Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins
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 turtle...
Published in: | Virus Evolution |
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Main Authors: | , , , , , , , , , , , |
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Format: | Article in Journal/Newspaper |
Language: | English |
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OXFORD UNIV PRESS
2017
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Online Access: | http://hdl.handle.net/10150/627073 https://doi.org/10.1093/ve/vex027 |
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ftunivarizona:oai:repository.arizona.edu:10150/627073 |
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record_format |
openpolar |
institution |
Open Polar |
collection |
The University of Arizona: UA Campus Repository |
op_collection_id |
ftunivarizona |
language |
English |
topic |
papillomavirus evolution bird reptile avian |
spellingShingle |
papillomavirus evolution bird reptile avian Van Doorslaer, Koenraad Ruoppolo, Valeria Schmidt, Annie Lescroël, Amelie Jongsomjit, Dennis Elrod, Megan Kraberger, Simona Stainton, Daisy Dugger, Katie M Ballard, Grant Ainley, David G Varsani, Arvind Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins |
topic_facet |
papillomavirus evolution bird reptile avian |
description |
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 Adelie penguin (Pygoscelis adeliae) from Cape Crozier, Ross Island (Antarctica). The new papillomavirus shares similar to 64 per cent genome-wide identity to a previously described Adelie 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. US National Science Foundation (NSF) [ANT-0944411]; State of Arizona Improving Health TRIF; National Institute of Food and Agriculture, U.S. Department of Agriculture, Hatch NC229; Center of Evolution and Medicine Venture Fund (Center of Evolution and Medicine, Arizona State University, USA) grant Open Access Journal. This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu. |
author2 |
Univ Arizona, ACBS & Bio5 |
format |
Article in Journal/Newspaper |
author |
Van Doorslaer, Koenraad Ruoppolo, Valeria Schmidt, Annie Lescroël, Amelie Jongsomjit, Dennis Elrod, Megan Kraberger, Simona Stainton, Daisy Dugger, Katie M Ballard, Grant Ainley, David G Varsani, Arvind |
author_facet |
Van Doorslaer, Koenraad Ruoppolo, Valeria Schmidt, Annie Lescroël, Amelie Jongsomjit, Dennis Elrod, Megan Kraberger, Simona Stainton, Daisy Dugger, Katie M Ballard, Grant Ainley, David G Varsani, Arvind |
author_sort |
Van Doorslaer, Koenraad |
title |
Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins |
title_short |
Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins |
title_full |
Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins |
title_fullStr |
Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins |
title_full_unstemmed |
Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins |
title_sort |
unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins |
publisher |
OXFORD UNIV PRESS |
publishDate |
2017 |
url |
http://hdl.handle.net/10150/627073 https://doi.org/10.1093/ve/vex027 |
long_lat |
ENVELOPE(169.400,169.400,-77.517,-77.517) ENVELOPE(169.400,169.400,-77.517,-77.517) ENVELOPE(-46.016,-46.016,-60.616,-60.616) |
geographic |
Cape Crozier Crozier Fulmar Ross Island |
geographic_facet |
Cape Crozier Crozier Fulmar Ross Island |
genre |
Adelie penguin Antarc* Antarctica Fulmarus glacialis Northern Fulmar Pygoscelis adeliae Ross Island |
genre_facet |
Adelie penguin Antarc* Antarctica Fulmarus glacialis Northern Fulmar Pygoscelis adeliae Ross Island |
op_relation |
http://academic.oup.com/ve/article/doi/10.1093/vex027/4372179/Unique-genome-organization-of-nonmammalian Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins 2017, 3 (2) Virus Evolution 2057-1577 29026649 doi:10.1093/ve/vex027 http://hdl.handle.net/10150/627073 Virus Evolution |
op_rights |
© The Author 2017. Published by Oxford University Press. |
op_doi |
https://doi.org/10.1093/ve/vex027 |
container_title |
Virus Evolution |
container_volume |
3 |
container_issue |
2 |
_version_ |
1766373168999563264 |
spelling |
ftunivarizona:oai:repository.arizona.edu:10150/627073 2023-05-15T13:04:51+02:00 Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins Van Doorslaer, Koenraad Ruoppolo, Valeria Schmidt, Annie Lescroël, Amelie Jongsomjit, Dennis Elrod, Megan Kraberger, Simona Stainton, Daisy Dugger, Katie M Ballard, Grant Ainley, David G Varsani, Arvind Univ Arizona, ACBS & Bio5 2017-07 http://hdl.handle.net/10150/627073 https://doi.org/10.1093/ve/vex027 en eng OXFORD UNIV PRESS http://academic.oup.com/ve/article/doi/10.1093/vex027/4372179/Unique-genome-organization-of-nonmammalian Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins 2017, 3 (2) Virus Evolution 2057-1577 29026649 doi:10.1093/ve/vex027 http://hdl.handle.net/10150/627073 Virus Evolution © The Author 2017. Published by Oxford University Press. papillomavirus evolution bird reptile avian Article 2017 ftunivarizona https://doi.org/10.1093/ve/vex027 2020-06-14T08:16:12Z 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 Adelie penguin (Pygoscelis adeliae) from Cape Crozier, Ross Island (Antarctica). The new papillomavirus shares similar to 64 per cent genome-wide identity to a previously described Adelie 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. US National Science Foundation (NSF) [ANT-0944411]; State of Arizona Improving Health TRIF; National Institute of Food and Agriculture, U.S. Department of Agriculture, Hatch NC229; Center of Evolution and Medicine Venture Fund (Center of Evolution and Medicine, Arizona State University, USA) grant Open Access Journal. This item from the UA Faculty Publications collection is made available by the University of Arizona with support from the University of Arizona Libraries. If you have questions, please contact us at repository@u.library.arizona.edu. Article in Journal/Newspaper Adelie penguin Antarc* Antarctica Fulmarus glacialis Northern Fulmar Pygoscelis adeliae Ross Island The University of Arizona: UA Campus Repository Cape Crozier ENVELOPE(169.400,169.400,-77.517,-77.517) Crozier ENVELOPE(169.400,169.400,-77.517,-77.517) Fulmar ENVELOPE(-46.016,-46.016,-60.616,-60.616) Ross Island Virus Evolution 3 2 |