Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts
Identifieur interne : 000401 ( Pmc/Corpus ); précédent : 000400; suivant : 000402Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts
Auteurs : Lu Fan ; David Reynolds ; Michael Liu ; Manuel Stark ; Staffan Kjelleberg ; Nicole S. Webster ; Torsten ThomasSource :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2012.
Abstract
Microorganisms often form symbiotic relationships with eukaryotes, and the complexity of these relationships can range from those with one single dominant symbiont to associations with hundreds of symbiont species. Microbial symbionts occupying equivalent niches in different eukaryotic hosts may share functional aspects, and convergent genome evolution has been reported for simple symbiont systems in insects. However, for complex symbiont communities, it is largely unknown how prevalent functional equivalence is and whether equivalent functions are conducted by evolutionarily convergent mechanisms. Sponges represent an evolutionarily divergent group of species with common physiological and ecological traits. They also host complex communities of microbial symbionts and thus are the ideal model to test whether functional equivalence and evolutionary convergence exist in complex symbiont communities across phylogenetically divergent hosts. Here we use a sampling design to determine the phylogenetic and functional profiles of microbial communities associated with six sponge species. We identify common functions in the six microbiomes, demonstrating the existence of functional equivalence. These core functions are consistent with our current understanding of the biological and ecological roles of sponge-associated microorganisms and also provide insight into symbiont functions. Importantly, core functions also are provided in each sponge species by analogous enzymes and biosynthetic pathways. Moreover, the abundance of elements involved in horizontal gene transfer suggests their key roles in the genomic evolution of symbionts. Our data thus demonstrate evolutionary convergence in complex symbiont communities and reveal the details and mechanisms that underpin the process.
Url:
DOI: 10.1073/pnas.1203287109
PubMed: 22699508
PubMed Central: 3390844
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PMC:3390844Le document en format XML
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<front><div type="abstract" xml:lang="en"><p>Microorganisms often form symbiotic relationships with eukaryotes, and the complexity of these relationships can range from those with one single dominant symbiont to associations with hundreds of symbiont species. Microbial symbionts occupying equivalent niches in different eukaryotic hosts may share functional aspects, and convergent genome evolution has been reported for simple symbiont systems in insects. However, for complex symbiont communities, it is largely unknown how prevalent functional equivalence is and whether equivalent functions are conducted by evolutionarily convergent mechanisms. Sponges represent an evolutionarily divergent group of species with common physiological and ecological traits. They also host complex communities of microbial symbionts and thus are the ideal model to test whether functional equivalence and evolutionary convergence exist in complex symbiont communities across phylogenetically divergent hosts. Here we use a sampling design to determine the phylogenetic and functional profiles of microbial communities associated with six sponge species. We identify common functions in the six microbiomes, demonstrating the existence of functional equivalence. These core functions are consistent with our current understanding of the biological and ecological roles of sponge-associated microorganisms and also provide insight into symbiont functions. Importantly, core functions also are provided in each sponge species by analogous enzymes and biosynthetic pathways. Moreover, the abundance of elements involved in horizontal gene transfer suggests their key roles in the genomic evolution of symbionts. Our data thus demonstrate evolutionary convergence in complex symbiont communities and reveal the details and mechanisms that underpin the process.</p>
</div>
</front>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id>
<journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id>
<journal-id journal-id-type="hwp">pnas</journal-id>
<journal-id journal-id-type="pmc">pnas</journal-id>
<journal-id journal-id-type="publisher-id">PNAS</journal-id>
<journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title>
</journal-title-group>
<issn pub-type="ppub">0027-8424</issn>
<issn pub-type="epub">1091-6490</issn>
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<article-id pub-id-type="pmc">3390844</article-id>
<article-id pub-id-type="publisher-id">201203287</article-id>
<article-id pub-id-type="doi">10.1073/pnas.1203287109</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>PNAS Plus</subject>
</subj-group>
<subj-group subj-group-type="heading"><subject>Biological Sciences</subject>
<subj-group><subject>Microbiology</subject>
</subj-group>
</subj-group>
<series-title>PNAS Plus</series-title>
</article-categories>
<title-group><article-title>Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts</article-title>
<alt-title alt-title-type="short">Evolution of complex symbiont communities</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Fan</surname>
<given-names>Lu</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Reynolds</surname>
<given-names>David</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Liu</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stark</surname>
<given-names>Manuel</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kjelleberg</surname>
<given-names>Staffan</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Webster</surname>
<given-names>Nicole S.</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thomas</surname>
<given-names>Torsten</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
<xref ref-type="corresp" rid="cor1"><sup>1</sup>
</xref>
</contrib>
<aff id="aff1"><sup>a</sup>
School of Biotechnology and Biomolecular Sciences and</aff>
<aff id="aff2"><sup>b</sup>
Centre for Marine Bio-Innovation,<institution>University of New South Wales</institution>
, Sydney, New South Wales 2052,<country>Australia</country>
;</aff>
<aff id="aff3"><sup>c</sup>
Institute of Molecular Life Sciences and</aff>
<aff id="aff4"><sup>d</sup>
Swiss Institute of Bioinformatics,<institution>University of Zurich</institution>
, 8057 Zurich,<country>Switzerland</country>
;</aff>
<aff id="aff5"><sup>e</sup>
Singapore Centre on Environmental Life Sciences Engineering,<institution>Nanyang Technological University</institution>
,<country>Republic of Singapore</country>
; and</aff>
<aff id="aff6"><sup>f</sup>
<institution>Australian Institute of Marine Science</institution>
, Townsville, Queensland 4810,<country>Australia</country>
</aff>
</contrib-group>
<author-notes><corresp id="cor1"><sup>1</sup>
To whom correspondence should be addressed. E-mail: <email>t.thomas@unsw.edu.au</email>
.</corresp>
<fn fn-type="edited-by"><p>Edited by W. Ford Doolittle, Dalhousie University, Halifax, NS, Canada, and approved May 21, 2012 (received for review February 24, 2012)</p>
</fn>
<fn fn-type="con"><p>Author contributions: L.F., N.S.W., and T.T. designed research; L.F., N.S.W., and T.T. performed research; L.F., D.R., M.L., M.S., and T.T. analyzed data; and L.F., D.R., S.K., N.S.W., and T.T. wrote the paper.</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><day>3</day>
<month>7</month>
<year>2012</year>
</pub-date>
<pub-date pub-type="epub"><day>13</day>
<month>6</month>
<year>2012</year>
</pub-date>
<volume>109</volume>
<issue>27</issue>
<fpage>E1878</fpage>
<lpage>E1887</lpage>
<page-range>E1878–E1887</page-range>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pnas.201203287.pdf"></self-uri>
<self-uri content-type="author-summary-pdf" xlink:type="simple" xlink:href="pnas.201203287_summary.pdf"></self-uri>
<abstract id="d34e220"><p>Microorganisms often form symbiotic relationships with eukaryotes, and the complexity of these relationships can range from those with one single dominant symbiont to associations with hundreds of symbiont species. Microbial symbionts occupying equivalent niches in different eukaryotic hosts may share functional aspects, and convergent genome evolution has been reported for simple symbiont systems in insects. However, for complex symbiont communities, it is largely unknown how prevalent functional equivalence is and whether equivalent functions are conducted by evolutionarily convergent mechanisms. Sponges represent an evolutionarily divergent group of species with common physiological and ecological traits. They also host complex communities of microbial symbionts and thus are the ideal model to test whether functional equivalence and evolutionary convergence exist in complex symbiont communities across phylogenetically divergent hosts. Here we use a sampling design to determine the phylogenetic and functional profiles of microbial communities associated with six sponge species. We identify common functions in the six microbiomes, demonstrating the existence of functional equivalence. These core functions are consistent with our current understanding of the biological and ecological roles of sponge-associated microorganisms and also provide insight into symbiont functions. Importantly, core functions also are provided in each sponge species by analogous enzymes and biosynthetic pathways. Moreover, the abundance of elements involved in horizontal gene transfer suggests their key roles in the genomic evolution of symbionts. Our data thus demonstrate evolutionary convergence in complex symbiont communities and reveal the details and mechanisms that underpin the process.</p>
</abstract>
<kwd-group><kwd>convergent evolution</kwd>
<kwd>metagenomics</kwd>
<kwd>nitrogen metabolism</kwd>
<kwd>eukaryotic-like proteins</kwd>
</kwd-group>
<custom-meta-group><custom-meta><meta-name>author-summary</meta-name>
<meta-value><xref ref-type="other" rid="author-summary"></xref>
</meta-value>
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</front>
</pmc>
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