1887

Abstract

The close interactions of dogs with humans and surrounding wildlife provide frequent opportunities for cross-species virus transmissions. In order to initiate an unbiased characterization of the eukaryotic viruses in the gut of dogs, this study used deep sequencing of partially purified viral capsid-protected nucleic acids from the faeces of 18 diarrhoeic dogs. Known canine parvoviruses, coronaviruses and rotaviruses were identified, and the genomes of the first reported canine kobuvirus and sapovirus were characterized. Canine kobuvirus, the first sequenced canine picornavirus and the closest genetic relative of the diarrhoea-causing human Aichi virus, was detected at high frequency in the faeces of both healthy and diarrhoeic dogs. Canine sapovirus constituted a novel genogroup within the genus , a group of viruses also associated with human and animal diarrhoea. These results highlight the high frequency of new virus detection possible even in extensively studied animal species using metagenomics approaches, and provide viral genomes for further disease-association studies.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.034611-0
2011-11-01
2019-10-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/11/2534.html?itemId=/content/journal/jgv/10.1099/vir.0.034611-0&mimeType=html&fmt=ahah

References

  1. Allander T. , Emerson S. U. , Engle R. E. , Purcell R. H. , Bukh J. . ( 2001; ). A virus discovery method incorporating DNase treatment and its application to the identification of two bovine parvovirus species. . Proc Natl Acad Sci U S A 98:, 11609–11614. [CrossRef] [PubMed]
    [Google Scholar]
  2. Barry A. F. , Alfieri A. F. , Alfieri A. A. . ( 2008; ). High genetic diversity in RdRp gene of Brazilian porcine sapovirus strains. . Vet Microbiol 131:, 185–191. [CrossRef] [PubMed]
    [Google Scholar]
  3. Buonavoglia C. , Martella V. . ( 2007; ). Canine respiratory viruses. . Vet Res 38:, 355–373. [CrossRef] [PubMed]
    [Google Scholar]
  4. Chevreux, B. (2005). mira: an automated genome and EST assembler. PhD thesis, Ruprecht-Karls University, Heidelberg, Germany.
  5. Chiba S. , Sakuma Y. , Kogasaka R. , Akihara M. , Horino K. , Nakao T. , Fukui S. . ( 1979; ). An outbreak of gastroenteritis associated with calicivirus in an infant home. . J Med Virol 4:, 249–254. [CrossRef] [PubMed]
    [Google Scholar]
  6. Cook G. C. . ( 1989; ). Canine-associated zoonoses: an unacceptable hazard to human health. . Q J Med 70:, 5–26.[PubMed]
    [Google Scholar]
  7. Coppinger R. , Coppinger L. . ( 2001; ). Dogs: a Startling New Understanding of Canine Origin, Behavior & Evolution. New York:: Scribner;.
    [Google Scholar]
  8. Decaro N. , Buonavoglia C. . ( 2008; ). An update on canine coronaviruses: viral evolution and pathobiology. . Vet Microbiol 132:, 221–234. [CrossRef] [PubMed]
    [Google Scholar]
  9. Decaro N. , Martella V. , Buonavoglia C. . ( 2008; ). Canine adenoviruses and herpesvirus. . Vet Clin North Am Small Anim Pract 38:, 799–814, viii. [CrossRef] [PubMed]
    [Google Scholar]
  10. Decaro N. , Mari V. , Campolo M. , Lorusso A. , Camero M. , Elia G. , Martella V. , Cordioli P. , Enjuanes L. , Buonavoglia C. . ( 2009; ). Recombinant canine coronaviruses related to transmissible gastroenteritis virus of swine are circulating in dogs. . J Virol 83:, 1532–1537. [CrossRef] [PubMed]
    [Google Scholar]
  11. Decaro N. , Mari V. , Elia G. , Addie D. D. , Camero M. , Lucente M. S. , Martella V. , Buonavoglia C. . ( 2010; ). Recombinant canine coronaviruses in dogs, Europe. . Emerg Infect Dis 16:, 41–47. [CrossRef] [PubMed]
    [Google Scholar]
  12. De Grazia S. , Martella V. , Giammanco G. M. , Gòmara M. I. , Ramirez S. , Cascio A. , Colomba C. , Arista S. . ( 2007; ). Canine-origin G3P[3] rotavirus strain in child with acute gastroenteritis. . Emerg Infect Dis 13:, 1091–1093.[PubMed] [CrossRef]
    [Google Scholar]
  13. Dubovi E. J. , Njaa B. L. . ( 2008; ). Canine influenza. . Vet Clin North Am Small Anim Pract 38:, 827–835, viii. [CrossRef] [PubMed]
    [Google Scholar]
  14. Erles K. , Brownlie J. . ( 2008; ). Canine respiratory coronavirus: an emerging pathogen in the canine infectious respiratory disease complex. . Vet Clin North Am Small Anim Pract 38:, 815–825, viii. [CrossRef] [PubMed]
    [Google Scholar]
  15. Farkas T. , Zhong W. M. , Jing Y. , Huang P. W. , Espinosa S. M. , Martinez N. , Morrow A. L. , Ruiz-Palacios G. M. , Pickering L. K. , Jiang X. . ( 2004; ). Genetic diversity among sapoviruses. . Arch Virol 149:, 1309–1323. [CrossRef] [PubMed]
    [Google Scholar]
  16. Greninger A. L. , Runckel C. , Chiu C. Y. , Haggerty T. , Parsonnet J. , Ganem D. , DeRisi J. L. . ( 2009; ). The complete genome of klassevirus - a novel picornavirus in pediatric stool. . Virol J 6:, 82. [CrossRef] [PubMed]
    [Google Scholar]
  17. Griot C. , Vandevelde M. , Schobesberger M. , Zurbriggen A. . ( 2003; ). Canine distemper, a re-emerging morbillivirus with complex neuropathogenic mechanisms. . Anim Health Res Rev 4:, 1–10.[CrossRef]
    [Google Scholar]
  18. Guo M. , Evermann J. F. , Saif L. J. . ( 2001; ). Detection and molecular characterization of cultivable caliciviruses from clinically normal mink and enteric caliciviruses associated with diarrhea in mink. . Arch Virol 146:, 479–493. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hansman G. S. , Oka T. , Katayama K. , Takeda N. . ( 2007; ). Human sapoviruses: genetic diversity, recombination, and classification. . Rev Med Virol 17:, 133–141. [CrossRef] [PubMed]
    [Google Scholar]
  20. Holtz L. R. , Finkbeiner S. R. , Zhao G. , Kirkwood C. D. , Girones R. , Pipas J. M. , Wang D. . ( 2009; ). Klassevirus 1, a previously undescribed member of the family Picornaviridae, is globally widespread. . Virol J 6:, 86. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kapoor A. , Simmonds P. , Gerold G. , Qaisar N. , Jain K. , Henriquez J. A. , Firth C. , Hirschberg D. L. , Rice C. M. et al. ( 2011; ). Characterization of a canine homolog of hepatitis C virus. . Proc Natl Acad Sci U S A 108:, 11608–11613.[CrossRef]
    [Google Scholar]
  22. Koopmans M. K. , Green K. Y. , Ando T. , Clarke I. N. , Estes M. K. , Matson D. O. , Nakata S. , Neill J. D. , Thiel H.-J. . ( 2005; ). Caliciviridae . . In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 843–851. Edited by Fauquet C. , Mayo M. , Maniloff J. , Desselberger U. , Ball L. . . San Diego:: Academic Press;.
    [Google Scholar]
  23. Kumar S. , Nei M. , Dudley J. , Tamura K. . ( 2008; ). mega: a biologist-centric software for evolutionary analysis of DNA and protein sequences. . Brief Bioinform 9:, 299–306. [CrossRef] [PubMed]
    [Google Scholar]
  24. Lackay S. N. , Kuang Y. , Fu Z. F. . ( 2008; ). Rabies in small animals. . Vet Clin North Am Small Anim Pract 38:, 851–861, ix. [CrossRef] [PubMed]
    [Google Scholar]
  25. L’Homme Y. , Sansregret R. , Plante-Fortier E. , Lamontagne A. M. , Lacroix G. , Ouardani M. , Deschamps J. , Simard G. , Simard C. . ( 2009; ). Genetic diversity of porcine Norovirus and Sapovirus: Canada, 2005–2007. . Arch Virol 154:, 581–593. [CrossRef] [PubMed]
    [Google Scholar]
  26. Li L. , Victoria J. , Kapoor A. , Blinkova O. , Wang C. , Babrzadeh F. , Mason C. J. , Pandey P. , Triki H. et al. ( 2009; ). A novel picornavirus associated with gastroenteritis. . J Virol 83:, 12002–12006. [CrossRef] [PubMed]
    [Google Scholar]
  27. Li L. , Victoria J. G. , Wang C. , Jones M. , Fellers G. M. , Kunz T. H. , Delwart E. . ( 2010; ). Bat guano virome: predominance of dietary viruses from insects and plants plus novel mammalian viruses. . J Virol 84:, 6955–6965. [CrossRef] [PubMed]
    [Google Scholar]
  28. Martella V. , Decaro N. , Elia G. , Buonavoglia C. . ( 2005; ). Surveillance activity for canine parvovirus in Italy. . J Vet Med B Infect Dis Vet Public Health 52:, 312–315.[PubMed] [CrossRef]
    [Google Scholar]
  29. Martella V. , Elia G. , Buonavoglia C. . ( 2008a; ). Canine distemper virus. . Vet Clin North Am Small Anim Pract 38:, 787–797, vii–viii. [CrossRef] [PubMed]
    [Google Scholar]
  30. Martella V. , Lorusso E. , Banyai K. , Decaro N. , Corrente M. , Elia G. , Cavalli A. , Radogna A. , Costantini V. et al. ( 2008b; ). Identification of a porcine calicivirus related genetically to human sapoviruses. . J Clin Microbiol 46:, 1907–1913. [CrossRef] [PubMed]
    [Google Scholar]
  31. Martella V. , Bányai K. , Lorusso E. , Bellacicco A. L. , Decaro N. , Mari V. , Saif L. , Costantini V. , De Grazia S. et al. ( 2008c; ). Genetic heterogeneity of porcine enteric caliciviruses identified from diarrhoeic piglets. . Virus Genes 36:, 365–373. [CrossRef] [PubMed]
    [Google Scholar]
  32. Martella V. , Bianchi A. , Bertoletti I. , Pedrotti L. , Gugiatti A. , Catella A. , Cordioli P. , Lucente M. S. , Elia G. , Buonavoglia C. . ( 2010; ). Canine distemper epizootic among red foxes, Italy, 2009. . Emerg Infect Dis 16:, 2007–2009.[PubMed] [CrossRef]
    [Google Scholar]
  33. Nakamura K. , Saga Y. , Iwai M. , Obara M. , Horimoto E. , Hasegawa S. , Kurata T. , Okumura H. , Nagoshi M. , Takizawa T. . ( 2010; ). Frequent detection of noroviruses and sapoviruses in swine and high genetic diversity of porcine sapovirus in Japan during Fiscal Year 2008. . J Clin Microbiol 48:, 1215–1222. [CrossRef] [PubMed]
    [Google Scholar]
  34. Nicholls P. K. , Stanley M. A. . ( 1999; ). Canine papillomavirus – a centenary review. . J Comp Pathol 120:, 219–233. [CrossRef] [PubMed]
    [Google Scholar]
  35. Okada M. , Yamashita Y. , Oseto M. , Ogawa T. , Kaiho I. , Shinozaki K. . ( 2006; ). Genetic variability in the sapovirus capsid protein. . Virus Genes 33:, 157–161. [CrossRef] [PubMed]
    [Google Scholar]
  36. Parrish C. R. . ( 1999; ). Host range relationships and the evolution of canine parvovirus. . Vet Microbiol 69:, 29–40. [CrossRef] [PubMed]
    [Google Scholar]
  37. Parrish C. R. , Kawaoka Y. . ( 2005; ). The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. . Annu Rev Microbiol 59:, 553–586. [CrossRef] [PubMed]
    [Google Scholar]
  38. Pollock R. V. , Coyne M. J. . ( 1993; ). Canine parvovirus. . Vet Clin North Am Small Anim Pract 23:, 555–568.[PubMed] [CrossRef]
    [Google Scholar]
  39. Pratelli A. . ( 2006; ). Genetic evolution of canine coronavirus and recent advances in prophylaxis. . Vet Res 37:, 191–200. [CrossRef] [PubMed]
    [Google Scholar]
  40. Renshaw R. W. , Zylich N. C. , Laverack M. A. , Glaser A. L. , Dubovi E. J. . ( 2010; ). Pneumovirus in dogs with acute respiratory disease. . Emerg Infect Dis 16:, 993–995.[PubMed] [CrossRef]
    [Google Scholar]
  41. Reuter G. , Boldizsár A. , Pankovics P. . ( 2009; ). Complete nucleotide and amino acid sequences and genetic organization of porcine kobuvirus, a member of a new species in the genus Kobuvirus, family Picornaviridae . . Arch Virol 154:, 101–108. [CrossRef] [PubMed]
    [Google Scholar]
  42. Reuter G. , Boros A. , Pankovics P. , Egyed L. . ( 2010; ). Kobuvirus in domestic sheep, Hungary. . Emerg Infect Dis 16:, 869–870.[PubMed] [CrossRef]
    [Google Scholar]
  43. Smiley J. R. , Chang K. O. , Hayes J. , Vinjé J. , Saif L. J. . ( 2002; ). Characterization of an enteropathogenic bovine calicivirus representing a potentially new calicivirus genus. . J Virol 76:, 10089–10098. [CrossRef] [PubMed]
    [Google Scholar]
  44. Truyen U. . ( 1999; ). Emergence and recent evolution of canine parvovirus. . Vet Microbiol 69:, 47–50. [CrossRef] [PubMed]
    [Google Scholar]
  45. Tsugawa T. , Hoshino Y. . ( 2008; ). Whole genome sequence and phylogenetic analyses reveal human rotavirus G3P[3] strains Ro1845 and HCR3A are examples of direct virion transmission of canine/feline rotaviruses to humans. . Virology 380:, 344–353. [CrossRef] [PubMed]
    [Google Scholar]
  46. Usuku S. , Kumazaki M. , Kitamura K. , Tochikubo O. , Noguchi Y. . ( 2008; ). An outbreak of food-borne gastroenteritis due to sapovirus among junior high school students. . Jpn J Infect Dis 61:, 438–441.[PubMed]
    [Google Scholar]
  47. Victoria J. G. , Kapoor A. , Li L. , Blinkova O. , Slikas B. , Wang C. , Naeem A. , Zaidi S. , Delwart E. . ( 2009; ). Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. . J Virol 83:, 4642–4651. [CrossRef] [PubMed]
    [Google Scholar]
  48. Willis A. M. . ( 2000; ). Canine viral infections. . Vet Clin North Am Small Anim Pract 30:, 1119–1133.[PubMed] [CrossRef]
    [Google Scholar]
  49. Wright N. G. . ( 1973; ). Recent advances in canine virus research. . J Small Anim Pract 14:, 241–250. [CrossRef] [PubMed]
    [Google Scholar]
  50. Yamashita T. , Sakae K. , Tsuzuki H. , Suzuki Y. , Ishikawa N. , Takeda N. , Miyamura T. , Yamazaki S. . ( 1998; ). Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans. . J Virol 72:, 8408–8412.[PubMed]
    [Google Scholar]
  51. Yamashita T. , Ito M. , Kabashima Y. , Tsuzuki H. , Fujiura A. , Sakae K. . ( 2003; ). Isolation and characterization of a new species of kobuvirus associated with cattle. . J Gen Virol 84:, 3069–3077. [CrossRef] [PubMed]
    [Google Scholar]
  52. Yang S. , Zhang W. , Shen Q. , Huang F. , Wang Y. , Zhu J. , Cui L. , Yang Z. , Hua X. . ( 2009; ). Molecular characterization and phylogenetic analysis of the complete genome of a porcine sapovirus from Chinese swine. . Virol J 6:, 216. [CrossRef] [PubMed]
    [Google Scholar]
  53. Yu J.-M. , Jin M. , Zhang Q. , Li H.-Y. , Li D.-D. , Xu Z.-Q. , Li J.-S. , Cui S.-X. , Yang S.-H. et al. ( 2009; ). Candidate porcine Kobuvirus, China. . Emerg Infect Dis 15:, 823–825. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.034611-0
Loading
/content/journal/jgv/10.1099/vir.0.034611-0
Loading

Data & Media loading...

Most Cited This Month

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