1887

Abstract

Pigeon circovirus (PiCV) has a ~2 kb genome circular ssDNA genome. All but one of the known PiCV isolates have been found infecting pigeons in various parts of the world. In this study, we screened 324 swab and tissue samples from Polish pigeons and recovered 30 complete genomes, 16 of which came from birds displaying no obvious pathology. Together with 17 other publicly available PiCV complete genomes sampled throughout the Northern Hemisphere and Australia, we find that PiCV displays a similar degree of genetic diversity to that of the related psittacine-infecting circovirus species, beak and feather disease virus (BFDV). We show that, as is the case with its pathology and epidemiology, PiCV also displays patterns of recombination, genomic secondary structure and natural selection that are generally very similar to those of BFDV. It is likely that breeding facilities play a significant role in the emergence of new recombinant PiCV variants and given that ~50 % of the domestic pigeon population is infected subclinically, all pigeon breeding stocks should be screened routinely for this virus.

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2014-06-01
2022-01-20
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References

  1. Abadie J., Nguyen F., Groizeleau C., Amenna N., Fernandez B., Guereaud C., Guigand L., Robart P., Lefebvre B., Wyers M. 2001; Pigeon circovirus infection: pathological observations and suggested pathogenesis. Avian Pathol 30:149–158 [View Article][PubMed]
    [Google Scholar]
  2. Allan G., Krakowka S., Ellis J., Charreyre C. 2012; Discovery and evolving history of two genetically related but phenotypically different viruses, porcine circoviruses 1 and 2. Virus Res 164:4–9 [View Article][PubMed]
    [Google Scholar]
  3. Bennett S. N., Holmes E. C., Chirivella M., Rodriguez D. M., Beltran M., Vorndam V., Gubler D. J., McMillan W. O. 2006; Molecular evolution of dengue 2 virus in Puerto Rico: positive selection in the viral envelope accompanies clade reintroduction. J Gen Virol 87:885–893 [View Article][PubMed]
    [Google Scholar]
  4. Biagini P., Bendinelli M., Hino S., Kakkola L., Mankertz A., Niel C., Okamoto H., Raidal S., Teo C. G., Todd D. 2012; Family - Circoviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses pp. 343–349 Edited by King A. M. Q., Lefkowitz E., Adams M. J., Carstens E. B. San Diego, CA: Elsevier;
    [Google Scholar]
  5. Blanchard P., Mahé D., Cariolet R., Keranflec’h A., Baudouard M. A., Cordioli P., Albina E., Jestin A. 2003; Protection of swine against post-weaning multisystemic wasting syndrome (PMWS) by porcine circovirus type 2 (PCV2) proteins. Vaccine 21:4565–4575 [View Article][PubMed]
    [Google Scholar]
  6. 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]
  7. 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]
  8. Coletti M., Franciosini M. P., Asdrubali G., Passamonti F. 2000; Atrophy of the primary lymphoid organs of meat pigeons in Italy associated with circoviruslike particles in the bursa of Fabricius. Avian Dis 44:454–459 [View Article][PubMed]
    [Google Scholar]
  9. Cságola A., Lorincz M., Tombácz K., Wladár Z., Kovács E., Tuboly T. 2012; Genetic diversity of pigeon circovirus in Hungary. Virus Genes 44:75–79 [View Article][PubMed]
    [Google Scholar]
  10. Duchatel J. P., Todd D., Curry A., Smyth J. A., Bustin J. C., Vindevogel H. 2005; New data on the transmission of pigeon circovirus. Vet Rec 157:413–415[PubMed] [CrossRef]
    [Google Scholar]
  11. Duchatel J. P., Todd D., Smyth J. A., Bustin J. C., Vindevogel H. 2006; Observations on detection, excretion and transmission of pigeon circovirus in adult, young and embryonic pigeons. Avian Pathol 35:30–34 [View Article][PubMed]
    [Google Scholar]
  12. Duffy S., Holmes E. C. 2008; Phylogenetic evidence for rapid rates of molecular evolution in the single-stranded DNA begomovirus tomato yellow leaf curl virus. J Virol 82:957–965 [View Article][PubMed]
    [Google Scholar]
  13. Duffy S., Holmes E. C. 2009; Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses. J Gen Virol 90:1539–1547 [View Article][PubMed]
    [Google Scholar]
  14. Duffy S., Shackelton L. A., Holmes E. C. 2008; Rates of evolutionary change in viruses: patterns and determinants. Nat Rev Genet 9:267–276 [View Article][PubMed]
    [Google Scholar]
  15. 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]
  16. Esteban D. J., Hutchinson A. P. 2011; Genes in the terminal regions of orthopoxvirus genomes experience adaptive molecular evolution. BMC Genomics 12:261 [View Article][PubMed]
    [Google Scholar]
  17. Faurez F., Dory D., Grasland B., Jestin A. 2009; Replication of porcine circoviruses. Virol J 6:60 [CrossRef]
    [Google Scholar]
  18. Finsterbusch T., Steinfeldt T., Doberstein K., Rödner C., Mankertz A. 2009; Interaction of the replication proteins and the capsid protein of porcine circovirus type 1 and 2 with host proteins. Virology 386:122–131 [View Article][PubMed]
    [Google Scholar]
  19. Firth C., Charleston M. A., Duffy S., Shapiro B., Holmes E. C. 2009; Insights into the evolutionary history of an emerging livestock pathogen: porcine circovirus 2. J Virol 83:12813–12821 [View Article][PubMed]
    [Google Scholar]
  20. Freick M., Müller H., Raue R. 2008; Rapid detection of pigeon herpesvirus, fowl adenovirus and pigeon circovirus in young racing pigeons by multiplex PCR. J Virol Methods 148:226–231 [View Article][PubMed]
    [Google Scholar]
  21. 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]
  22. Grau-Roma L., Fraile L., Segalés J. 2011; Recent advances in the epidemiology, diagnosis and control of diseases caused by porcine circovirus type 2. Vet J 187:23–32 [View Article][PubMed]
    [Google Scholar]
  23. Grigoras I., Timchenko T., Grande-Pérez A., Katul L., Vetten H. J., Gronenborn B. 2010; High variability and rapid evolution of a nanovirus. J Virol 84:9105–9117 [View Article][PubMed]
    [Google Scholar]
  24. 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]
  25. Harkins G. W., Delport W., Duffy S., Wood N., Monjane A. L., Owor B. E., Donaldson L., Saumtally S., Triton G. other authors 2009; Experimental evidence indicating that mastreviruses probably did not co-diverge with their hosts. Virol J 6:104 [View Article][PubMed]
    [Google Scholar]
  26. Harkins G. W., Martin D. P., Christoffels A., Varsani A. 2014; Towards inferring the global movement of beak and feather disease virus. Virology 450-451:24–33 [View Article][PubMed]
    [Google Scholar]
  27. Heath L., Martin D. P., Warburton L., Perrin M., Horsfield W., Kingsley C., Rybicki E. P., Williamson A. L. 2004; Evidence of unique genotypes of beak and feather disease virus in southern Africa. J Virol 78:9277–9284 [View Article][PubMed]
    [Google Scholar]
  28. Heath L., Williamson A. L., Rybicki E. P. 2006; The capsid protein of beak and feather disease virus binds to the viral DNA and is responsible for transporting the replication-associated protein into the nucleus. J Virol 80:7219–7225 [CrossRef]
    [Google Scholar]
  29. 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]
  30. Julian L., Piasecki T., Chrzastek K., Walters M., Muhire B., Harkins G. W., Martin D. P., Varsani A. 2013; Extensive recombination detected among beak and feather disease virus isolates from breeding facilities in Poland. J Gen Virol 94:1086–1095 [View Article][PubMed]
    [Google Scholar]
  31. Katoh K., Standley D. M. 2013; mafft multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780 [View Article][PubMed]
    [Google Scholar]
  32. Kosakovsky Pond S. L., Posada D., Gravenor M. B., Woelk C. H., Frost S. D. 2006; gard: a genetic algorithm for recombination detection. Bioinformatics 22:3096–3098 [View Article][PubMed]
    [Google Scholar]
  33. Krapez U., Slavec B., Steyer A. F., Pintaric S., Dobeic M., Rojs O. Z., Dovc A. 2012; Prevalence of pigeon circovirus infections in feral pigeons in Ljubljana, Slovenia. Avian Dis 56:432–435 [View Article][PubMed]
    [Google Scholar]
  34. 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]
  35. Lefeuvre P., Martin D. P., Harkins G., Lemey P., Gray A. J., Meredith S., Lakay F., Monjane A., Lett J. M. other authors 2010; The spread of tomato yellow leaf curl virus from the Middle East to the world. PLoS Pathog 6:e1001164 [View Article][PubMed]
    [Google Scholar]
  36. Mankertz A., Hattermann K., Ehlers B., Soike D. 2000; Cloning and sequencing of columbid circovirus (CoCV), a new circovirus from pigeons. Arch Virol 145:2469–2479 [View Article][PubMed]
    [Google Scholar]
  37. Markham N. R., Zuker M. 2008; UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 453:3–31 [View Article][PubMed]
    [Google Scholar]
  38. Martin D., Rybicki E. 2000; rdp: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563 [View Article][PubMed]
    [Google Scholar]
  39. 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]
  40. 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]
  41. 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]
  42. Meng X. J. 2012; Spread like a wildfire – the omnipresence of porcine circovirus type 2 (PCV2) and its ever-expanding association with diseases in pigs. Virus Res 164:1–3 [View Article][PubMed]
    [Google Scholar]
  43. Moulton V., Zuker M., Steel M., Pointon R., Penny D. 2000; Metrics on RNA secondary structures. J Comput Biol 7:277–292 [View Article][PubMed]
    [Google Scholar]
  44. 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 158:1411–1424 [View Article][PubMed]
    [Google Scholar]
  45. Muhire B. M., Golden M., Murrell B., Lefeuvre P., Lett J. M., Gray A., Poon A. Y., Ngandu N. K., Semegni Y. other authors 2014; Evidence of pervasive biologically functional secondary-structures within the genomes of eukaryotic single-stranded DNA viruses. J Virol 88:1972–1989 [View Article][PubMed]
    [Google Scholar]
  46. Murrell B., Wertheim J. O., Moola S., Weighill T., Scheffler K., Kosakovsky Pond S. L. 2012; Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764 [View Article][PubMed]
    [Google Scholar]
  47. Murrell B., Moola S., Mabona A., Weighill T., Sheward D., Kosakovsky Pond S. L., Scheffler K. 2013; fubar: a fast, unconstrained Bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205 [View Article][PubMed]
    [Google Scholar]
  48. 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]
  49. Paré J. A., Brash M. L., Hunter D. B., Hampson R. J. 1999; Observations on pigeon circovirus infection in Ontario. Can Vet J 40:659–662[PubMed]
    [Google Scholar]
  50. Patterson A. R., Opriessnig T. 2010; Epidemiology and horizontal transmission of porcine circovirus type 2 (PCV2). Anim Health Res Rev 11:217–234 [View Article][PubMed]
    [Google Scholar]
  51. Pogranichnyy R. M., Yoon K. J., Harms P. A., Swenson S. L., Zimmerman J. J., Sorden S. D. 2000; Characterization of immune response of young pigs to porcine circovirus type 2 infection. Viral Immunol 13:143–153 [View Article][PubMed]
    [Google Scholar]
  52. Posada D. 2009; Selection of models of DNA evolution with jModelTest. Methods Mol Biol 537:93–112 [View Article][PubMed]
    [Google Scholar]
  53. 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]
  54. Rahaus M., Desloges N., Probst S., Loebbert B., Lanttermann W., Wolff M. H. 2008; Detection of beak and feather disease virus DNA in embryonated eggs of psittacine birds. Vet Med (Praha) 53:53–58
    [Google Scholar]
  55. Raue R., Schmidt V., Freick M., Reinhardt B., Johne R., Kamphausen L., Kaleta E. F., Müller H., Krautwald-Junghanns M.-E. 2005; A disease complex associated with pigeon circovirus infection: young pigeon disease syndrome. Avian Pathol 34:418–425 [View Article][PubMed]
    [Google Scholar]
  56. Rigby M. A., Holmes E. C., Pistello M., Mackay A., Leigh Brown A. J., Neil J. C. 1993; Evolution of structural proteins of feline immunodeficiency virus: molecular epidemiology and evidence of selection for change. J Gen Virol 74:425–436 [View Article][PubMed]
    [Google Scholar]
  57. Segalés J., Kekarainen T., Cortey M. 2013; The natural history of porcine circovirus type 2: from an inoffensive virus to a devastating swine disease?. Vet Microbiol 165:13–20 [View Article][PubMed]
    [Google Scholar]
  58. Seibert S. A., Howell C. Y., Hughes M. K., Hughes A. L. 1995; Natural selection on the gag, pol, and env genes of human immunodeficiency virus 1 (HIV-1). Mol Biol Evol 12:803–813[PubMed]
    [Google Scholar]
  59. Smith J. M. 1992; Analyzing the mosaic structure of genes. J Mol Evol 34:126–129 [View Article][PubMed]
    [Google Scholar]
  60. Stenzel T. A., Pestka D., Tykałowski B., Śmiałek M., Koncicki A. 2012; Epidemiological investigation of selected pigeon viral infections in Poland. Vet Rec 171:562 [View Article][PubMed]
    [Google Scholar]
  61. 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]
  62. Todd D., Weston J. H., Soike D., Smyth J. A. 2001; Genome sequence determinations and analyses of novel circoviruses from goose and pigeon. Virology 286:354–362 [View Article][PubMed]
    [Google Scholar]
  63. Todd D., Fringuelli E., Scott A. N., Borghmans B. J., Duchatel J. P., Shivaprasad H. L., Raidal S. R., Abadie J. X., Franciosini M. P., Smyth J. A. 2008; Sequence comparison of pigeon circoviruses. Res Vet Sci 84:311–319 [View Article][PubMed]
    [Google Scholar]
  64. 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]
  65. Woods L. W., Latimer K. S. 2000; Circovirus infection of nonpsittacine birds. J Avian Med Surg 14:154–163 [View Article]
    [Google Scholar]
  66. Woods L. W., Latimer K. S., Barr B. C., Niagro F. D., Campagnoli R. P., Nordhausen R. W., Castro A. E. 1993; Circovirus-like infection in a pigeon. J Vet Diagn Invest 5:609–612 [View Article][PubMed]
    [Google Scholar]
  67. Woods L. W., Latimer K. S., Niagro F. D., Riddell C., Crowley A. M., Anderson M. L., Daft B. M., Moore J. D., Campagnoli R. P., Nordhausen R. W. 1994; A retrospective study of circovirus infection in pigeons: nine cases (1986–1993). J Vet Diagn Invest 6:156–164 [View Article][PubMed]
    [Google Scholar]
  68. Zhang Z., Lu C., Wang Y., Wang S., Dai D., Chen Z., Fan H. 2011; Molecular characterization and epidemiological investigation of Pigeon circovirus isolated in eastern China. J Vet Diagn Invest 23:665–672 [View Article][PubMed]
    [Google Scholar]
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