High global diversity of cycloviruses amongst dragonflies Free

Abstract

Members of the family , specifically the genus , were thought to infect only vertebrates; however, members of a sister group under the same family, the proposed genus , have been detected recently in insects. In an effort to explore the diversity of cycloviruses and better understand the evolution of these novel ssDNA viruses, here we present five cycloviruses isolated from three dragonfly species (, and ) collected in Australia, New Zealand and the USA, respectively. The genomes of these five viruses share similar genome structure to other cycloviruses, with a circular ~1.7 kb genome and two major bidirectionally transcribed ORFs. The genomic sequence data gathered during this study were combined with all cyclovirus genomes available in public databases to identify conserved motifs and regulatory elements in the intergenic regions, as well as determine diversity and recombinant regions within their genomes. The genomes reported here represent four different cyclovirus species, three of which are novel. Our results confirm that cycloviruses circulate widely in winged-insect populations; in eight different cyclovirus species identified in dragonflies to date, some of these exhibit a broad geographical distribution. Recombination analysis revealed both intra- and inter-species recombination events amongst cycloviruses, including genomes recovered from disparate sources (e.g. goat meat and human faeces). Similar to other well-characterized circular ssDNA viruses, recombination may play an important role in cyclovirus evolution.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.052654-0
2013-08-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/8/1827.html?itemId=/content/journal/jgv/10.1099/vir.0.052654-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410[PubMed] [CrossRef]
    [Google Scholar]
  2. 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]
  3. Argüello-Astorga G. R., Ruiz-Medrano R. 2001; An iteron-related domain is associated to Motif 1 in the replication proteins of geminiviruses: identification of potential interacting amino acid-base pairs by a comparative approach. Arch Virol 146:1465–1485 [View Article][PubMed]
    [Google Scholar]
  4. Argüello-Astorga G. R., Guevara-González R. G., Herrera-Estrella L. R., Rivera-Bustamante R. F. 1994; Geminivirus replication origins have a group-specific organization of iterative elements: a model for replication. Virology 203:90–100 [View Article][PubMed]
    [Google Scholar]
  5. Biagini P., Bendinelli M., Hino S., Kakkola L., Mankertz A., Niel C., Okamoto H., Raidal S., Teo C. G., Todd D. 2012; Circoviridae. In Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses pp. 343–349 Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. Amsterdam.: Elsevier Academic Press;
    [Google Scholar]
  6. Blinkova O., Victoria J., Li Y., Keele B. F., Sanz C., Ndjango J. B. N., Peeters M., Travis D., Lonsdorf E. V. other authors 2010; Novel circular DNA viruses in stool samples of wild-living chimpanzees. J Gen Virol 91:74–86 [View Article][PubMed]
    [Google Scholar]
  7. Boni M. F., Posada D., Feldman M. W. 2007; An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:1035–1047 [View Article][PubMed]
    [Google Scholar]
  8. Cai L., Ni J., Xia Y., Zi Z., Ning K., Qiu P., Li X., Wang B., Liu Q. other authors 2012; Identification of an emerging recombinant cluster in porcine circovirus type 2. Virus Res 165:95–102 [View Article][PubMed]
    [Google Scholar]
  9. Cheung A. K. 2009; Homologous recombination within the capsid gene of porcine circovirus type 2 subgroup viruses via natural co-infection. Arch Virol 154:531–534 [View Article][PubMed]
    [Google Scholar]
  10. Dayaram A., Opong A., Jäschke A., Hadfield J., Baschiera M., Dobson R. C. J., 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]
  11. 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]
  12. 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]
  13. Ge X., Li J., Peng C., Wu L., Yang X., Wu Y., Zhang Y., Shi Z. 2011; Genetic diversity of novel circular ssDNA viruses in bats in China. J Gen Virol 92:2646–2653 [View Article][PubMed]
    [Google Scholar]
  14. Gibbs M. J., Armstrong J. S., Gibbs A. J. 2000; Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582 [View Article][PubMed]
    [Google Scholar]
  15. 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]
  16. Gutierrez C. 1999; Geminivirus DNA replication. Cell Mol Life Sci 56:313–329 [View Article][PubMed]
    [Google Scholar]
  17. Hanley-Bowdoin L., Settlage S. B., Orozco B. M., Nagar S., Robertson D. 2000; Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit Rev Biochem Mol Biol 35:105–140[PubMed]
    [Google Scholar]
  18. Heyraud-Nitschke F., Schumacher S., Laufs J., Schaefer S., Schell J., Gronenborn B. 1995; Determination of the origin cleavage and joining domain of geminivirus Rep proteins. Nucleic Acids Res 23:910–916 [View Article][PubMed]
    [Google Scholar]
  19. 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]
  20. Julian L., Lorenzo A., Chenuet J. P., Bonzon M., Marchal C., Vignon L., Collings D. A., Walters M., Jackson B., Varsani A. 2012; Evidence of multiple introductions of beak and feather disease virus into the Pacific islands of Nouvelle-Caledonie (New Caledonia). J Gen Virol 93:2466–2472 [View Article][PubMed]
    [Google Scholar]
  21. Julian L., Piasecki T., Chrzastek K., Walters M., Muhire B., Harkins G. W., Martin D. P., Varsani A. 2013; Extensive recombination detected amongst Beak and feather disease virus isolates from breeding facilities in Poland. J Gen Virol 94:1086–1095 [View Article][PubMed]
    [Google Scholar]
  22. Kapoor A., Dubovi E. J., Henriquez-Rivera J. A., Lipkin W. I. 2012; Complete genome sequence of the first canine circovirus. J Virol 86:7018 [View Article][PubMed]
    [Google Scholar]
  23. Kim H. K., Park S. J., Nguyen V. G., Song D. S., Moon H. J., Kang B. K., Park B. K. 2012; Identification of a novel single-stranded, circular DNA virus from bovine stool. J Gen Virol 93:635–639 [View Article][PubMed]
    [Google Scholar]
  24. Laufs J., Traut W., Heyraud F., Matzeit V., Rogers S. G., Schell J., Gronenborn B. 1995; In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus. Proc Natl Acad Sci U S A 92:3879–3883 [View Article][PubMed]
    [Google Scholar]
  25. Lefeuvre P., Lett J. M., Varsani A., Martin D. P. 2009; Widely conserved recombination patterns among single-stranded DNA viruses. J Virol 83:2697–2707 [View Article][PubMed]
    [Google Scholar]
  26. 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 2010; 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]
  27. Li L., Shan T., 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. Londoño A., Riego-Ruiz L., Argüello-Astorga G. R. 2010; DNA-binding specificity determinants of replication proteins encoded by eukaryotic ssDNA viruses are adjacent to widely separated RCR conserved motifs. Arch Virol 155:1033–1046 [View Article][PubMed]
    [Google Scholar]
  29. Martin D., Rybicki E. 2000; rdp: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563 [View Article][PubMed]
    [Google Scholar]
  30. Martin D. P., Posada D., Crandall K. A., Williamson C. 2005; A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21:98–102 [View Article][PubMed]
    [Google Scholar]
  31. Martin D. P., Lemey P., Lott M., Moulton V., Posada D., Lefeuvre P. 2010; rdp3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463 [View Article][PubMed]
    [Google Scholar]
  32. Martin D. P., Biagini P., Lefeuvre P., Golden M., Roumagnac P., Varsani A. 2011; Recombination in eukaryotic single stranded DNA viruses. Viruses 3:1699–1738 [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. Mu C., Yang Q., Zhang Y., Zhou Y., Zhang J., Martin D. P., Xia P., Cui B. 2012; Genetic variation and phylogenetic analysis of porcine circovirus type 2 infections in central China. Virus Genes 45:463–473 [View Article][PubMed]
    [Google Scholar]
  35. Muhire B., Martin D. P., Brown J. K., Navas-Castillo J., Moriones E., Zerbini F. M., Rivera-Bustamante R., Malathi V. G., Briddon R. W., Varsani A. 2013; A genome-wide pairwise-identity-based proposal for the classification of viruses in the genus Mastrevirus (family Geminiviridae). Arch Virol (in press) doi: 10.1007/s00705-012-1601-7 [View Article][PubMed]
    [Google Scholar]
  36. Padidam M., Sawyer S., Fauquet C. M. 1999; Possible emergence of new geminiviruses by frequent recombination. Virology 265:218–225 [View Article][PubMed]
    [Google Scholar]
  37. Padilla-Rodriguez M., Rosario K., Breitbart M. 2013; Novel cyclovirus discovered in the Florida woods cockroach Eurycotis floridana (Walker). Arch Virol (in press) doi: 10.1007/s00705-013-1606-x [View Article][PubMed]
    [Google Scholar]
  38. Phan T. G., Kapusinszky B., Wang C., Rose R. K., Lipton H. L., Delwart E. L. 2011; The fecal viral flora of wild rodents. PLoS Pathog 7:e1002218 [View Article][PubMed]
    [Google Scholar]
  39. Posada D., Crandall K. A. 2001; Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci U S A 98:13757–13762 [View Article][PubMed]
    [Google Scholar]
  40. 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]
  41. Rosario K., Dayaram A., Marinov M., Ware J., Kraberger S., Stainton D., Breitbart M., Varsani A. 2012a; Diverse circular ssDNA viruses discovered in dragonflies (Odonata: Epiprocta). J Gen Virol 93:2668–2681 [View Article][PubMed]
    [Google Scholar]
  42. Rosario K., Duffy S., Breitbart M. 2012b; A field guide to eukaryotic circular single-stranded DNA viruses: insights gained from metagenomics. Arch Virol 157:1851–1871 [View Article][PubMed]
    [Google Scholar]
  43. Rosario K., Padilla-Rodriguez M., Kraberger S., Stainton D., Martin D. P., Breitbart M., Varsani A. 2013; Discovery of a novel mastrevirus and alphasatellite-like circular DNA in dragonflies (Epiprocta) from Puerto Rico. Virus Res 171:231–237 [View Article][PubMed]
    [Google Scholar]
  44. Sikorski A., Argüello-Astorga G. R., Dayaram A., Dobson R. C. J., Varsani A. 2013; Discovery of a novel circular single-stranded DNA virus from porcine faeces. Arch Virol 158:283–289 [View Article][PubMed]
    [Google Scholar]
  45. Smith J. M. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129 [View Article][PubMed]
    [Google Scholar]
  46. Steinfeldt T., Finsterbusch T., Mankertz A. 2001; Rep and Rep’ protein of porcine circovirus type 1 bind to the origin of replication in vitro. Virology 291:152–160 [View Article][PubMed]
    [Google Scholar]
  47. Timchenko T., Katul L., Sano Y., de Kouchkovsky F., Vetten H. J., Gronenborn B. 2000; The master rep concept in nanovirus replication: identification of missing genome components and potential for natural genetic reassortment. Virology 274:189–195 [View Article][PubMed]
    [Google Scholar]
  48. van den Brand J. M. A., van Leeuwen M., Schapendonk C. M., Simon J. H., Haagmans B. L., Osterhaus A. D. M. E., 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]
  49. 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]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.052654-0
Loading
/content/journal/jgv/10.1099/vir.0.052654-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed