Virus discovery in all three major lineages of terrestrial arthropods highlights the diversity of single-stranded DNA viruses associated with invertebrates

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1 College of Marine Science, University of South Florida, Saint Petersburg, Florida, United States
2 Department of Biological Sciences, University of Toronto, Scarborough, Scarborough, Ontario, Canada
3 Department of Biology, University of Vermont, Burlington, Vermont, United States
4 Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States
5 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts, United States
6 Department of Biological Sciences, University of South Florida Saint Petersburg, Saint Petersburg, Florida, United States
7 School of Forest Resources and Conservation, University of Florida, Gainesville, Florida, United States
8 The Biodesign Center for Fundamental and Applied Microbiomics, School of Life Sciences, Center for Evolution and Medicine, Arizona State University, Tempe, Arizona, United States
9 Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Cape Town, South Africa
DOI
10.7287/peerj.preprints.27093v1
Published
Accepted
Subject Areas
Biodiversity, Entomology, Genomics, Microbiology, Virology
Keywords
invertebrate, arthropod, CRESS DNA, ssDNA, replication-associated protein (Rep), spider, insect, discovery, virus
Copyright
© 2018 Rosario et al.
Licence
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ Preprints) and either DOI or URL of the article must be cited.
Cite this article
Rosario K, Mettel KA, Benner BE, Johnson R, Scott C, Yusseff-Vanegas SZ, Baker CC, Cassill DL, Storer C, Varsani A, Breitbart M. 2018. Virus discovery in all three major lineages of terrestrial arthropods highlights the diversity of single-stranded DNA viruses associated with invertebrates. PeerJ Preprints 6:e27093v1

Abstract

Viruses encoding a replication-associated protein (Rep) within a covalently closed, single-stranded (ss)DNA genome are among the smallest viruses known to infect eukaryotic organisms, including economically valuable agricultural crops and livestock. Although circular Rep-encoding ssDNA (CRESS DNA) viruses are a widespread group for which our knowledge is rapidly expanding, biased sampling towards vertebrates and land plants has limited our understanding of their diversity and evolution. Here we screened terrestrial arthropods for CRESS DNA viruses and report the identification of 44 viral genomes and replicons associated with specimens representing all three major terrestrial arthropod lineages, namely Euchelicerata (spiders), Hexapoda (insects), and Myriapoda (millipedes). We identified virus genomes belonging to three established CRESS DNA viral families (Circoviridae, Genomoviridae, and Smacoviridae); however, over half of the arthropod-associated virus genomes are only distantly related to currently classified CRESS DNA viral sequences. Although members of viral and satellite families known to infect plants (Geminiviridae, Nanoviridae, Alphasatellitidae) were not identified in this study, these plant-infecting CRESS DNA viruses and replicons are transmitted by hemipterans. Therefore, members from six out of the seven established CRESS DNA viral families circulate among arthropods. Furthermore, a phylogenetic analysis of Reps, including endogenous viral sequences, reported to date from a wide array of organisms revealed that most of the known CRESS DNA viral diversity circulates among invertebrates. Our results highlight the vast and unexplored diversity of CRESS DNA viruses among invertebrates and parallel findings from RNA viral discovery efforts in undersampled taxa.

Author Comment

This is a submission to PeerJ for review.

Supplemental Information

Alignment used to create approximately maximum likelihood tree shown in Figure 1 in fasta format

Alignment used to create approximately maximum likelihood tree shown in Figure 1 in fasta format. Details regarding sequence acronyms, descriptions, and accession numbers can be found in Supplemental Data S2.

DOI: 10.7287/peerj.preprints.27093v1/supp-1

Excel workbook containing three worksheets (W#) with details on intrinsically disordered protein (IDP) profiles, sequences used for Figure 1, accession numbers of non-CRESS DNA molecules

Excel workbook containing three worksheets (W#) with the following information: details regarding intrinsically disordered protein (IDP) profiles (W1), detailed information for sequences found in the alignment used to create approximately maximum likelihood tree shown in Figure 1 (Data S1) (W2), and a table listing accession numbers and information regarding non-CRESS DNA molecules detected in terrestrial arthropods (W3).

DOI: 10.7287/peerj.preprints.27093v1/supp-2