Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins
Identifieur interne : 002B91 ( Pmc/Curation ); précédent : 002B90; suivant : 002B92Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins
Auteurs : Koenraad Van Doorslaer [États-Unis] ; Valeria Ruoppolo [Brésil] ; Annie Schmidt [États-Unis] ; Amelie Lescroël [États-Unis, France] ; Dennis Jongsomjit [États-Unis] ; Megan Elrod [États-Unis] ; Simona Kraberger [États-Unis] ; Daisy Stainton [Australie] ; Katie M. Dugger [États-Unis] ; Grant Ballard [États-Unis] ; David G. Ainley [États-Unis] ; Arvind Varsani [États-Unis, Afrique du Sud]Source :
- Virus Evolution [ 2057-1577 ] ; 2017.
Abstract
The family
Url:
DOI: 10.1093/ve/vex027
PubMed: 29026649
PubMed Central: 5632515
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<author><name sortKey="Elrod, Megan" sort="Elrod, Megan" uniqKey="Elrod M" first="Megan" last="Elrod">Megan Elrod</name>
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<author><name sortKey="Kraberger, Simona" sort="Kraberger, Simona" uniqKey="Kraberger S" first="Simona" last="Kraberger">Simona Kraberger</name>
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<author><name sortKey="Varsani, Arvind" sort="Varsani, Arvind" uniqKey="Varsani A" first="Arvind" last="Varsani">Arvind Varsani</name>
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<country xml:lang="fr">États-Unis</country>
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<series><title level="j">Virus Evolution</title>
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<front><div type="abstract" xml:lang="en"><title>Abstract</title>
<p>The family <italic>Papillomaviridae</italic>
contains more than 320 papillomavirus types, with most having been identified as infecting skin and mucosal epithelium in mammalian hosts. To date, only nine non-mammalian papillomaviruses have been described from birds (<italic>n</italic>
= 5), a fish (<italic>n</italic>
= 1), a snake (<italic>n</italic>
= 1), and turtles (<italic>n</italic>
= 2). The identification of papillomaviruses in sauropsids and a sparid fish suggests that early ancestors of papillomaviruses were already infecting the earliest Euteleostomi. The Euteleostomi clade includes more than 90 per cent of the living vertebrate species, and progeny virus could have been passed on to all members of this clade, inhabiting virtually every habitat on the planet. As part of this study, we isolated a novel papillomavirus from a 16-year-old female Adélie penguin (<italic>Pygoscelis adeliae</italic>
) from Cape Crozier, Ross Island (Antarctica). The new papillomavirus shares ∼64 per cent genome-wide identity to a previously described Adélie penguin papillomavirus. Phylogenetic analyses show that the non-mammalian viruses (expect the python, <italic>Morelia spilota</italic>
, associated papillomavirus) cluster near the base of the papillomavirus evolutionary tree. A papillomavirus isolated from an avian host (Northern fulmar; <italic>Fulmarus glacialis</italic>
), like the two turtle papillomaviruses, lacks a putative E9 protein that is found in all other avian papillomaviruses. Furthermore, the Northern fulmar papillomavirus has an E7 more similar to the mammalian viruses than the other avian papillomaviruses. Typical E6 proteins of mammalian papillomaviruses have two Zinc finger motifs, whereas the sauropsid papillomaviruses only have one such motif. Furthermore, this motif is absent in the fish papillomavirus. Thus, it is highly likely that the most recent common ancestor of the mammalian and sauropsid papillomaviruses had a single motif E6. It appears that a motif duplication resulted in mammalian papillomaviruses having a double Zinc finger motif in E6. We estimated the divergence time between Northern fulmar-associated papillomavirus and the other Sauropsid papillomaviruses be to around 250 million years ago, during the Paleozoic-Mesozoic transition and our analysis dates the root of the papillomavirus tree between 400 and 600 million years ago. Our analysis shows evidence for niche adaptation and that these non-mammalian viruses have highly divergent E6 and E7 proteins, providing insights into the evolution of the early viral (onco-)proteins.</p>
</div>
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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">Virus Evol</journal-id>
<journal-id journal-id-type="iso-abbrev">Virus Evol</journal-id>
<journal-id journal-id-type="publisher-id">vevolu</journal-id>
<journal-title-group><journal-title>Virus Evolution</journal-title>
</journal-title-group>
<issn pub-type="epub">2057-1577</issn>
<publisher><publisher-name>Oxford University Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">29026649</article-id>
<article-id pub-id-type="pmc">5632515</article-id>
<article-id pub-id-type="doi">10.1093/ve/vex027</article-id>
<article-id pub-id-type="publisher-id">vex027</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0002-2985-0733</contrib-id>
<name><surname>Van Doorslaer</surname>
<given-names>Koenraad</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff1">1</xref>
<xref ref-type="corresp" rid="vex027-cor1"></xref>
<xref ref-type="author-notes" rid="vex027-FM1"></xref>
<pmc-comment>vandoorslaer@email.arizona.edu </pmc-comment>
</contrib>
<contrib contrib-type="author"><name><surname>Ruoppolo</surname>
<given-names>Valeria</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Schmidt</surname>
<given-names>Annie</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lescroël</surname>
<given-names>Amelie</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff3">3</xref>
<xref ref-type="aff" rid="vex027-aff4">4</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Jongsomjit</surname>
<given-names>Dennis</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Elrod</surname>
<given-names>Megan</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kraberger</surname>
<given-names>Simona</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff5">5</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Stainton</surname>
<given-names>Daisy</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff6">6</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Dugger</surname>
<given-names>Katie M</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff7">7</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ballard</surname>
<given-names>Grant</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff3">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ainley</surname>
<given-names>David G</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff8">8</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="false">http://orcid.org/0000-0003-4111-2415</contrib-id>
<name><surname>Varsani</surname>
<given-names>Arvind</given-names>
</name>
<xref ref-type="aff" rid="vex027-aff5">5</xref>
<xref ref-type="aff" rid="vex027-aff9">9</xref>
<xref ref-type="corresp" rid="vex027-cor1"></xref>
<xref ref-type="author-notes" rid="vex027-FM2"></xref>
<pmc-comment>vandoorslaer@email.arizona.edu </pmc-comment>
</contrib>
</contrib-group>
<aff id="vex027-aff1"><label>1</label>
ACBS and Bio5, University of Arizona, 1657 E Helen St, Tucson, AZ 85721, USA</aff>
<aff id="vex027-aff2"><label>2</label>
Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, Brazil</aff>
<aff id="vex027-aff3"><label>3</label>
Point Blue Conservation Science, Petaluma, CA 94954, USA</aff>
<aff id="vex027-aff4"><label>4</label>
Centre d'Ecologie Fonctionnelle et Evolutive – CNRS, UMR 5175, Montpellier, France</aff>
<aff id="vex027-aff5"><label>5</label>
The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life sciences, Arizona State University, Tempe, AZ 85287, USA</aff>
<aff id="vex027-aff6"><label>6</label>
School of Biological Sciences, The University of Queensland, Brisbane, QLD, Australia</aff>
<aff id="vex027-aff7"><label>7</label>
U.S. Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit, Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR 97331, USA</aff>
<aff id="vex027-aff8"><label>8</label>
HT Harvey and Associates, Los Gatos, CA 95032, USA</aff>
<aff id="vex027-aff9"><label>9</label>
Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Observatory, Cape Town, 7925, South Africa</aff>
<author-notes><corresp id="vex027-cor1"><label>*</label>
Corresponding authors: E-mails: <email>vandoorslaer@email.arizona.edu</email>
and <email>arvind.varsani@asu.edu</email>
</corresp>
<fn id="vex027-FM1"><label>†</label>
<p><ext-link ext-link-type="uri" xlink:href="http://orcid.org/0000-0002-2985-0733">http://orcid.org/0000-0002-2985-0733</ext-link>
</p>
</fn>
<fn id="vex027-FM2"><label>‡</label>
<p><ext-link ext-link-type="uri" xlink:href="http://orcid.org/0000-0003-4111-2415">http://orcid.org/0000-0003-4111-2415</ext-link>
</p>
</fn>
</author-notes>
<pub-date pub-type="collection"><month>7</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="epub" iso-8601-date="2017-10-06"><day>06</day>
<month>10</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>06</day>
<month>10</month>
<year>2017</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on the . </pmc-comment>
<volume>3</volume>
<issue>2</issue>
<elocation-id>vex027</elocation-id>
<permissions><copyright-statement>© The Author 2017. Published by Oxford University Press.</copyright-statement>
<copyright-year>2017</copyright-year>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/" license-type="cc-by"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution 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 reuse, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p>
</license>
</permissions>
<self-uri xlink:href="vex027.pdf"></self-uri>
<abstract><title>Abstract</title>
<p>The family <italic>Papillomaviridae</italic>
contains more than 320 papillomavirus types, with most having been identified as infecting skin and mucosal epithelium in mammalian hosts. To date, only nine non-mammalian papillomaviruses have been described from birds (<italic>n</italic>
= 5), a fish (<italic>n</italic>
= 1), a snake (<italic>n</italic>
= 1), and turtles (<italic>n</italic>
= 2). The identification of papillomaviruses in sauropsids and a sparid fish suggests that early ancestors of papillomaviruses were already infecting the earliest Euteleostomi. The Euteleostomi clade includes more than 90 per cent of the living vertebrate species, and progeny virus could have been passed on to all members of this clade, inhabiting virtually every habitat on the planet. As part of this study, we isolated a novel papillomavirus from a 16-year-old female Adélie penguin (<italic>Pygoscelis adeliae</italic>
) from Cape Crozier, Ross Island (Antarctica). The new papillomavirus shares ∼64 per cent genome-wide identity to a previously described Adélie penguin papillomavirus. Phylogenetic analyses show that the non-mammalian viruses (expect the python, <italic>Morelia spilota</italic>
, associated papillomavirus) cluster near the base of the papillomavirus evolutionary tree. A papillomavirus isolated from an avian host (Northern fulmar; <italic>Fulmarus glacialis</italic>
), like the two turtle papillomaviruses, lacks a putative E9 protein that is found in all other avian papillomaviruses. Furthermore, the Northern fulmar papillomavirus has an E7 more similar to the mammalian viruses than the other avian papillomaviruses. Typical E6 proteins of mammalian papillomaviruses have two Zinc finger motifs, whereas the sauropsid papillomaviruses only have one such motif. Furthermore, this motif is absent in the fish papillomavirus. Thus, it is highly likely that the most recent common ancestor of the mammalian and sauropsid papillomaviruses had a single motif E6. It appears that a motif duplication resulted in mammalian papillomaviruses having a double Zinc finger motif in E6. We estimated the divergence time between Northern fulmar-associated papillomavirus and the other Sauropsid papillomaviruses be to around 250 million years ago, during the Paleozoic-Mesozoic transition and our analysis dates the root of the papillomavirus tree between 400 and 600 million years ago. Our analysis shows evidence for niche adaptation and that these non-mammalian viruses have highly divergent E6 and E7 proteins, providing insights into the evolution of the early viral (onco-)proteins.</p>
</abstract>
<kwd-group><kwd>papillomavirus</kwd>
<kwd>evolution</kwd>
<kwd>bird</kwd>
<kwd>reptile</kwd>
<kwd>avian</kwd>
</kwd-group>
<funding-group><award-group award-type="grant"><funding-source><named-content content-type="funder-name">Cooperative State Research, Education, and Extension Service</named-content>
<named-content content-type="funder-identifier">10.13039/100007014</named-content>
</funding-source>
<award-id>NC229</award-id>
</award-group>
<award-group award-type="grant"><funding-source><named-content content-type="funder-name">National Science Foundation</named-content>
<named-content content-type="funder-identifier">10.13039/100000001</named-content>
</funding-source>
<award-id>ANT-0944411</award-id>
</award-group>
</funding-group>
<counts><page-count count="12"></page-count>
</counts>
</article-meta>
</front>
</pmc>
</record>
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