A novel group of diverse Polinton-like viruses discovered by metagenome analysis
Identifieur interne : 000686 ( Ncbi/Merge ); précédent : 000685; suivant : 000687A novel group of diverse Polinton-like viruses discovered by metagenome analysis
Auteurs : Natalya Yutin [États-Unis] ; Sofiya Shevchenko [États-Unis] ; Vladimir Kapitonov [États-Unis] ; Mart Krupovic [France] ; Eugene V. Koonin [États-Unis]Source :
- BMC Biology [ 1741-7007 ] ; 2015.
Abstract
The rapidly growing metagenomic databases provide increasing opportunities for computational discovery of new groups of organisms. Identification of new viruses is particularly straightforward given the comparatively small size of viral genomes, although fast evolution of viruses complicates the analysis of novel sequences. Here we report the metagenomic discovery of a distinct group of diverse viruses that are distantly related to the eukaryotic virus-like transposons of the Polinton superfamily.
The sequence of the putative major capsid protein (MCP) of the unusual linear virophage associated with
The discovery of PLV substantially expands the emerging class of eukaryotic viruses and transposons that also includes Polintons and virophages. This class of selfish elements is extremely widespread and might have been a hotbed of eukaryotic virus, transposon and plasmid evolution. New families of these elements are expected to be discovered.
The online version of this article (doi:10.1186/s12915-015-0207-4) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1186/s12915-015-0207-4
PubMed: 26560305
PubMed Central: 4642659
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A novel group of diverse Polinton-like viruses discovered by metagenome analysis</title>
<author><name sortKey="Yutin, Natalya" sort="Yutin, Natalya" uniqKey="Yutin N" first="Natalya" last="Yutin">Natalya Yutin</name>
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<author><name sortKey="Koonin, Eugene V" sort="Koonin, Eugene V" uniqKey="Koonin E" first="Eugene V." last="Koonin">Eugene V. Koonin</name>
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<front><div type="abstract" xml:lang="en"><sec><title>Background</title>
<p>The rapidly growing metagenomic databases provide increasing opportunities for computational discovery of new groups of organisms. Identification of new viruses is particularly straightforward given the comparatively small size of viral genomes, although fast evolution of viruses complicates the analysis of novel sequences. Here we report the metagenomic discovery of a distinct group of diverse viruses that are distantly related to the eukaryotic virus-like transposons of the Polinton superfamily.</p>
</sec>
<sec><title>Results</title>
<p>The sequence of the putative major capsid protein (MCP) of the unusual linear virophage associated with <italic>Phaeocystis globosa</italic>
virus (PgVV) was used as a bait to identify potential related viruses in metagenomic databases. Assembly of the contigs encoding the PgVV MCP homologs followed by comprehensive sequence analysis of the proteins encoded in these contigs resulted in the identification of a large group of Polinton-like viruses (PLV) that resemble Polintons (polintoviruses) and virophages in genome size, and share with them a conserved minimal morphogenetic module that consists of major and minor capsid proteins and the packaging ATPase. With a single exception, the PLV lack the retrovirus-type integrase that is encoded in the genomes of all Polintons and the Mavirus group of virophages. However, some PLV encode a newly identified tyrosine recombinase-integrase that is common in bacteria and bacteriophages and is also found in the Organic Lake virophage group. Although several PLV genomes and individual genes are integrated into algal genomes, it appears likely that most of the PLV are viruses. Given the absence of protease and retrovirus-type integrase, the PLV could resemble the ancestral polintoviruses that evolved from bacterial tectiviruses. Apart from the conserved minimal morphogenetic module, the PLV widely differ in their genome complements but share a gene network with Polintons and virophages, suggestive of multiple gene exchanges within a shared gene pool.</p>
</sec>
<sec><title>Conclusions</title>
<p>The discovery of PLV substantially expands the emerging class of eukaryotic viruses and transposons that also includes Polintons and virophages. This class of selfish elements is extremely widespread and might have been a hotbed of eukaryotic virus, transposon and plasmid evolution. New families of these elements are expected to be discovered.</p>
</sec>
<sec><title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12915-015-0207-4) contains supplementary material, which is available to authorized users.</p>
</sec>
</div>
</front>
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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">BMC Biol</journal-id>
<journal-id journal-id-type="iso-abbrev">BMC Biol</journal-id>
<journal-title-group><journal-title>BMC Biology</journal-title>
</journal-title-group>
<issn pub-type="epub">1741-7007</issn>
<publisher><publisher-name>BioMed Central</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26560305</article-id>
<article-id pub-id-type="pmc">4642659</article-id>
<article-id pub-id-type="publisher-id">207</article-id>
<article-id pub-id-type="doi">10.1186/s12915-015-0207-4</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>A novel group of diverse Polinton-like viruses discovered by metagenome analysis</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Yutin</surname>
<given-names>Natalya</given-names>
</name>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Shevchenko</surname>
<given-names>Sofiya</given-names>
</name>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kapitonov</surname>
<given-names>Vladimir</given-names>
</name>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Krupovic</surname>
<given-names>Mart</given-names>
</name>
<xref ref-type="aff" rid="Aff2"></xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Koonin</surname>
<given-names>Eugene V.</given-names>
</name>
<address><email>koonin@ncbi.nlm.nih.gov</email>
</address>
<xref ref-type="aff" rid="Aff1"></xref>
</contrib>
<aff id="Aff1"><label></label>
National Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894 USA</aff>
<aff id="Aff2"><label></label>
Unité Biologie Moléculaire du Gène chez les Extrêmophiles, Department of Microbiology, Institut Pasteur, Paris, France</aff>
</contrib-group>
<pub-date pub-type="epub"><day>11</day>
<month>11</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>11</day>
<month>11</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><year>2015</year>
</pub-date>
<volume>13</volume>
<elocation-id>95</elocation-id>
<history><date date-type="received"><day>14</day>
<month>8</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>28</day>
<month>10</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>© Yutin et al. 2015</copyright-statement>
<license license-type="OpenAccess"><license-p><bold>Open Access</bold>
This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/publicdomain/zero/1.0/">http://creativecommons.org/publicdomain/zero/1.0/</ext-link>
) applies to the data made available in this article, unless otherwise stated.</license-p>
</license>
</permissions>
<abstract id="Abs1"><sec><title>Background</title>
<p>The rapidly growing metagenomic databases provide increasing opportunities for computational discovery of new groups of organisms. Identification of new viruses is particularly straightforward given the comparatively small size of viral genomes, although fast evolution of viruses complicates the analysis of novel sequences. Here we report the metagenomic discovery of a distinct group of diverse viruses that are distantly related to the eukaryotic virus-like transposons of the Polinton superfamily.</p>
</sec>
<sec><title>Results</title>
<p>The sequence of the putative major capsid protein (MCP) of the unusual linear virophage associated with <italic>Phaeocystis globosa</italic>
virus (PgVV) was used as a bait to identify potential related viruses in metagenomic databases. Assembly of the contigs encoding the PgVV MCP homologs followed by comprehensive sequence analysis of the proteins encoded in these contigs resulted in the identification of a large group of Polinton-like viruses (PLV) that resemble Polintons (polintoviruses) and virophages in genome size, and share with them a conserved minimal morphogenetic module that consists of major and minor capsid proteins and the packaging ATPase. With a single exception, the PLV lack the retrovirus-type integrase that is encoded in the genomes of all Polintons and the Mavirus group of virophages. However, some PLV encode a newly identified tyrosine recombinase-integrase that is common in bacteria and bacteriophages and is also found in the Organic Lake virophage group. Although several PLV genomes and individual genes are integrated into algal genomes, it appears likely that most of the PLV are viruses. Given the absence of protease and retrovirus-type integrase, the PLV could resemble the ancestral polintoviruses that evolved from bacterial tectiviruses. Apart from the conserved minimal morphogenetic module, the PLV widely differ in their genome complements but share a gene network with Polintons and virophages, suggestive of multiple gene exchanges within a shared gene pool.</p>
</sec>
<sec><title>Conclusions</title>
<p>The discovery of PLV substantially expands the emerging class of eukaryotic viruses and transposons that also includes Polintons and virophages. This class of selfish elements is extremely widespread and might have been a hotbed of eukaryotic virus, transposon and plasmid evolution. New families of these elements are expected to be discovered.</p>
</sec>
<sec><title>Electronic supplementary material</title>
<p>The online version of this article (doi:10.1186/s12915-015-0207-4) contains supplementary material, which is available to authorized users.</p>
</sec>
</abstract>
<custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2015</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
<affiliations><list><country><li>France</li>
<li>États-Unis</li>
</country>
<region><li>Maryland</li>
</region>
<settlement><li>Paris</li>
</settlement>
</list>
<tree><country name="États-Unis"><region name="Maryland"><name sortKey="Yutin, Natalya" sort="Yutin, Natalya" uniqKey="Yutin N" first="Natalya" last="Yutin">Natalya Yutin</name>
</region>
<name sortKey="Kapitonov, Vladimir" sort="Kapitonov, Vladimir" uniqKey="Kapitonov V" first="Vladimir" last="Kapitonov">Vladimir Kapitonov</name>
<name sortKey="Koonin, Eugene V" sort="Koonin, Eugene V" uniqKey="Koonin E" first="Eugene V." last="Koonin">Eugene V. Koonin</name>
<name sortKey="Shevchenko, Sofiya" sort="Shevchenko, Sofiya" uniqKey="Shevchenko S" first="Sofiya" last="Shevchenko">Sofiya Shevchenko</name>
</country>
<country name="France"><noRegion><name sortKey="Krupovic, Mart" sort="Krupovic, Mart" uniqKey="Krupovic M" first="Mart" last="Krupovic">Mart Krupovic</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>
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