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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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.
Cite this as
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 PeerJ Preprints 6:e27093v1 https://doi.org/10.7287/peerj.preprints.27093v1note This preprint is not peer-reviewed. You may wish to reference the subsequent peer-reviewed version of this article.
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This is a submission to PeerJ for review.
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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.
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).
Additional Information
Competing Interests
Mya Breitbart is an Academic Editor for PeerJ. The authors declare that they have no competing interests.
Author Contributions
Karyna Rosario conceived and designed the experiments, performed the experiments, analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the paper, approved the final draft.
Kaitlin A Mettel performed the experiments, approved the final draft.
Bayleigh E Benner performed the experiments, approved the final draft.
Ryan Johnson performed the experiments, approved the final draft.
Catherine Scott contributed reagents/materials/analysis tools, approved the final draft.
Sohath Z Yusseff-Vanegas contributed reagents/materials/analysis tools, approved the final draft.
Christopher CM Baker contributed reagents/materials/analysis tools, approved the final draft.
Deby L Cassill contributed reagents/materials/analysis tools, approved the final draft.
Caroline Storer contributed reagents/materials/analysis tools, approved the final draft.
Arvind Varsani analyzed the data, prepared figures and/or tables, approved the final draft.
Mya Breitbart conceived and designed the experiments, analyzed the data, prepared figures and/or tables, approved the final draft.
DNA Deposition
The following information was supplied regarding the deposition of DNA sequences:
The genomes and replicons described here are accessible via GenBank accession numbers: MG917674 to MG917677 and MH545497 to MH545543.
Data Deposition
The following information was supplied regarding data availability:
The research in this article did not generate any data or code beyond the genome sequences deposited into Genbank.
Funding
This work was funded through NSF Assembling the Tree of Life Program grant DEB-1239976 to K. Rosario and M. Breitbart. Field work for blow fly collections in the Caribbean was funded through NSF grants DEB-1314749 and DEB-1050253 to I. Agnarsson and G. Binford from the University of Vermont and Lewis & Clark College, respectively. Fungus-farming termites and ant samples from Africa were collected in the course of fieldwork funded by NSF grant DEB-1355122 to C. Tarnita and R. Pringle from Princeton University. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
