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Identification of Adomavirus Virion Proteins

Nicole L. Welch, Michael J. Tisza, Gabriel J. Starrett, Anna K. Belford, Diana V. Pastrana, Yuk-Ying S. Pang, John T. Schiller, Ping An, Paul G. Cantalupo, James M. Pipas, Samantha Koda, Kuttichantran Subramaniam, Thomas B. Waltzek, Chao Bian, Qiong Shi, Zhiqiang Ruan, View ORCID ProfileTerry Fei Fan Ng, View ORCID ProfileChristopher B. Buck
doi: https://doi.org/10.1101/341131
Nicole L. Welch
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD, 20892 USA
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Michael J. Tisza
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD, 20892 USA
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Gabriel J. Starrett
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD, 20892 USA
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Anna K. Belford
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD, 20892 USA
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Diana V. Pastrana
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD, 20892 USA
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Yuk-Ying S. Pang
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD, 20892 USA
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John T. Schiller
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD, 20892 USA
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Ping An
2Dept. of Biological Sciences, Univ. of Pittsburgh, Pittsburgh, PA 15260 USA
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Paul G. Cantalupo
2Dept. of Biological Sciences, Univ. of Pittsburgh, Pittsburgh, PA 15260 USA
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James M. Pipas
2Dept. of Biological Sciences, Univ. of Pittsburgh, Pittsburgh, PA 15260 USA
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Samantha Koda
3Dept. of Infectious Disease and Pathology, Univ. of Florida, Gainesville, FL, 32611 USA
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Kuttichantran Subramaniam
3Dept. of Infectious Disease and Pathology, Univ. of Florida, Gainesville, FL, 32611 USA
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Thomas B. Waltzek
3Dept. of Infectious Disease and Pathology, Univ. of Florida, Gainesville, FL, 32611 USA
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Chao Bian
4Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI, Shenzhen, Guangdong 518083, China
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Qiong Shi
4Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI, Shenzhen, Guangdong 518083, China
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Zhiqiang Ruan
4Shenzhen Key Lab of Marine Genomics, Guangdong Provincial Key Lab of Molecular Breeding in Marine Economic Animals, BGI Academy of Marine Sciences, BGI, Shenzhen, Guangdong 518083, China
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Terry Fei Fan Ng
5College of Veterinary Medicine, University of Georgia, Athens, GA 30602 USA
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  • ORCID record for Terry Fei Fan Ng
Christopher B. Buck
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD, 20892 USA
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  • ORCID record for Christopher B. Buck
  • For correspondence: buckc{at}mail.nih.gov
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Abstract

Adenoviruses, papillomaviruses, and polyomaviruses are collectively known as small DNA tumor viruses. Although it has long been recognized that small DNA tumor virus oncoproteins and capsid proteins show a variety of structural and functional similarities, it is unclear whether these similarities reflect descent from a common ancestor, convergent evolution, horizontal gene transfer among virus lineages, or acquisition of genes from host cells. Here, we report the discovery of a dozen new members of an emerging virus family, the Adomaviridae, that unite a papillomavirus/polyomavirus-like replicase gene with an adenovirus-like virion maturational protease. Adomaviruses were initially discovered in a lethal disease outbreak among endangered Japanese eels. New adomavirus genomes were found in additional commercially important fish species, such as tilapia, as well as in reptiles. The search for adomavirus sequences also revealed an additional candidate virus family, which we refer to as xenomaviruses, in mollusk datasets. Analysis of native adomavirus virions and expression of recombinant proteins showed that the virion structural proteins of adomaviruses are homologous to those of both adenoviruses and another emerging animal virus family called adintoviruses. The results pave the way toward development of vaccines against adomaviruses and suggest a framework that ties small DNA tumor viruses into a shared evolutionary history.

Author Summary In contrast to cellular organisms, viruses do not encode any universally conserved genes. Even within a given family of viruses, the amino acid sequences encoded by homologous genes can diverge to the point of unrecognizability. Although members of an emerging virus family, the Adomaviridae, encode replicative DNA helicase proteins that are recognizably similar to those of polyomaviruses and papillomaviruses, the functions of other adomavirus genes have been difficult to identify. Using a combination of laboratory and bioinformatic approaches, we identify the adomavirus virion structural proteins. The results link adomavirus virion protein operons to those of other midsize non-enveloped DNA viruses, including adenoviruses and adintoviruses.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. This article is a US Government work. It is not subject to copyright under 17 USC 105 and is also made available for use under a CC0 license.
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Posted March 04, 2020.
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Identification of Adomavirus Virion Proteins
Nicole L. Welch, Michael J. Tisza, Gabriel J. Starrett, Anna K. Belford, Diana V. Pastrana, Yuk-Ying S. Pang, John T. Schiller, Ping An, Paul G. Cantalupo, James M. Pipas, Samantha Koda, Kuttichantran Subramaniam, Thomas B. Waltzek, Chao Bian, Qiong Shi, Zhiqiang Ruan, Terry Fei Fan Ng, Christopher B. Buck
bioRxiv 341131; doi: https://doi.org/10.1101/341131
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Identification of Adomavirus Virion Proteins
Nicole L. Welch, Michael J. Tisza, Gabriel J. Starrett, Anna K. Belford, Diana V. Pastrana, Yuk-Ying S. Pang, John T. Schiller, Ping An, Paul G. Cantalupo, James M. Pipas, Samantha Koda, Kuttichantran Subramaniam, Thomas B. Waltzek, Chao Bian, Qiong Shi, Zhiqiang Ruan, Terry Fei Fan Ng, Christopher B. Buck
bioRxiv 341131; doi: https://doi.org/10.1101/341131

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