Provirophages in the Bigelowiella genome bear testimony to past encounters with giant viruses
Identifieur interne : 000074 ( Pmc/Checkpoint ); précédent : 000073; suivant : 000075Provirophages in the Bigelowiella genome bear testimony to past encounters with giant viruses
Auteurs : Guillaume Blanc [France] ; Lucie Gallot-Lavallée [France] ; Florian Maumus [France]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2015.
Abstract
Virophages are viruses that hijack the replication machinery of giant viruses for their own replication. Virophages negatively impact giant virus replication and improve the survival chances of eukaryotic cells infected by giant viruses. In this study, we identified segments of the
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DOI: 10.1073/pnas.1506469112
PubMed: 26305943
PubMed Central: 4586850
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Provirophages in the Bigelowiella genome bear testimony to past encounters with giant viruses</title><author><name sortKey="Blanc, Guillaume" sort="Blanc, Guillaume" uniqKey="Blanc G" first="Guillaume" last="Blanc">Guillaume Blanc</name><affiliation wicri:level="1"><nlm:aff id="aff1">Laboratoire Information Génomique et Structurale, UMR7256 (Institut de Microbiologie de la Méditerranée FR3479) CNRS,<institution>Aix-Marseille Université</institution>, 13288 Marseille cedex 9,<country>France</country>;</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Gallot Lavallee, Lucie" sort="Gallot Lavallee, Lucie" uniqKey="Gallot Lavallee L" first="Lucie" last="Gallot-Lavallée">Lucie Gallot-Lavallée</name><affiliation wicri:level="1"><nlm:aff id="aff1">Laboratoire Information Génomique et Structurale, UMR7256 (Institut de Microbiologie de la Méditerranée FR3479) CNRS,<institution>Aix-Marseille Université</institution>, 13288 Marseille cedex 9,<country>France</country>;</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Maumus, Florian" sort="Maumus, Florian" uniqKey="Maumus F" first="Florian" last="Maumus">Florian Maumus</name><affiliation wicri:level="1"><nlm:aff id="aff2">INRA, UR1164 Unité de Recherche Génomique-Info,<institution>Institut National de la Recherche Agronomique de Versailles-Grignon</institution>, 78026 Versailles,<country>France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26305943</idno><idno type="pmc">4586850</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4586850</idno><idno type="RBID">PMC:4586850</idno><idno type="doi">10.1073/pnas.1506469112</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000047</idno><idno type="wicri:Area/Pmc/Curation">000047</idno><idno type="wicri:Area/Pmc/Checkpoint">000074</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Provirophages in the Bigelowiella genome bear testimony to past encounters with giant viruses</title><author><name sortKey="Blanc, Guillaume" sort="Blanc, Guillaume" uniqKey="Blanc G" first="Guillaume" last="Blanc">Guillaume Blanc</name><affiliation wicri:level="1"><nlm:aff id="aff1">Laboratoire Information Génomique et Structurale, UMR7256 (Institut de Microbiologie de la Méditerranée FR3479) CNRS,<institution>Aix-Marseille Université</institution>, 13288 Marseille cedex 9,<country>France</country>;</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Gallot Lavallee, Lucie" sort="Gallot Lavallee, Lucie" uniqKey="Gallot Lavallee L" first="Lucie" last="Gallot-Lavallée">Lucie Gallot-Lavallée</name><affiliation wicri:level="1"><nlm:aff id="aff1">Laboratoire Information Génomique et Structurale, UMR7256 (Institut de Microbiologie de la Méditerranée FR3479) CNRS,<institution>Aix-Marseille Université</institution>, 13288 Marseille cedex 9,<country>France</country>;</nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Maumus, Florian" sort="Maumus, Florian" uniqKey="Maumus F" first="Florian" last="Maumus">Florian Maumus</name><affiliation wicri:level="1"><nlm:aff id="aff2">INRA, UR1164 Unité de Recherche Génomique-Info,<institution>Institut National de la Recherche Agronomique de Versailles-Grignon</institution>, 78026 Versailles,<country>France</country></nlm:aff><country xml:lang="fr">France</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Virophages are viruses that hijack the replication machinery of giant viruses for their own replication. Virophages negatively impact giant virus replication and improve the survival chances of eukaryotic cells infected by giant viruses. In this study, we identified segments of the <italic>Bigelowiella natans</italic> genome that originate from virophages and giant viruses, revealing genomic footprints of battles between these viral entities that occurred in this unicellular alga. Interestingly, genes of virophage origin are transcribed, suggesting that they are functional. We hypothesize that virophage integration may be beneficial to both the virophage and <italic>B. natans</italic> by increasing the chances for the virophage to coinfect the cell with a giant virus prey and by defending the host cell against fatal giant virus infections.</p></div></front></TEI><pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<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><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26305943</article-id><article-id pub-id-type="pmc">4586850</article-id><article-id pub-id-type="publisher-id">201506469</article-id><article-id pub-id-type="doi">10.1073/pnas.1506469112</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><series-title>From the Cover</series-title></article-categories><title-group><article-title>Provirophages in the Bigelowiella genome bear testimony to past encounters with giant viruses</article-title><alt-title alt-title-type="short">Viral battle vestiges in algal genome</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Blanc</surname><given-names>Guillaume</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gallot-Lavallée</surname><given-names>Lucie</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Maumus</surname><given-names>Florian</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1"><sup>2</sup></xref></contrib><aff id="aff1"><sup>a</sup>Laboratoire Information Génomique et Structurale, UMR7256 (Institut de Microbiologie de la Méditerranée FR3479) CNRS,<institution>Aix-Marseille Université</institution>, 13288 Marseille cedex 9,<country>France</country>;</aff><aff id="aff2"><sup>b</sup>INRA, UR1164 Unité de Recherche Génomique-Info,<institution>Institut National de la Recherche Agronomique de Versailles-Grignon</institution>, 78026 Versailles,<country>France</country></aff></contrib-group><author-notes><corresp id="cor1"><sup>2</sup>To whom correspondence may be addressed. Email: <email>guillaume.blanc@igs.cnrs-mrs.fr</email> or <email>fmaumus@versailles.inra.fr</email>.</corresp><fn fn-type="edited-by"><p>Edited by Peter Palese, Icahn School of Medicine at Mount Sinai, New York, NY, and approved July 24, 2015 (received for review April 1, 2015)</p></fn><fn fn-type="con"><p>Author contributions: G.B. and F.M. designed research; G.B., L.G.-L., and F.M. performed research; G.B., L.G.-L., and F.M. analyzed data; and G.B. and F.M. wrote the paper.</p></fn><fn fn-type="equal" id="fn1"><p><sup>1</sup>G.B. and F.M. contributed equally to this work.</p></fn></author-notes><pub-date pub-type="ppub"><day>22</day><month>9</month><year>2015</year></pub-date><pub-date pub-type="epub"><day>24</day><month>8</month><year>2015</year></pub-date><volume>112</volume><issue>38</issue><fpage>E5318</fpage><lpage>E5326</lpage><self-uri xlink:title="pdf" xlink:href="pnas.201506469.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Virophages are viruses that hijack the replication machinery of giant viruses for their own replication. Virophages negatively impact giant virus replication and improve the survival chances of eukaryotic cells infected by giant viruses. In this study, we identified segments of the <italic>Bigelowiella natans</italic> genome that originate from virophages and giant viruses, revealing genomic footprints of battles between these viral entities that occurred in this unicellular alga. Interestingly, genes of virophage origin are transcribed, suggesting that they are functional. We hypothesize that virophage integration may be beneficial to both the virophage and <italic>B. natans</italic> by increasing the chances for the virophage to coinfect the cell with a giant virus prey and by defending the host cell against fatal giant virus infections.</p></abstract><abstract><p>Virophages are recently discovered double-stranded DNA virus satellites that prey on giant viruses (nucleocytoplasmic large DNA viruses; NCLDVs), which are themselves parasites of unicellular eukaryotes. This coupled parasitism can result in the indirect control of eukaryotic cell mortality by virophages. However, the details of such tripartite relationships remain largely unexplored. We have discovered ∼300 predicted genes of putative virophage origin in the nuclear genome of the unicellular alga <italic>Bigelowiella natans</italic>. Physical clustering of these genes indicates that virophage genomes are integrated into the <italic>B. natans</italic> genome. Virophage inserts show high levels of similarity and synteny between each other, indicating that they are closely related. Virophage genes are transcribed not only in the sequenced <italic>B. natans</italic> strain but also in other <italic>Bigelowiella</italic> isolates, suggesting that transcriptionally active virophage inserts are widespread in <italic>Bigelowiella</italic> populations. Evidence that <italic>B. natans</italic> is also a host to NCLDV members is provided by the identification of NCLDV inserts in its genome. These putative large DNA viruses may be infected by <italic>B. natans</italic> virophages. We also identify four repeated elements sharing structural and genetic similarities with transpovirons—a class of mobile elements first discovered in giant viruses—that were probably independently inserted in the <italic>B. natans</italic> genome. We argue that endogenized provirophages may be beneficial to both the virophage and <italic>B. natans</italic> by (<italic>i</italic>) increasing the chances for the virophage to coinfect the host cell with an NCLDV prey and (<italic>ii</italic>) defending the host cell against fatal NCLDV infections.</p></abstract><kwd-group><kwd>virophage</kwd><kwd>nucleocytoplasmic large DNA virus</kwd><kwd>microbial community</kwd><kwd>endogenous virus</kwd><kwd>Maverick/polinton</kwd></kwd-group><counts><page-count count="9"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>France</li></country></list><tree><country name="France"><noRegion><name sortKey="Blanc, Guillaume" sort="Blanc, Guillaume" uniqKey="Blanc G" first="Guillaume" last="Blanc">Guillaume Blanc</name></noRegion><name sortKey="Gallot Lavallee, Lucie" sort="Gallot Lavallee, Lucie" uniqKey="Gallot Lavallee L" first="Lucie" last="Gallot-Lavallée">Lucie Gallot-Lavallée</name><name sortKey="Maumus, Florian" sort="Maumus, Florian" uniqKey="Maumus F" first="Florian" last="Maumus">Florian Maumus</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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