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

Research output: Contribution to journalArticle

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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 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.

LanguageEnglish (US)
Article numbere5761
JournalPeerJ
Volume2018
Issue number10
DOIs
StatePublished - Jan 1 2018
Externally publishedYes

Fingerprint

ssDNA viruses
single-stranded DNA
DNA Viruses
Arthropods
Single-Stranded DNA
Invertebrates
Viruses
arthropods
invertebrates
viruses
replicon
genome
Genes
Nanoviridae
Replicon
Circoviridae
Viral Genome
Myriapoda
Hexapoda
Geminiviridae

Keywords

  • Arthropod
  • CRESS DNA
  • Discovery
  • Endogenous
  • Insect
  • Invertebrate
  • Replication-associated protein (Rep)
  • Spider
  • ssDNA
  • Virus

ASJC Scopus subject areas

  • Neuroscience(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Rosario, K., Mettel, K. A., Benner, B. E., Johnson, R., Scott, C., Yusseff-Vanegas, S. Z., ... 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, 2018(10), [e5761]. https://doi.org/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. / Rosario, Karyna; Mettel, Kaitlin A.; Benner, Bayleigh E.; Johnson, Ryan; Scott, Catherine; Yusseff-Vanegas, Sohath Z.; Baker, Christopher C.M.; Cassill, Deby L.; Storer, Caroline; Varsani, Arvind; Breitbart, Mya.

In: PeerJ, Vol. 2018, No. 10, e5761, 01.01.2018.

Research output: Contribution to journalArticle

Rosario, K, Mettel, KA, Benner, BE, Johnson, R, Scott, C, Yusseff-Vanegas, SZ, Baker, CCM, 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, vol. 2018, no. 10, e5761. https://doi.org/10.7717/peerj.5761
Rosario, Karyna ; Mettel, Kaitlin A. ; Benner, Bayleigh E. ; Johnson, Ryan ; Scott, Catherine ; Yusseff-Vanegas, Sohath Z. ; Baker, Christopher C.M. ; Cassill, Deby L. ; Storer, Caroline ; Varsani, Arvind ; Breitbart, Mya. / Virus discovery in all three major lineages of terrestrial arthropods highlights the diversity of single-stranded DNA viruses associated with invertebrates. In: PeerJ. 2018 ; Vol. 2018, No. 10.
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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 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.",
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