Bacterial DNA Sifted from the Trichoplax adhaerens (Animalia: Placozoa) Genome Project Reveals a Putative Rickettsial Endosymbiont
Identifieur interne : 000395 ( Ncbi/Merge ); précédent : 000394; suivant : 000396Bacterial DNA Sifted from the Trichoplax adhaerens (Animalia: Placozoa) Genome Project Reveals a Putative Rickettsial Endosymbiont
Auteurs : Timothy Driscoll ; Joseph J. Gillespie ; Eric K. Nordberg ; Abdu F. Azad ; Bruno W. Sobral [Suisse]Source :
- Genome Biology and Evolution [ 1759-6653 ] ; 2013.
Abstract
Eukaryotic genome sequencing projects often yield bacterial DNA sequences, data typically considered as microbial contamination. However, these sequences may also indicate either symbiont genes or lateral gene transfer (LGT) to host genomes. These bacterial sequences can provide clues about eukaryote–microbe interactions. Here, we used the genome of the primitive animal
Url:
DOI: 10.1093/gbe/evt036
PubMed: 23475938
PubMed Central: 3641634
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(Animalia: Placozoa) Genome Project Reveals a Putative Rickettsial Endosymbiont</title>
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<affiliation><nlm:aff id="evt036-AFF2">Department of Microbiology and Immunology, University of Maryland School of Medicine</nlm:aff>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Bacterial DNA Sifted from the <italic>Trichoplax adhaerens</italic>
(Animalia: Placozoa) Genome Project Reveals a Putative Rickettsial Endosymbiont</title>
<author><name sortKey="Driscoll, Timothy" sort="Driscoll, Timothy" uniqKey="Driscoll T" first="Timothy" last="Driscoll">Timothy Driscoll</name>
<affiliation><nlm:aff id="evt036-AFF1">Virginia Bioinformatics Institute at Virginia Polytechnic Institute and State University</nlm:aff>
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<author><name sortKey="Gillespie, Joseph J" sort="Gillespie, Joseph J" uniqKey="Gillespie J" first="Joseph J." last="Gillespie">Joseph J. Gillespie</name>
<affiliation><nlm:aff id="evt036-AFF1">Virginia Bioinformatics Institute at Virginia Polytechnic Institute and State University</nlm:aff>
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<affiliation><nlm:aff id="evt036-AFF2">Department of Microbiology and Immunology, University of Maryland School of Medicine</nlm:aff>
<wicri:noCountry code="subfield">University of Maryland School of Medicine</wicri:noCountry>
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<author><name sortKey="Nordberg, Eric K" sort="Nordberg, Eric K" uniqKey="Nordberg E" first="Eric K." last="Nordberg">Eric K. Nordberg</name>
<affiliation><nlm:aff id="evt036-AFF1">Virginia Bioinformatics Institute at Virginia Polytechnic Institute and State University</nlm:aff>
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<author><name sortKey="Azad, Abdu F" sort="Azad, Abdu F" uniqKey="Azad A" first="Abdu F." last="Azad">Abdu F. Azad</name>
<affiliation><nlm:aff id="evt036-AFF2">Department of Microbiology and Immunology, University of Maryland School of Medicine</nlm:aff>
<wicri:noCountry code="subfield">University of Maryland School of Medicine</wicri:noCountry>
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<author><name sortKey="Sobral, Bruno W" sort="Sobral, Bruno W" uniqKey="Sobral B" first="Bruno W." last="Sobral">Bruno W. Sobral</name>
<affiliation><nlm:aff id="evt036-AFF1">Virginia Bioinformatics Institute at Virginia Polytechnic Institute and State University</nlm:aff>
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<wicri:regionArea>Present address: Nestlé Institute of Health Sciences SA, Campus EPFL, Quartier de L'innovation, Lausanne</wicri:regionArea>
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<series><title level="j">Genome Biology and Evolution</title>
<idno type="eISSN">1759-6653</idno>
<imprint><date when="2013">2013</date>
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<front><div type="abstract" xml:lang="en"><p>Eukaryotic genome sequencing projects often yield bacterial DNA sequences, data typically considered as microbial contamination. However, these sequences may also indicate either symbiont genes or lateral gene transfer (LGT) to host genomes. These bacterial sequences can provide clues about eukaryote–microbe interactions. Here, we used the genome of the primitive animal <italic>Trichoplax adhaerens</italic>
(Metazoa: Placozoa), which is known to harbor an uncharacterized Gram-negative endosymbiont, to search for the presence of bacterial DNA sequences. Bioinformatic and phylogenomic analyses of extracted data from the genome assembly (181 bacterial coding sequences [CDS]) and trace read archive (16S rDNA) revealed a dominant proteobacterial profile strongly skewed to Rickettsiales (<italic>Alphaproteobacteria</italic>
) genomes. By way of phylogenetic analysis of 16S rDNA and 113 proteins conserved across proteobacterial genomes, as well as identification of 27 rickettsial signature genes, we propose a Rickettsiales endosymbiont of <italic>T. adhaerens</italic>
(RETA). The majority (93%) of the identified bacterial CDS belongs to small scaffolds containing prokaryotic-like genes; however, 12 CDS were identified on large scaffolds comprised of eukaryotic-like genes, suggesting that <italic>T</italic>
. <italic>adhaerens</italic>
might have recently acquired bacterial genes. These putative LGTs may coincide with the placozoan’s aquatic niche and symbiosis with RETA. This work underscores the rich, and relatively untapped, resource of eukaryotic genome projects for harboring data pertinent to host–microbial interactions. The nature of unknown (or poorly characterized) bacterial species may only emerge via analysis of host genome sequencing projects, particularly if these species are resistant to cell culturing, as are many obligate intracellular microbes. Our work provides methodological insight for such an approach.</p>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Genome Biol Evol</journal-id>
<journal-id journal-id-type="iso-abbrev">Genome Biol Evol</journal-id>
<journal-id journal-id-type="publisher-id">gbe</journal-id>
<journal-id journal-id-type="hwp">gbe</journal-id>
<journal-title-group><journal-title>Genome Biology and Evolution</journal-title>
</journal-title-group>
<issn pub-type="epub">1759-6653</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">23475938</article-id>
<article-id pub-id-type="pmc">3641634</article-id>
<article-id pub-id-type="doi">10.1093/gbe/evt036</article-id>
<article-id pub-id-type="publisher-id">evt036</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Bacterial DNA Sifted from the <italic>Trichoplax adhaerens</italic>
(Animalia: Placozoa) Genome Project Reveals a Putative Rickettsial Endosymbiont</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Driscoll</surname>
<given-names>Timothy</given-names>
</name>
<xref ref-type="aff" rid="evt036-AFF1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="evt036-FN1"><sup>†</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gillespie</surname>
<given-names>Joseph J.</given-names>
</name>
<xref ref-type="aff" rid="evt036-AFF1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="evt036-AFF2"><sup>2</sup>
</xref>
<xref ref-type="corresp" rid="evt036-COR1">*</xref>
<xref ref-type="author-notes" rid="evt036-FN1"><sup>†</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nordberg</surname>
<given-names>Eric K.</given-names>
</name>
<xref ref-type="aff" rid="evt036-AFF1"><sup>1</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Azad</surname>
<given-names>Abdu F.</given-names>
</name>
<xref ref-type="aff" rid="evt036-AFF2"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Sobral</surname>
<given-names>Bruno W.</given-names>
</name>
<xref ref-type="aff" rid="evt036-AFF1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="evt036-AFF3"><sup>3</sup>
</xref>
</contrib>
</contrib-group>
<aff id="evt036-AFF1"><sup>1</sup>
Virginia Bioinformatics Institute at Virginia Polytechnic Institute and State University</aff>
<aff id="evt036-AFF2"><sup>2</sup>
Department of Microbiology and Immunology, University of Maryland School of Medicine</aff>
<aff id="evt036-AFF3"><sup>3</sup>
Present address: Nestlé Institute of Health Sciences SA, Campus EPFL, Quartier de L'innovation, Lausanne, Switzerland</aff>
<author-notes><corresp id="evt036-COR1">*Corresponding author: E-mail: <email>jgille@vbi.vt.edu</email>
.</corresp>
<fn id="evt036-FN1"><p><sup>†</sup>
These authors contributed equally to this work.</p>
</fn>
<fn id="evt036-FN2"><p><bold>Associate editor:</bold>
Shu-Miaw Chaw</p>
</fn>
</author-notes>
<pub-date pub-type="ppub"><year>2013</year>
</pub-date>
<pub-date pub-type="epub"><day>7</day>
<month>3</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="collection"><month>4</month>
<year>2013</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>7</day>
<month>3</month>
<year>2013</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
. </pmc-comment>
<volume>5</volume>
<issue>4</issue>
<fpage>621</fpage>
<lpage>645</lpage>
<history><date date-type="accepted"><day>1</day>
<month>3</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s) 2013. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.</copyright-statement>
<copyright-year>2013</copyright-year>
<license license-type="creative-commons" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/"><license-p><pmc-comment>CREATIVE COMMONS</pmc-comment>
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/">http://creativecommons.org/licenses/by-nc/3.0/</ext-link>
), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<abstract><p>Eukaryotic genome sequencing projects often yield bacterial DNA sequences, data typically considered as microbial contamination. However, these sequences may also indicate either symbiont genes or lateral gene transfer (LGT) to host genomes. These bacterial sequences can provide clues about eukaryote–microbe interactions. Here, we used the genome of the primitive animal <italic>Trichoplax adhaerens</italic>
(Metazoa: Placozoa), which is known to harbor an uncharacterized Gram-negative endosymbiont, to search for the presence of bacterial DNA sequences. Bioinformatic and phylogenomic analyses of extracted data from the genome assembly (181 bacterial coding sequences [CDS]) and trace read archive (16S rDNA) revealed a dominant proteobacterial profile strongly skewed to Rickettsiales (<italic>Alphaproteobacteria</italic>
) genomes. By way of phylogenetic analysis of 16S rDNA and 113 proteins conserved across proteobacterial genomes, as well as identification of 27 rickettsial signature genes, we propose a Rickettsiales endosymbiont of <italic>T. adhaerens</italic>
(RETA). The majority (93%) of the identified bacterial CDS belongs to small scaffolds containing prokaryotic-like genes; however, 12 CDS were identified on large scaffolds comprised of eukaryotic-like genes, suggesting that <italic>T</italic>
. <italic>adhaerens</italic>
might have recently acquired bacterial genes. These putative LGTs may coincide with the placozoan’s aquatic niche and symbiosis with RETA. This work underscores the rich, and relatively untapped, resource of eukaryotic genome projects for harboring data pertinent to host–microbial interactions. The nature of unknown (or poorly characterized) bacterial species may only emerge via analysis of host genome sequencing projects, particularly if these species are resistant to cell culturing, as are many obligate intracellular microbes. Our work provides methodological insight for such an approach.</p>
</abstract>
<kwd-group><kwd>endosymbiont, genome-mining, host–microbe interactions, intracellular bacteria, Rickettsiales, symbiosis</kwd>
</kwd-group>
<counts><page-count count="25"></page-count>
</counts>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>Suisse</li>
</country>
<region><li>Canton de Vaud</li>
</region>
<settlement><li>Lausanne</li>
</settlement>
</list>
<tree><noCountry><name sortKey="Azad, Abdu F" sort="Azad, Abdu F" uniqKey="Azad A" first="Abdu F." last="Azad">Abdu F. Azad</name>
<name sortKey="Driscoll, Timothy" sort="Driscoll, Timothy" uniqKey="Driscoll T" first="Timothy" last="Driscoll">Timothy Driscoll</name>
<name sortKey="Gillespie, Joseph J" sort="Gillespie, Joseph J" uniqKey="Gillespie J" first="Joseph J." last="Gillespie">Joseph J. Gillespie</name>
<name sortKey="Nordberg, Eric K" sort="Nordberg, Eric K" uniqKey="Nordberg E" first="Eric K." last="Nordberg">Eric K. Nordberg</name>
</noCountry>
<country name="Suisse"><region name="Canton de Vaud"><name sortKey="Sobral, Bruno W" sort="Sobral, Bruno W" uniqKey="Sobral B" first="Bruno W." last="Sobral">Bruno W. Sobral</name>
</region>
</country>
</tree>
</affiliations>
</record>
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