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

Karyna Rosario; Kaitlin A Mettel; Bayleigh E Benner; Ryan Johnson; Catherine Scott; Sohath Z Yusseff-Vanegas; Christopher C M Baker; Deby L Cassill; Caroline Storer; Arvind Varsani; Mya Breitbart

doi:10.7717/peerj.5761

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

PeerJ. 2018 Oct 11:6:e5761. doi: 10.7717/peerj.5761. eCollection 2018.

Authors

Affiliations

¹ College of Marine Science, University of South Florida, Saint Petersburg, FL, USA.
² Department of Biological Sciences, University of Toronto, Scarborough, Scarborough, ON, Canada.
³ Department of Biology, University of Vermont, Burlington, VT, USA.
⁴ Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, USA.
⁵ Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, USA.
⁶ Department of Biological Sciences, University of South Florida Saint Petersburg, Saint Petersburg, FL, USA.
⁷ School of Forest Resources and Conservation, University of Florida, Gainesville, FL, USA.
⁸ The Biodesign Center for Fundamental and Applied Microbiomics, School of Life Sciences, Center for Evolution and Medicine, Arizona State University, Tempe, AZ, USA.
⁹ Structural Biology Research Unit, Department of Clinical Laboratory Sciences, University of Cape Town, Cape Town, South Africa.

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 toward 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 viral 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.

Keywords: Arthropod; CRESS DNA; Discovery; Endogenous; Insect; Invertebrate; Replication-associated protein (Rep); Spider; Virus; ssDNA.

Grants and funding

This work was funded through NSF Assembling the Tree of Life Program grant DEB-1239976 to Karyna Rosario and Mya Breitbart. Field work for blow fly collections in the Caribbean was funded through NSF grants DEB-1314749 and DEB-1050253 to Ingi Agnarsson and Greta Binford from the University of Vermont and Lewis & Clark College, respectively (Principal Investigators for Sohath Z Yusseff-Vanegas). Fungus-farming termites and ant samples from Africa were collected in the course of fieldwork funded by NSF grant DEB-1355122 to Corina Tarnita and Robert Pringle from Princeton University (Principal Investigators for Christopher CM Baker). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.