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 Brenchley; Stephan P. Rosshart; Barbara Rehermann; John Doorbar; Blake A. Ta’ala; Olga Pletnikova; Juan C. Troncoso; Susan M. Resnick; Ben Bolduc; Matthew B. Sullivan; Arvind Varsani; Anca M. Segall; Christopher B. Buck

doi:10.7554/eLife.51971

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 Brenchley, Stephan P. Rosshart, Barbara Rehermann, John Doorbar, Blake A. Ta’ala, Olga Pletnikova, Juan C. TroncosoSusan M. Resnick, Ben Bolduc, Matthew B. Sullivan, Arvind Varsani, Anca M. Segall, Christopher B. Buck

Life Sciences, School of (SOLS)

Research output: Contribution to journal › Article › peer-review

116 Scopus citations

Abstract

Although millions of distinct virus species likely exist, only approximately 9000 are catalogued in GenBank’s RefSeq database. We selectively enriched for the genomes of circular DNA viruses in over 70 animal samples, ranging from nematodes to human tissue specimens. A bioinformatics pipeline, Cenote-Taker, was developed to automatically annotate over 2500 complete 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 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.

Original language	English (US)
Article number	e51971
Journal	eLife
Volume	9
DOIs	https://doi.org/10.7554/eLife.51971
State	Published - Feb 2020

ASJC Scopus subject areas

General Neuroscience
General Biochemistry, Genetics and Molecular Biology
General Immunology and Microbiology

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10.7554/eLife.51971

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Tisza, M. J., Pastrana, D. V., Welch, N. L., Stewart, B., Peretti, A., Starrett, G. J., Pang, Y. Y. S., Krishnamurthy, S. R., Pesavento, P. A., McDermott, D. H., Murphy, P. M., Whited, J. L., Miller, B., Brenchley, J., Rosshart, S. P., Rehermann, B., Doorbar, J., Ta’ala, B. A., Pletnikova, O., ... Buck, C. B. (2020). Discovery of several thousand highly diverse circular DNA viruses. eLife, 9, Article e51971. https://doi.org/10.7554/eLife.51971

Tisza, MJ, Pastrana, DV, Welch, NL, Stewart, B, Peretti, A, Starrett, GJ, Pang, YYS, Krishnamurthy, SR, Pesavento, PA, McDermott, DH, Murphy, PM, Whited, JL, Miller, B, Brenchley, J, Rosshart, SP, Rehermann, B, Doorbar, J, Ta’ala, BA, Pletnikova, O, Troncoso, JC, Resnick, SM, Bolduc, B, Sullivan, MB, Varsani, A, Segall, AM & Buck, CB 2020, 'Discovery of several thousand highly diverse circular DNA viruses', eLife, vol. 9, e51971. https://doi.org/10.7554/eLife.51971

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title = "Discovery of several thousand highly diverse circular DNA viruses",

abstract = "Although millions of distinct virus species likely exist, only approximately 9000 are catalogued in GenBank{\textquoteright}s RefSeq database. We selectively enriched for the genomes of circular DNA viruses in over 70 animal samples, ranging from nematodes to human tissue specimens. A bioinformatics pipeline, Cenote-Taker, was developed to automatically annotate over 2500 complete 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 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 {\textquoteleft}dark matter{\textquoteright} 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.",

author = "Tisza, {Michael J.} and Pastrana, {Diana V.} and Welch, {Nicole L.} and Brittany Stewart and Alberto Peretti and Starrett, {Gabriel J.} and Pang, {Yuk Ying S.} and Krishnamurthy, {Siddharth R.} and Pesavento, {Patricia A.} and McDermott, {David H.} and Murphy, {Philip M.} and Whited, {Jessica L.} and Bess Miller and Jason Brenchley and Rosshart, {Stephan P.} and Barbara Rehermann and John Doorbar and Ta{\textquoteright}ala, {Blake A.} and Olga Pletnikova and Troncoso, {Juan C.} and Resnick, {Susan M.} and Ben Bolduc and Sullivan, {Matthew B.} and Arvind Varsani and Segall, {Anca M.} and Buck, {Christopher B.}",

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AU - Pang, Yuk Ying S.

AU - Krishnamurthy, Siddharth R.

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AU - Pletnikova, Olga

AU - Troncoso, Juan C.

AU - Resnick, Susan M.

AU - Bolduc, Ben

AU - Sullivan, Matthew B.

AU - Varsani, Arvind

AU - Segall, Anca M.

AU - Buck, Christopher B.

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Discovery of several thousand highly diverse circular DNA viruses

Abstract

ASJC Scopus subject areas

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