Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula

There is growing interest in uncovering the viral diversity present in wild animal species. The remote Antarctic region is home to a wealth of uncovered microbial diversity, some of which is associated with its megafauna, including penguin species, the dominant avian biota. Penguins interface with a...

Full description

Bibliographic Details
Main Authors: Hila Levy, Rafaela S. Fontenele, Ciara Harding, Crystal Suazo, Simona Kraberger, Kara Schmidlin, Anni Djurhuus, Caitlin E. Black, Tom Hart, Adrian L. Smith, Arvind Varsani
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/12/9/1029
_version_ 1797553564032172032
author Hila Levy
Rafaela S. Fontenele
Ciara Harding
Crystal Suazo
Simona Kraberger
Kara Schmidlin
Anni Djurhuus
Caitlin E. Black
Tom Hart
Adrian L. Smith
Arvind Varsani
author_facet Hila Levy
Rafaela S. Fontenele
Ciara Harding
Crystal Suazo
Simona Kraberger
Kara Schmidlin
Anni Djurhuus
Caitlin E. Black
Tom Hart
Adrian L. Smith
Arvind Varsani
author_sort Hila Levy
collection DOAJ
description There is growing interest in uncovering the viral diversity present in wild animal species. The remote Antarctic region is home to a wealth of uncovered microbial diversity, some of which is associated with its megafauna, including penguin species, the dominant avian biota. Penguins interface with a number of other biota in their roles as marine mesopredators and several species overlap in their ranges and habitats. To characterize the circular single-stranded viruses related to those in the phylum <i>Cressdnaviricota</i> from these environmental sentinel species, cloacal swabs (<i>n</i> = 95) were obtained from King Penguins in South Georgia, and congeneric Adélie Penguins, Chinstrap Penguins, and Gentoo Penguins across the South Shetland Islands and Antarctic Peninsula. Using a combination of high-throughput sequencing, abutting primers-based PCR recovery of circular genomic elements, cloning, and Sanger sequencing, we detected 97 novel sequences comprising 40 ssDNA viral genomes and 57 viral-like circular molecules from 45 individual penguins. We present their detection patterns, with Chinstrap Penguins harboring the highest number of new sequences. The novel Antarctic viruses identified appear to be host-specific, while one circular molecule was shared between sympatric Chinstrap and Gentoo Penguins. We also report viral genotype sharing between three adult-chick pairs, one in each Pygoscelid species. Sequence similarity network approaches coupled with Maximum likelihood phylogenies of the clusters indicate the 40 novel viral genomes do not fall within any known viral families and likely fall within the recently established phylum <i>Cressdnaviricota</i> based on their replication-associated protein sequences. Similarly, 83 capsid protein sequences encoded by the viruses or viral-like circular molecules identified in this study do not cluster with any of those encoded by classified viral groups. Further research is warranted to expand knowledge of the Antarctic virome and would help elucidate the importance of viral-like molecules in vertebrate host evolution.
first_indexed 2024-03-10T16:18:19Z
format Article
id doaj.art-1d7a2a4b8dad40dd8e8a492bd1394bcb
institution Directory Open Access Journal
issn 1999-4915
language English
last_indexed 2024-03-10T16:18:19Z
publishDate 2020-09-01
publisher MDPI AG
record_format Article
series Viruses
spelling doaj.art-1d7a2a4b8dad40dd8e8a492bd1394bcb2023-11-20T13:52:53ZengMDPI AGViruses1999-49152020-09-01129102910.3390/v12091029Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic PeninsulaHila Levy0Rafaela S. Fontenele1Ciara Harding2Crystal Suazo3Simona Kraberger4Kara Schmidlin5Anni Djurhuus6Caitlin E. Black7Tom Hart8Adrian L. Smith9Arvind Varsani10Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3SZ, UKThe Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ 85287-5001, USA.The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ 85287-5001, USA.The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ 85287-5001, USA.The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ 85287-5001, USA.The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ 85287-5001, USA.Faculty of Science and Technology, University of the Faroe Islands, Vestarabryggja 15, FO-100 Tórshavn, Faroe IslandsDepartment of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, SwitzerlandDepartment of Zoology, University of Oxford, South Parks Road, Oxford OX1 3SZ, UKDepartment of Zoology, University of Oxford, South Parks Road, Oxford OX1 3SZ, UKThe Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ 85287-5001, USA.There is growing interest in uncovering the viral diversity present in wild animal species. The remote Antarctic region is home to a wealth of uncovered microbial diversity, some of which is associated with its megafauna, including penguin species, the dominant avian biota. Penguins interface with a number of other biota in their roles as marine mesopredators and several species overlap in their ranges and habitats. To characterize the circular single-stranded viruses related to those in the phylum <i>Cressdnaviricota</i> from these environmental sentinel species, cloacal swabs (<i>n</i> = 95) were obtained from King Penguins in South Georgia, and congeneric Adélie Penguins, Chinstrap Penguins, and Gentoo Penguins across the South Shetland Islands and Antarctic Peninsula. Using a combination of high-throughput sequencing, abutting primers-based PCR recovery of circular genomic elements, cloning, and Sanger sequencing, we detected 97 novel sequences comprising 40 ssDNA viral genomes and 57 viral-like circular molecules from 45 individual penguins. We present their detection patterns, with Chinstrap Penguins harboring the highest number of new sequences. The novel Antarctic viruses identified appear to be host-specific, while one circular molecule was shared between sympatric Chinstrap and Gentoo Penguins. We also report viral genotype sharing between three adult-chick pairs, one in each Pygoscelid species. Sequence similarity network approaches coupled with Maximum likelihood phylogenies of the clusters indicate the 40 novel viral genomes do not fall within any known viral families and likely fall within the recently established phylum <i>Cressdnaviricota</i> based on their replication-associated protein sequences. Similarly, 83 capsid protein sequences encoded by the viruses or viral-like circular molecules identified in this study do not cluster with any of those encoded by classified viral groups. Further research is warranted to expand knowledge of the Antarctic virome and would help elucidate the importance of viral-like molecules in vertebrate host evolution.https://www.mdpi.com/1999-4915/12/9/1029<i>Cressdnaviricota</i>circular moleculespenguinsvirusesAntarctica<i>Pygoscelis antarcticus</i>
spellingShingle Hila Levy
Rafaela S. Fontenele
Ciara Harding
Crystal Suazo
Simona Kraberger
Kara Schmidlin
Anni Djurhuus
Caitlin E. Black
Tom Hart
Adrian L. Smith
Arvind Varsani
Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula
Viruses
<i>Cressdnaviricota</i>
circular molecules
penguins
viruses
Antarctica
<i>Pygoscelis antarcticus</i>
title Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula
title_full Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula
title_fullStr Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula
title_full_unstemmed Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula
title_short Identification and Distribution of Novel Cressdnaviruses and Circular Molecules in Four Penguin Species in South Georgia and the Antarctic Peninsula
title_sort identification and distribution of novel cressdnaviruses and circular molecules in four penguin species in south georgia and the antarctic peninsula
topic <i>Cressdnaviricota</i>
circular molecules
penguins
viruses
Antarctica
<i>Pygoscelis antarcticus</i>
url https://www.mdpi.com/1999-4915/12/9/1029
work_keys_str_mv AT hilalevy identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT rafaelasfontenele identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT ciaraharding identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT crystalsuazo identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT simonakraberger identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT karaschmidlin identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT annidjurhuus identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT caitlineblack identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT tomhart identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT adrianlsmith identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula
AT arvindvarsani identificationanddistributionofnovelcressdnavirusesandcircularmoleculesinfourpenguinspeciesinsouthgeorgiaandtheantarcticpeninsula