Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins.
Identifieur interne : 000377 ( PubMed/Curation ); précédent : 000376; suivant : 000378Unique 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] ; 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]Source :
- Virus evolution [ 2057-1577 ] ; 2017.
Abstract
The family Papillomaviridae 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 (n = 5), a fish (n = 1), a snake (n = 1), and turtles (n = 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 (Pygoscelis adeliae) 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, Morelia spilota, associated papillomavirus) cluster near the base of the papillomavirus evolutionary tree. A papillomavirus isolated from an avian host (Northern fulmar; Fulmarus glacialis), 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.
DOI: 10.1093/ve/vex027
PubMed: 29026649
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xml:lang="fr">États-Unis</country><wicri:regionArea>ACBS and Bio5, University of Arizona, 1657 E Helen St, Tucson, AZ 85721</wicri:regionArea></affiliation></author><author><name sortKey="Ruoppolo, Valeria" sort="Ruoppolo, Valeria" uniqKey="Ruoppolo V" first="Valeria" last="Ruoppolo">Valeria Ruoppolo</name><affiliation wicri:level="1"><nlm:affiliation>Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo</wicri:regionArea></affiliation></author><author><name sortKey="Schmidt, Annie" sort="Schmidt, Annie" uniqKey="Schmidt A" first="Annie" last="Schmidt">Annie Schmidt</name><affiliation wicri:level="1"><nlm:affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Point Blue Conservation Science, Petaluma, CA 94954</wicri:regionArea></affiliation></author><author><name sortKey="Lescroel, Amelie" sort="Lescroel, Amelie" uniqKey="Lescroel A" first="Amelie" last="Lescroël">Amelie Lescroël</name><affiliation wicri:level="1"><nlm:affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Point Blue Conservation Science, Petaluma, CA 94954</wicri:regionArea></affiliation></author><author><name sortKey="Jongsomjit, Dennis" sort="Jongsomjit, Dennis" uniqKey="Jongsomjit D" first="Dennis" last="Jongsomjit">Dennis Jongsomjit</name><affiliation wicri:level="1"><nlm:affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Point Blue Conservation Science, Petaluma, CA 94954</wicri:regionArea></affiliation></author><author><name sortKey="Elrod, Megan" sort="Elrod, Megan" uniqKey="Elrod M" first="Megan" last="Elrod">Megan Elrod</name><affiliation wicri:level="1"><nlm:affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Point Blue Conservation Science, Petaluma, CA 94954</wicri:regionArea></affiliation></author><author><name sortKey="Kraberger, Simona" sort="Kraberger, Simona" uniqKey="Kraberger S" first="Simona" last="Kraberger">Simona Kraberger</name><affiliation wicri:level="1"><nlm:affiliation>The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life sciences, Arizona State University, Tempe, AZ 85287, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life sciences, Arizona State University, Tempe, AZ 85287</wicri:regionArea></affiliation></author><author><name sortKey="Stainton, Daisy" sort="Stainton, Daisy" uniqKey="Stainton D" first="Daisy" last="Stainton">Daisy Stainton</name><affiliation wicri:level="1"><nlm:affiliation>School of Biological Sciences, The University of Queensland, Brisbane, QLD, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>School of Biological Sciences, The University of Queensland, Brisbane, QLD</wicri:regionArea></affiliation></author><author><name sortKey="Dugger, Katie M" sort="Dugger, Katie M" uniqKey="Dugger K" first="Katie M" last="Dugger">Katie M. Dugger</name><affiliation wicri:level="1"><nlm:affiliation>U.S. Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit, Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR 97331, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>U.S. Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit, Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR 97331</wicri:regionArea></affiliation></author><author><name sortKey="Ballard, Grant" sort="Ballard, Grant" uniqKey="Ballard G" first="Grant" last="Ballard">Grant Ballard</name><affiliation wicri:level="1"><nlm:affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Point Blue Conservation Science, Petaluma, CA 94954</wicri:regionArea></affiliation></author><author><name sortKey="Ainley, David G" sort="Ainley, David G" uniqKey="Ainley D" first="David G" last="Ainley">David G. Ainley</name><affiliation wicri:level="1"><nlm:affiliation>HT Harvey and Associates, Los Gatos, CA 95032, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>HT Harvey and Associates, Los Gatos, CA 95032</wicri:regionArea></affiliation></author><author><name sortKey="Varsani, Arvind" sort="Varsani, Arvind" uniqKey="Varsani A" first="Arvind" last="Varsani">Arvind Varsani</name><affiliation wicri:level="1"><nlm:affiliation>The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life sciences, Arizona State University, Tempe, AZ 85287, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life sciences, Arizona State University, Tempe, AZ 85287</wicri:regionArea></affiliation></author></analytic><series><title level="j">Virus evolution</title><idno type="ISSN">2057-1577</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The family Papillomaviridae 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 (n = 5), a fish (n = 1), a snake (n = 1), and turtles (n = 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 (Pygoscelis adeliae) 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, Morelia spilota, associated papillomavirus) cluster near the base of the papillomavirus evolutionary tree. A papillomavirus isolated from an avian host (Northern fulmar; Fulmarus glacialis), 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.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">29026649</PMID><DateCreated><Year>2017</Year><Month>10</Month><Day>13</Day></DateCreated><DateRevised><Year>2017</Year><Month>10</Month><Day>17</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">2057-1577</ISSN><JournalIssue CitedMedium="Print"><Volume>3</Volume><Issue>2</Issue><PubDate><Year>2017</Year><Month>Jul</Month></PubDate></JournalIssue><Title>Virus evolution</Title><ISOAbbreviation>Virus Evol</ISOAbbreviation></Journal><ArticleTitle>Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins.</ArticleTitle><Pagination><MedlinePgn>vex027</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1093/ve/vex027</ELocationID><Abstract><AbstractText>The family Papillomaviridae 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 (n = 5), a fish (n = 1), a snake (n = 1), and turtles (n = 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 (Pygoscelis adeliae) 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, Morelia spilota, associated papillomavirus) cluster near the base of the papillomavirus evolutionary tree. A papillomavirus isolated from an avian host (Northern fulmar; Fulmarus glacialis), 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.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Van Doorslaer</LastName><ForeName>Koenraad</ForeName><Initials>K</Initials><Identifier Source="ORCID">0000-0002-2985-0733</Identifier><AffiliationInfo><Affiliation>ACBS and Bio5, University of Arizona, 1657 E Helen St, Tucson, AZ 85721, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ruoppolo</LastName><ForeName>Valeria</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>Laboratório de Patologia Comparada de Animais Selvagens (LAPCOM), Departamento de Patologia, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São Paulo, São Paulo, Brazil.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schmidt</LastName><ForeName>Annie</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lescroël</LastName><ForeName>Amelie</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Centre d'Ecologie Fonctionnelle et Evolutive - CNRS, UMR 5175, Montpellier, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jongsomjit</LastName><ForeName>Dennis</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Elrod</LastName><ForeName>Megan</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kraberger</LastName><ForeName>Simona</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life sciences, Arizona State University, Tempe, AZ 85287, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Stainton</LastName><ForeName>Daisy</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>School of Biological Sciences, The University of Queensland, Brisbane, QLD, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dugger</LastName><ForeName>Katie M</ForeName><Initials>KM</Initials><AffiliationInfo><Affiliation>U.S. Geological Survey, Oregon Cooperative Fish and Wildlife Research Unit, Department of Fisheries and Wildlife, Oregon State University, Corvallis, OR 97331, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ballard</LastName><ForeName>Grant</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Point Blue Conservation Science, Petaluma, CA 94954, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ainley</LastName><ForeName>David G</ForeName><Initials>DG</Initials><AffiliationInfo><Affiliation>HT Harvey and Associates, Los Gatos, CA 95032, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Varsani</LastName><ForeName>Arvind</ForeName><Initials>A</Initials><Identifier Source="ORCID">0000-0003-4111-2415</Identifier><AffiliationInfo><Affiliation>The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life sciences, Arizona State University, Tempe, AZ 85287, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Observatory, Cape Town, 7925, South 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