Skip to content
1887

Journal of General Virology header logo Journal of General Virology

Volume 93, Issue 12

Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta) Free

Abstract

Viruses with circular ssDNA genomes that encode a replication initiator protein (Rep) are among the smallest viruses known to infect both eukaryotic and prokaryotic organisms. In the past few years an overwhelming diversity of novel circular Rep-encoding ssDNA (CRESS-DNA) viruses has been unearthed from various hosts and environmental sources. Since there is limited information regarding CRESS-DNA viruses in invertebrates, this study explored the diversity of CRESS-DNA viruses circulating among insect populations by _targeting dragonflies (Epiprocta), top insect predators that accumulate viruses from their insect prey over space and time. Using degenerate PCR and rolling circle amplification coupled with restriction digestion, 17 CRESS-DNA viral genomes were recovered from eight different dragonfly species collected in tropical and temperate regions. Nine of the genomes are similar to cycloviruses and represent five species within this genus, suggesting that cycloviruses are commonly associated with insects. Three of the CRESS-DNA viruses share conserved genomic features with recently described viruses similar to the mycovirus Sclerotinia sclerotiorum hypovirulence-associated DNA virus 1, leading to the proposal of the genus Gemycircularvirus. The remaining viruses are divergent species representing four novel CRESS-DNA viral genera, including a gokushovirus-like prokaryotic virus (microphage) and three eukaryotic viruses with Reps similar to circoviruses. The novelty of CRESS-DNA viruses identified in dragonflies using simple molecular techniques indicates that there is an unprecedented diversity of ssDNA viruses among insect populations.

  • Received:
  • Accepted:
  • Published Online:
© 2012 SGM
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.045948-0
2012-12-01
2024-12-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/12/2668.html?itemId=/content/journal/jgv/10.1099/vir.0.045948-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J. H., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [View Article][PubMed]
     [Google Scholar]
  2. Angly F. E., Felts B., Breitbart M., Salamon P., Edwards R. A., Carlson C., Chan A. M., Haynes M., Kelley S.other authors 2006; The marine viromes of four oceanic regions. PLoS Biol 4:e368 [View Article][PubMed]
     [Google Scholar]
  3. Anisimova M., Gascuel O. 2006; Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol 55:539–552 [View Article][PubMed]
     [Google Scholar]
  4. Brentlinger K. L., Hafenstein S., Novak C. R., Fane B. A., Borgon R., McKenna R., Agbandje-McKenna M. 2002; Microviridae, a family divided: isolation, characterization, and genome sequence of phiMH2K, a bacteriophage of the obligate intracellular parasitic bacterium Bdellovibrio bacteriovorus. J Bacteriol 184:1089–1094 [View Article][PubMed]
     [Google Scholar]
  5. Cherwa, J. E. & Fane, B. A. (2012). Microviridae In Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses, pp. 385–393. Edited by King, A. M. Q., Adams, M. J., Carsten, E. B. & Lefkowitz, E. J. San Diego, CA: Elsevier Academic Press
  6. Dayaram A., Opong A., Jäschke A., Hadfield J., Baschiera M., Dobson R. C., Offei S. K., Shepherd D. N., Martin D. P., Varsani A. 2012; Molecular characterisation of a novel cassava associated circular ssDNA virus. Virus Res 166:130–135 [View Article][PubMed]
     [Google Scholar]
  7. Delwart E., Li L. 2012; Rapidly expanding genetic diversity and host range of the Circoviridae viral family and other Rep encoding small circular ssDNA genomes. Virus Res 164:114–121 [View Article][PubMed]
     [Google Scholar]
  8. Desnues C., Rodriguez-Brito B., Rayhawk S., Kelley S., Tran T., Haynes M., Liu H., Furlan M., Wegley L.other authors 2008; Biodiversity and biogeography of phages in modern stromatolites and thrombolites. Nature 452:340–343 [View Article][PubMed]
     [Google Scholar]
  9. Diemer G. S., Stedman K. M. 2012; A novel virus genome discovered in an extreme environment suggests recombination between unrelated groups of RNA and DNA viruses. Biol Direct 7:13 [View Article][PubMed]
     [Google Scholar]
  10. Dowd P. F. 1992; Insect fungal symbionts: a promising source of detoxifying enzymes. J Ind Microbiol 9:149–161 [View Article]
     [Google Scholar]
  11. Edgar R. C. 2004; muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797 [View Article][PubMed]
     [Google Scholar]
  12. Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. 2005 Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses San Diego, CA: Academic Press;
     [Google Scholar]
  13. FDA 2011; The Food Defect Action Levels. In Defect Levels Handbook Edited by U. S. F. a. D. Administration http://www.fda.gov/Food/GuidanceComplianceRegulatoryInformation/GuidanceDocuments/Sanitation/ucm056174.htm
     [Google Scholar]
  14. Fujii R., Kitaoka M., Hayashi K. 2006; Error-prone rolling circle amplification: the simplest random mutagenesis protocol. Nat Protoc 1:2493–2497 [View Article][PubMed]
     [Google Scholar]
  15. Ge X. Y., Li J. L., Peng C., Wu L. J., Yang X. L., Wu Y. Q., Zhang Y. Z., Shi Z. L. 2011; Genetic diversity of novel circular ssDNA viruses in bats in China. J Gen Virol 92:2646–2653 [View Article][PubMed]
     [Google Scholar]
  16. Guindon S., Dufayard J.-F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010; New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321 [View Article][PubMed]
     [Google Scholar]
  17. Gutierrez C. 1999; Geminivirus DNA replication. Cell Mol Life Sci 56:313–329 [View Article][PubMed]
     [Google Scholar]
  18. Hadfield J., Linderme D., Shepherd D. N., Bezuidenhout M., Lefeuvre P., Martin D. P., Varsani A. 2011; Complete genome sequence of a dahlia common mosaic virus isolate from New Zealand. Arch Virol 156:2297–2301 [View Article][PubMed]
     [Google Scholar]
  19. Haible D., Kober S., Jeske H. 2006; Rolling circle amplification revolutionizes diagnosis and genomics of geminiviruses. J Virol Methods 135:9–16 [View Article][PubMed]
     [Google Scholar]
  20. Hajek A. E., St. Leger R. J. 1994; Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39:293–322 [View Article]
     [Google Scholar]
  21. Hogenhout S. A., Ammar D., Whitfield A. E., Redinbaugh M. G. 2008; Insect vector interactions with persistently transmitted viruses. Annu Rev Phytopathol 46:327–359 [View Article][PubMed]
     [Google Scholar]
  22. Ilyina T. V., Koonin E. V. 1992; Conserved sequence motifs in the initiator proteins for rolling circle DNA replication encoded by diverse replicons from eubacteria, eucaryotes and archaebacteria. Nucleic Acids Res 20:3279–3285 [View Article][PubMed]
     [Google Scholar]
  23. Kim K. H., Chang H. W., Nam Y. D., Roh S. W., Kim M. S., Sung Y., Jeon C. O., Oh H. M., Bae J. W. 2008; Amplification of uncultured single-stranded DNA viruses from rice paddy soil. Appl Environ Microbiol 74:5975–5985 [View Article][PubMed]
     [Google Scholar]
  24. Krupovic M., Forterre P. 2011; Microviridae goes temperate: microvirus-related proviruses reside in the genomes of Bacteroidetes. PLoS ONE 6:e19893 [View Article][PubMed]
     [Google Scholar]
  25. Li L., Kapoor A., Slikas B., Bamidele O. S., Wang C., Shaukat S., Masroor M. A., Wilson M. L., Ndjango J.-B. N.other authors 2010a; Multiple diverse circoviruses infect farm animals and are commonly found in human and chimpanzee feces. J Virol 84:1674–1682 [View Article][PubMed]
     [Google Scholar]
  26. Li L., Victoria J. G., Wang C., Jones M., Fellers G. M., Kunz T. H., Delwart E. 2010b; Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. J Virol 84:6955–6965 [View Article][PubMed]
     [Google Scholar]
  27. Li L. L., Shan T. L., Soji O. B., Alam M. M., Kunz T. H., Zaidi S. Z., Delwart E. 2011; Possible cross-species transmission of circoviruses and cycloviruses among farm animals. J Gen Virol 92:768–772 [View Article][PubMed]
     [Google Scholar]
  28. Liu B. L., Everson J. S., Fane B., Giannikopoulou P., Vretou E., Lambden P. R., Clarke I. N. 2000; Molecular characterization of a bacteriophage (Chp2) from Chlamydia psittaci. J Virol 74:3464–3469 [View Article][PubMed]
     [Google Scholar]
  29. Liu H. Q., Fu Y. P., Li B., Yu X., Xie J. T., Cheng J. S., Ghabrial S. A., Li G. Q., Yi X. H., Jiang D. H. 2011; Widespread horizontal gene transfer from circular single-stranded DNA viruses to eukaryotic genomes. BMC Evol Biol 11:276 [View Article][PubMed]
     [Google Scholar]
  30. Lőrincz M., Cságola A., Farkas S. L., Székely C., Tuboly T. 2011; First detection and analysis of a fish circovirus. J Gen Virol 92:1817–1821 [View Article][PubMed]
     [Google Scholar]
  31. Lőrincz M., Dán A., Láng M., Csaba G., Tóth A. G., Székely C., Cságola A., Tuboly T. 2012; Novel circovirus in European catfish (Silurus glanis). Arch Virol 157:1173–1176 [View Article][PubMed]
     [Google Scholar]
  32. Marchler-Bauer A., Lu S., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C.other authors 2011; CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39:Database issueD225–D229 [View Article][PubMed]
     [Google Scholar]
  33. Massaro M., Ortiz-Catedral L., Julian L., Galbraith J. A., Kurenbach B., Kearvell J., Kemp J., van Hal J., Elkington S.other authors 2012; Molecular characterisation of beak and feather disease virus (BFDV) in New Zealand and its implications for managing an infectious disease. Arch Virol 157:1651–1663 [View Article][PubMed]
     [Google Scholar]
  34. Nash T. E., Dallas M. B., Reyes M. I., Buhrman G. K., Ascencio-Ibañez J. T., Hanley-Bowdoin L. 2011; Functional analysis of a novel motif conserved across geminivirus Rep proteins. J Virol 85:1182–1192 [View Article][PubMed]
     [Google Scholar]
  35. Ng T. F. F., Manire C., Borrowman K., Langer T., Ehrhart L., Breitbart M. 2009a; Discovery of a novel single-stranded DNA virus from a sea turtle fibropapilloma by using viral metagenomics. J Virol 83:2500–2509 [View Article][PubMed]
     [Google Scholar]
  36. Ng T. F. F., Suedmeyer W. K., Wheeler E., Gulland F., Breitbart M. 2009b; Novel anellovirus discovered from a mortality event of captive California sea lions. J Gen Virol 90:1256–1261 [View Article][PubMed]
     [Google Scholar]
  37. Ng T. F., Duffy S., Polston J. E., Bixby E., Vallad G. E., Breitbart M. 2011a; Exploring the diversity of plant DNA viruses and their satellites using vector-enabled metagenomics on whiteflies. PLoS ONE 6:e19050 [View Article][PubMed]
     [Google Scholar]
  38. Ng T. F. F., Willner D. L., Lim Y. W., Schmieder R., Chau B., Nilsson C., Anthony S., Ruan Y. J., Rohwer F., Breitbart M. 2011b; Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS ONE 6:e20579 [View Article][PubMed]
     [Google Scholar]
  39. Niagro F. D., Forsthoefel A. N., Lawther R. P., Kamalanathan L., Ritchie B. W., Latimer K. S., Lukert P. D. 1998; Beak and feather disease virus and porcine circovirus genomes: intermediates between the geminiviruses and plant circoviruses. Arch Virol 143:1723–1744 [View Article][PubMed]
     [Google Scholar]
  40. Owor B. E., Shepherd D. N., Taylor N. J., Edema R., Monjane A. L., Thomson J. A., Martin D. P., Varsani A. 2007; Successful application of FTA Classic Card technology and use of bacteriophage phi29 DNA polymerase for large-scale field sampling and cloning of complete maize streak virus genomes. J Virol Methods 140:100–105 [View Article][PubMed]
     [Google Scholar]
  41. Piasecki T., Kurenbach B., Chrząstek K., Bednarek K., Kraberger S., Martin D. P., Varsani A. 2012; Molecular characterisation of an avihepadnavirus isolated from Psittacula krameri (ring-necked parrot). Arch Virol 157:585–590 [View Article][PubMed]
     [Google Scholar]
  42. Punta M., Coggill P. C., Eberhardt R. Y., Mistry J., Tate J., Boursnell C., Pang N., Forslund K., Ceric G.other authors 2012; The Pfam protein families database. Nucleic Acids Res 40:Database issueD290–D301 [View Article][PubMed]
     [Google Scholar]
  43. Renaudin J., Bové J. M. 1994; Spv1 and Spv4, spiroplasma viruses with circular, single-stranded DNA genomes, and their contribution to the molecular biology of spiroplasmas. In Advances in Virus Research pp. 429–463 Edited by Karl Maramorosch F. A. M., Aaron J. S. Salt Lake City, UT: Academic Press; [View Article]
     [Google Scholar]
  44. Rosario K., Breitbart M. 2011; Exploring the viral world through metagenomics. Curr Opin Virol 1:289–297 [View Article][PubMed]
     [Google Scholar]
  45. Rosario K., Nilsson C., Lim Y. W., Ruan Y., Breitbart M. 2009; Metagenomic analysis of viruses in reclaimed water. Environ Microbiol 11:2806–2820 [View Article][PubMed]
     [Google Scholar]
  46. Rosario K., Marinov M., Stainton D., Kraberger S., Wiltshire E. J., Collings D. A., Walters M., Martin D. P., Breitbart M., Varsani A. 2011; Dragonfly cyclovirus, a novel single-stranded DNA virus discovered in dragonflies (Odonata: Anisoptera). J Gen Virol 92:1302–1308 [View Article][PubMed]
     [Google Scholar]
  47. Rosario K., Duffy S., Breitbart M. 2012; A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 157:1851–1871 [View Article]
     [Google Scholar]
  48. Shepherd D. N., Martin D. P., Lefeuvre P., Monjane A. L., Owor B. E., Rybicki E. P., Varsani A. 2008; A protocol for the rapid isolation of full geminivirus genomes from dried plant tissue. J Virol Methods 149:97–102 [View Article][PubMed]
     [Google Scholar]
  49. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
     [Google Scholar]
  50. Tucker K. P., Parsons R., Symonds E. M., Breitbart M. 2011; Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean. ISME J 5:822–830 [View Article][PubMed]
     [Google Scholar]
  51. van den Brand J. M., van Leeuwen M., Schapendonk C. M., Simon J. H., Haagmans B. L., Osterhaus A. D., Smits S. L. 2012; Metagenomic analysis of the viral flora of pine marten and European badger feces. J Virol 86:2360–2365 [View Article][PubMed]
     [Google Scholar]
  52. Varsani A., Regnard G. L., Bragg R., Hitzeroth I. I., Rybicki E. P. 2011; Global genetic diversity and geographical and host-species distribution of beak and feather disease virus isolates. J Gen Virol 92:752–767 [View Article][PubMed]
     [Google Scholar]
  53. Yoon H. S., Price D. C., Stepanauskas R., Rajah V. D., Sieracki M. E., Wilson W. H., Yang E. C., Duffy S., Bhattacharya D. 2011; Single-cell genomics reveals organismal interactions in uncultivated marine protists. Science 332:714–717 [View Article][PubMed]
     [Google Scholar]
  54. Yu X., Li B., Fu Y. P., Jiang D. H., Ghabrial S. A., Li G. Q., Peng Y. L., Xie J. T., Cheng J. S.other authors 2010; A geminivirus-related DNA mycovirus that confers hypovirulence to a plant pathogenic fungus. Proc Natl Acad Sci U S A 107:8387–8392 [View Article][PubMed]
     [Google Scholar]
/content/journal/jgv/10.1099/vir.0.045948-0
Loading
Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta)
J. Gen. Virol. 93, 2668 (2012); https://doi.org/10.1099/vir.0.045948-0
/content/journal/jgv/10.1099/vir.0.045948-0
/content/journal/jgv/10.1099/vir.0.045948-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error
  NODES
admin 1
INTERN 5
Note 1