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Discovery of several thousand highly diverse circular DNA viruses

Michael J. Tisza, Diana V. Pastrana, Nicole L. Welch, Brittany Stewart, Alberto Peretti, Gabriel J. Starrett, Yuk-Ying S. Pang, Siddharth R. Krishnamurthy, Patricia A. Pesavento, David H. McDermott, Philip M. Murphy, Jessica L. Whited, Bess Miller, Jason M. Brenchley, Stephan P. Rosshart, Barbara Rehermann, John Doorbar, Blake A. Ta’ala, Olga Pletnikova, Juan Troncoso, Susan M. Resnick, Ben Bolduc, Matthew B. Sullivan, Arvind Varsani, Anca M. Segall, View ORCID ProfileChristopher B. Buck
doi: https://doi.org/10.1101/555375
Michael J. Tisza
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD 20892-4263
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Diana V. Pastrana
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD 20892-4263
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Nicole L. Welch
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD 20892-4263
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Brittany Stewart
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD 20892-4263
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Alberto Peretti
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD 20892-4263
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Gabriel J. Starrett
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD 20892-4263
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Yuk-Ying S. Pang
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD 20892-4263
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Siddharth R. Krishnamurthy
2Metaorganism Immunity Section, Laboratory of Immune System Biology, NIAID, NIH, Bethesda, MD 20892-4263
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Patricia A. Pesavento
3Department of Pathology, Microbiology, and Immunology, University of California, Davis, CA 95616, USA
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David H. McDermott
4Molecular Signaling Section, Laboratory of Molecular Immunology, NIAID, Bethesda, Maryland, USA
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Philip M. Murphy
4Molecular Signaling Section, Laboratory of Molecular Immunology, NIAID, Bethesda, Maryland, USA
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Jessica L. Whited
5Department of Orthopedic Surgery, Harvard Medical School, The Harvard Stem Cell Institute, Brigham and Women’s Hospital, 60 Fenwood Road, Boston, MA, 02115, USA
6Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, MA, 02142, USA
7Department of Stem Cell and Regenerative Biology, Harvard University, 7 Divinity Avenue, Cambridge, MA, 02138, USA
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Bess Miller
5Department of Orthopedic Surgery, Harvard Medical School, The Harvard Stem Cell Institute, Brigham and Women’s Hospital, 60 Fenwood Road, Boston, MA, 02115, USA
6Broad Institute of MIT and Harvard, 7 Cambridge Center, Cambridge, MA, 02142, USA
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Jason M. Brenchley
8Barrier Immunity Section, Lab of Viral Diseases, NIAID, NIH, MD 20892
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Stephan P. Rosshart
9Immunology Section, Liver Diseases Branch, NIDDK, NIH, Bethesda, MD 20892-1800
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Barbara Rehermann
9Immunology Section, Liver Diseases Branch, NIDDK, NIH, Bethesda, MD 20892-1800
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John Doorbar
10Department of Pathology, University of Cambridge, Tennis Court Road, Cambridge, CB2 1QP, UK
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Blake A. Ta’ala
11Mililani Mauka Elementary, Mililani, HI, 96789, USA
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Olga Pletnikova
12Department of Pathology (Neuropathology), Johns Hopkins University School of Medicine, Baltimore, MD, USA
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Juan Troncoso
12Department of Pathology (Neuropathology), Johns Hopkins University School of Medicine, Baltimore, MD, USA
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Susan M. Resnick
13Laboratory of Behavioral Neuroscience, National Institute on Aging, Baltimore, MD 21224, USA
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Ben Bolduc
14Department of Microbiology, Ohio State University, Columbus, Ohio, United States
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Matthew B. Sullivan
14Department of Microbiology, Ohio State University, Columbus, Ohio, United States
15Civil, Environmental and Geodetic Engineering, Ohio State University, Columbus, Ohio, United States
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Arvind Varsani
16The Biodesign Center of Fundamental and Applied Microbiomics, School of Life Sciences, Center for Evolution and Medicine, Arizona State University, 1001 S. McAllister Ave, Tempe, AZ 85287-5001, USA
17Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Rondebosch, 7701, Cape Town, South Africa
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Anca M. Segall
18Viral Information Institute & Department of Biology, San Diego State University, San Diego, CA, 92182-4614, USA
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Christopher B. Buck
1Lab of Cellular Oncology, NCI, NIH, Bethesda, MD 20892-4263
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  • ORCID record for Christopher B. Buck
  • For correspondence: buckc@mail.nih.gov
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Summary

Although it is suspected that there are millions of distinct viral species, fewer than 9,000 are catalogued in GenBank’s RefSeq database. We selectively enriched for and amplified the genomes of circular DNA viruses in over 70 animal samples, ranging from cultured soil nematodes to human tissue specimens. A bioinformatics pipeline, Cenote-Taker, was developed to automatically annotate over 2,500 circular genomes in a GenBank-compliant format. The new genomes belong to dozens of established and emerging viral families. Some appear to be the result of previously undescribed recombination events between ssDNA viruses and ssRNA viruses. In addition, hundreds of circular DNA elements that do not encode any discernable similarities to previously characterized sequences were identified. To characterize these “dark matter” sequences, we used an artificial neural network to identify candidate viral capsid proteins, several of which formed virus-like particles when expressed in culture. These data further the understanding of viral sequence diversity and allow for high throughput documentation of the virosphere.

Footnotes

  • ↵19 Lead contact

  • https://www.ncbi.nlm.nih.gov/bioproject/PRJNA393166

  • https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA396064

  • https://ccrod.cancer.gov/confluence/display/LCOTF/DarkMatter

  • http://www.cyverse.org/discovery-environment

Copyright 
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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Discovery of several thousand highly diverse circular DNA viruses
Michael J. Tisza, Diana V. Pastrana, Nicole L. Welch, Brittany Stewart, Alberto Peretti, Gabriel J. Starrett, Yuk-Ying S. Pang, Siddharth R. Krishnamurthy, Patricia A. Pesavento, David H. McDermott, Philip M. Murphy, Jessica L. Whited, Bess Miller, Jason M. Brenchley, Stephan P. Rosshart, Barbara Rehermann, John Doorbar, Blake A. Ta’ala, Olga Pletnikova, Juan Troncoso, Susan M. Resnick, Ben Bolduc, Matthew B. Sullivan, Arvind Varsani, Anca M. Segall, Christopher B. Buck
bioRxiv 555375; doi: https://doi.org/10.1101/555375
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Discovery of several thousand highly diverse circular DNA viruses
Michael J. Tisza, Diana V. Pastrana, Nicole L. Welch, Brittany Stewart, Alberto Peretti, Gabriel J. Starrett, Yuk-Ying S. Pang, Siddharth R. Krishnamurthy, Patricia A. Pesavento, David H. McDermott, Philip M. Murphy, Jessica L. Whited, Bess Miller, Jason M. Brenchley, Stephan P. Rosshart, Barbara Rehermann, John Doorbar, Blake A. Ta’ala, Olga Pletnikova, Juan Troncoso, Susan M. Resnick, Ben Bolduc, Matthew B. Sullivan, Arvind Varsani, Anca M. Segall, Christopher B. Buck
bioRxiv 555375; doi: https://doi.org/10.1101/555375

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