
For the first time, the authors show that intraspecific genetic variation affects microbiome composition in a marine sponge (Ircinia campana), with positive correlations observed between genetic and microbiome similarity. This has significant implications for our understanding of the ecological and evolutionary relationships between host and microbiome in this important model system. |
| doi_str_mv | 10.1111/1365-2656.13065 |
| format | Article |
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Here, we examined the influence of genetic variation and geographic location on the composition of the Ircinia campana microbiome.
We developed new microsatellite markers to genotype I. campana from two locations in the Florida Keys, USA, and characterized their microbiomes using V4 16S rRNA amplicon sequencing.
We show that microbial community composition and diversity is influenced by host genotype, with more genetically similar sponges hosting more similar microbial communities. We also found that although I. campana was not genetically differentiated between sites, microbiome composition differed by location.
Our results demonstrate that both host genetics and geography influence the composition of the sponge microbiome. Host genotypic influence on microbiome composition may be due to stable vertical transmission of the microbial community from parent to offspring, making microbiomes more similar by descent. Alternatively, sponge genotypic variation may reflect variation in functional traits that influence the acquisition of environmental microbes. This study reveals drivers of microbiome variation within and among locations, and shows the importance of intraspecific variability in mediating eco‐evolutionary dynamics of host‐associated microbiomes.
For the first time, the authors show that intraspecific genetic variation affects microbiome composition in a marine sponge (Ircinia campana), with positive correlations observed between genetic and microbiome similarity. This has significant implications for our understanding of the ecological and evolutionary relationships between host and microbiome in this important model system.</description><identifier>ISSN: 0021-8790</identifier><identifier>EISSN: 1365-2656</identifier><identifier>DOI: 10.1111/1365-2656.13065</identifier><identifier>PMID: 31325164</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Animals ; bacteria ; Communities ; Community composition ; Composition ; core microbiome ; Ecological effects ; eco‐evolutionary dynamics ; Florida ; Genetic diversity ; Genetic markers ; Genetics ; Genotypes ; Geographical locations ; Geography ; host–microbe interactions ; Ircinia campana ; Marine microorganisms ; Microbial activity ; Microbiomes ; Microbiota ; Microorganisms ; Microsatellites ; Molecular Ecology ; Offspring ; Phylogeny ; Porifera ; RNA, Ribosomal, 16S ; rRNA 16S ; Seawater ; Sponges</subject><ispartof>The Journal of animal ecology, 2019-11, Vol.88 (11), p.1684-1695</ispartof><rights>2019 The Authors. published by John Wiley & Sons Ltd on behalf of British Ecological Society</rights><rights>2019 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.</rights><rights>Journal of Animal Ecology © 2019 British Ecological Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4275-c6b101d6faf7e9729e6496fc903a684ec3bdffbecc98d8fa79b819e1c71883233</citedby><cites>FETCH-LOGICAL-c4275-c6b101d6faf7e9729e6496fc903a684ec3bdffbecc98d8fa79b819e1c71883233</cites><orcidid>0000-0002-8849-8194 ; 0000-0003-4743-049X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2F1365-2656.13065$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2F1365-2656.13065$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,1417,1433,27924,27925,45574,45575,46409,46833</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31325164$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Tate, Ann</contributor><creatorcontrib>Griffiths, Sarah M.</creatorcontrib><creatorcontrib>Antwis, Rachael E.</creatorcontrib><creatorcontrib>Lenzi, Luca</creatorcontrib><creatorcontrib>Lucaci, Anita</creatorcontrib><creatorcontrib>Behringer, Donald C.</creatorcontrib><creatorcontrib>Butler, Mark J.</creatorcontrib><creatorcontrib>Preziosi, Richard F.</creatorcontrib><creatorcontrib>Tate, Ann</creatorcontrib><title>Host genetics and geography influence microbiome composition in the sponge Ircinia campana</title><title>The Journal of animal ecology</title><addtitle>J Anim Ecol</addtitle><description>Marine sponges are hosts to large, diverse communities of microorganisms. These microbiomes are distinct among sponge species and from seawater bacterial communities, indicating a key role of host identity in shaping its resident microbial community. However, the factors governing intraspecific microbiome variability are underexplored and may shed light on the evolutionary and ecological relationships between host and microbiome.
Here, we examined the influence of genetic variation and geographic location on the composition of the Ircinia campana microbiome.
We developed new microsatellite markers to genotype I. campana from two locations in the Florida Keys, USA, and characterized their microbiomes using V4 16S rRNA amplicon sequencing.
We show that microbial community composition and diversity is influenced by host genotype, with more genetically similar sponges hosting more similar microbial communities. We also found that although I. campana was not genetically differentiated between sites, microbiome composition differed by location.
Our results demonstrate that both host genetics and geography influence the composition of the sponge microbiome. Host genotypic influence on microbiome composition may be due to stable vertical transmission of the microbial community from parent to offspring, making microbiomes more similar by descent. Alternatively, sponge genotypic variation may reflect variation in functional traits that influence the acquisition of environmental microbes. This study reveals drivers of microbiome variation within and among locations, and shows the importance of intraspecific variability in mediating eco‐evolutionary dynamics of host‐associated microbiomes.
For the first time, the authors show that intraspecific genetic variation affects microbiome composition in a marine sponge (Ircinia campana), with positive correlations observed between genetic and microbiome similarity. This has significant implications for our understanding of the ecological and evolutionary relationships between host and microbiome in this important model system.</description><subject>Animals</subject><subject>bacteria</subject><subject>Communities</subject><subject>Community composition</subject><subject>Composition</subject><subject>core microbiome</subject><subject>Ecological effects</subject><subject>eco‐evolutionary dynamics</subject><subject>Florida</subject><subject>Genetic diversity</subject><subject>Genetic markers</subject><subject>Genetics</subject><subject>Genotypes</subject><subject>Geographical locations</subject><subject>Geography</subject><subject>host–microbe interactions</subject><subject>Ircinia campana</subject><subject>Marine microorganisms</subject><subject>Microbial activity</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>Microorganisms</subject><subject>Microsatellites</subject><subject>Molecular Ecology</subject><subject>Offspring</subject><subject>Phylogeny</subject><subject>Porifera</subject><subject>RNA, Ribosomal, 16S</subject><subject>rRNA 16S</subject><subject>Seawater</subject><subject>Sponges</subject><issn>0021-8790</issn><issn>1365-2656</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><recordid>eNqFkUtv1DAURi0EokNhzQ5ZYsMmrR-JHxukquoLVXRTNmwsx7mecZXYIU5A8-_xMGVEu8GbK_seH_n6Q-g9JSe0rFPKRVMx0YgTyoloXqDV4eQlWhHCaKWkJkfoTc4PhBDJCH-NjjjlrKGiXqHv1ynPeA0R5uAytrErm7Se7LjZ4hB9v0B0gIfgptSGNAB2aRhTDnNIsQB43gDOY4prwDeTCzFY7Oww2mjfolfe9hnePdZj9O3y4v78urq9u7o5P7utXM1kUznRUkI74a2XoCXTIGotvNOEW6FqcLztvG_BOa065a3UraIaqJNUKc44P0af995xaQfoHMR5sr0ZpzDYaWuSDeZpJ4aNWaefRiittdBF8OlRMKUfC-TZDCE76HsbIS3ZMCaoFoo2sqAfn6EPaZliGc8wThkRRNY74emeKp-W8wT-8BhKzC43s0vJ7FIyf3IrNz78O8OB_xtUAcQe-BV62P7PZ76cfb3Ym38DDjWkCQ</recordid><startdate>201911</startdate><enddate>201911</enddate><creator>Griffiths, Sarah M.</creator><creator>Antwis, Rachael E.</creator><creator>Lenzi, Luca</creator><creator>Lucaci, Anita</creator><creator>Behringer, Donald C.</creator><creator>Butler, Mark J.</creator><creator>Preziosi, Richard F.</creator><creator>Tate, Ann</creator><general>Blackwell Publishing Ltd</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</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>7QG</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8849-8194</orcidid><orcidid>https://orcid.org/0000-0003-4743-049X</orcidid></search><sort><creationdate>201911</creationdate><title>Host genetics and geography influence microbiome composition in the sponge Ircinia campana</title><author>Griffiths, Sarah M. ; Antwis, Rachael E. ; Lenzi, Luca ; Lucaci, Anita ; Behringer, Donald C. ; Butler, Mark J. ; Preziosi, Richard F. ; Tate, Ann</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4275-c6b101d6faf7e9729e6496fc903a684ec3bdffbecc98d8fa79b819e1c71883233</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>bacteria</topic><topic>Communities</topic><topic>Community composition</topic><topic>Composition</topic><topic>core microbiome</topic><topic>Ecological effects</topic><topic>eco‐evolutionary dynamics</topic><topic>Florida</topic><topic>Genetic diversity</topic><topic>Genetic markers</topic><topic>Genetics</topic><topic>Genotypes</topic><topic>Geographical locations</topic><topic>Geography</topic><topic>host–microbe interactions</topic><topic>Ircinia campana</topic><topic>Marine microorganisms</topic><topic>Microbial activity</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>Microorganisms</topic><topic>Microsatellites</topic><topic>Molecular Ecology</topic><topic>Offspring</topic><topic>Phylogeny</topic><topic>Porifera</topic><topic>RNA, Ribosomal, 16S</topic><topic>rRNA 16S</topic><topic>Seawater</topic><topic>Sponges</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Griffiths, Sarah M.</creatorcontrib><creatorcontrib>Antwis, Rachael E.</creatorcontrib><creatorcontrib>Lenzi, Luca</creatorcontrib><creatorcontrib>Lucaci, Anita</creatorcontrib><creatorcontrib>Behringer, Donald C.</creatorcontrib><creatorcontrib>Butler, Mark J.</creatorcontrib><creatorcontrib>Preziosi, Richard F.</creatorcontrib><creatorcontrib>Tate, Ann</creatorcontrib><collection>Wiley Online Library (Open Access Collection)</collection><collection>Wiley Online Library (Open Access Collection)</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of animal ecology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Griffiths, Sarah M.</au><au>Antwis, Rachael E.</au><au>Lenzi, Luca</au><au>Lucaci, Anita</au><au>Behringer, Donald C.</au><au>Butler, Mark J.</au><au>Preziosi, Richard F.</au><au>Tate, Ann</au><au>Tate, Ann</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Host genetics and geography influence microbiome composition in the sponge Ircinia campana</atitle><jtitle>The Journal of animal ecology</jtitle><addtitle>J Anim Ecol</addtitle><date>2019-11</date><risdate>2019</risdate><volume>88</volume><issue>11</issue><spage>1684</spage><epage>1695</epage><pages>1684-1695</pages><issn>0021-8790</issn><eissn>1365-2656</eissn><abstract>Marine sponges are hosts to large, diverse communities of microorganisms. These microbiomes are distinct among sponge species and from seawater bacterial communities, indicating a key role of host identity in shaping its resident microbial community. However, the factors governing intraspecific microbiome variability are underexplored and may shed light on the evolutionary and ecological relationships between host and microbiome.
Here, we examined the influence of genetic variation and geographic location on the composition of the Ircinia campana microbiome.
We developed new microsatellite markers to genotype I. campana from two locations in the Florida Keys, USA, and characterized their microbiomes using V4 16S rRNA amplicon sequencing.
We show that microbial community composition and diversity is influenced by host genotype, with more genetically similar sponges hosting more similar microbial communities. We also found that although I. campana was not genetically differentiated between sites, microbiome composition differed by location.
Our results demonstrate that both host genetics and geography influence the composition of the sponge microbiome. Host genotypic influence on microbiome composition may be due to stable vertical transmission of the microbial community from parent to offspring, making microbiomes more similar by descent. Alternatively, sponge genotypic variation may reflect variation in functional traits that influence the acquisition of environmental microbes. This study reveals drivers of microbiome variation within and among locations, and shows the importance of intraspecific variability in mediating eco‐evolutionary dynamics of host‐associated microbiomes.
For the first time, the authors show that intraspecific genetic variation affects microbiome composition in a marine sponge (Ircinia campana), with positive correlations observed between genetic and microbiome similarity. This has significant implications for our understanding of the ecological and evolutionary relationships between host and microbiome in this important model system.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>31325164</pmid><doi>10.1111/1365-2656.13065</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-8849-8194</orcidid><orcidid>https://orcid.org/0000-0003-4743-049X</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals bacteria Communities Community composition Composition core microbiome Ecological effects eco‐evolutionary dynamics Florida Genetic diversity Genetic markers Genetics Genotypes Geographical locations Geography host–microbe interactions Ircinia campana Marine microorganisms Microbial activity Microbiomes Microbiota Microorganisms Microsatellites Molecular Ecology Offspring Phylogeny Porifera RNA, Ribosomal, 16S rRNA 16S Seawater Sponges |
| title | Host genetics and geography influence microbiome composition in the sponge Ircinia campana |
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