1887

Abstract

Metagenomics was used to characterize viral genomes in clinical specimens of horses with various organ-specific diseases of unknown aetiology. A novel parvovirus as well as a previously described hepacivirus closely related to human hepatitis C virus and equid herpesvirus 2 were identified in the cerebrospinal fluid of horses with neurological signs. Four co-infecting picobirnaviruses, including an unusual genome with fused RNA segments, and a divergent anellovirus were found in the plasma of two febrile horses. A novel cyclovirus genome was characterized from the nasal secretion of another febrile animal. Lastly, a small circular DNA genome with a Rep gene, from a virus we called kirkovirus, was identified in the liver and spleen of a horse with fatal idiopathic hepatopathy. This study expands the number of viruses found in horses, and characterizes their genomes to assist future epidemiological studies of their transmission and potential association with various equine diseases.

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2015-09-01
2024-03-28
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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 [View Article][PubMed]
    [Google Scholar]
  2. Allander T., Tammi M.T., Eriksson M., Bjerkner A., Tiveljung-Lindell A., Andersson B. 2005; Cloning of a human parvovirus by molecular screening of respiratory tract samples. Proc Natl Acad Sci U S A 102:12891–12896 [View Article][PubMed]
    [Google Scholar]
  3. Aramouni M., Kekarainen T., Ganges L., Tarradas J., Segalés J. 2013; Increased viral load and prevalence of Torque teno sus virus 2 (TTSuV2) in pigs experimentally infected with classical swine fever virus (CSFV). Virus Res 172:81–84 [View Article][PubMed]
    [Google Scholar]
  4. Bányai K., Potgieter C., Gellért Á., Ganesh B., Tempesta M., Lorusso E., Buonavoglia C., Martella V. 2014; Genome sequencing identifies genetic and antigenic divergence of porcine picobirnaviruses. J Gen Virol 95:2233–2239 [View Article][PubMed]
    [Google Scholar]
  5. Barah F., Whiteside S., Batista S., Morris J. 2014; Neurological aspects of human parvovirus B19 infection: a systematic review. Rev Med Virol 24:154–168 [View Article][PubMed]
    [Google Scholar]
  6. Benjamin L.A., Lewthwaite P., Vasanthapuram R., Zhao G., Sharp C., Simmonds P., Wang D., Solomon T. 2011; Human parvovirus 4 as potential cause of encephalitis in children, India. Emerg Infect Dis 17:1484–1487[PubMed]
    [Google Scholar]
  7. Biagini P. 2009; Classification of TTV and related viruses (anelloviruses). Curr Top Microbiol Immunol 331:21–33[PubMed]
    [Google Scholar]
  8. Burbelo P.D., Dubovi E.J., Simmonds P., Medina J.L., Henriquez J.A., Mishra N., Wagner J., Tokarz R., Cullen J.M., other authors. 2012; Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J Virol 86:6171–6178 [View Article][PubMed]
    [Google Scholar]
  9. Cann A.J., Fandrich S.E., Heaphy S. 2005; Analysis of the virus population present in equine faeces indicates the presence of hundreds of uncharacterized virus genomes. Virus Genes 30:151–156 [View Article][PubMed]
    [Google Scholar]
  10. Chandriani S., Skewes-Cox P., Zhong W., Ganem D.E., Divers T.J., Van Blaricum A.J., Tennant B.C., Kistler A.L. 2013; Identification of a previously undescribed divergent virus from the Flaviviridae family in an outbreak of equine serum hepatitis. Proc Natl Acad Sci U S A 110:E1407–E1415 [View Article][PubMed]
    [Google Scholar]
  11. Chen M., Sun H., Lan D., Hua X., Cui L., Yuan C., Yang Z. 2014; Molecular detection of genogroup I and II picobirnaviruses in pigs in China. Virus Genes 48:553–556 [View Article][PubMed]
    [Google Scholar]
  12. Cheung A.K., Wu G., Wang D., Bayles D.O., Lager K.M., Vincent A.L. 2010; Identification and molecular cloning of a novel porcine parvovirus. Arch Virol 155:801–806 [View Article][PubMed]
    [Google Scholar]
  13. Cotmore S.F., Agbandje-McKenna M., Chiorini J.A., Mukha D.V., Pintel D.J., Qiu J., Soderlund-Venermo M., Tattersall P., Tijssen P., other authors. 2014; The family Parvoviridae . Arch Virol 159:1239–1247 [View Article][PubMed]
    [Google Scholar]
  14. Cullinane A., Newton J.R. 2013; Equine influenza – a global perspective. Vet Microbiol 167:205–214 [View Article][PubMed]
    [Google Scholar]
  15. De Vlaminck I., Khush K.K., Strehl C., Kohli B., Luikart H., Neff N.F., Okamoto J., Snyder T.M., Cornfield D.N., other authors. 2013; Temporal response of the human virome to immunosuppression and antiviral therapy. Cell 155:1178–1187 [View Article][PubMed]
    [Google Scholar]
  16. Delwart E. 2012; Animal virus discovery: improving animal health, understanding zoonoses, and opportunities for vaccine development. Curr Opin Virol 2:344–352 [View Article][PubMed]
    [Google Scholar]
  17. 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]
  18. Deng X., Naccache S.N., Ng T., Federman S., Li L., Chiu C.Y., Delwart E.L. 2015; An ensemble strategy that significantly improves de novo assembly of microbial genomes from metagenomic next-generation sequencing data. Nucleic Acids Res 43:e46 [View Article][PubMed]
    [Google Scholar]
  19. Douvoyiannis M., Litman N., Goldman D.L. 2009; Neurologic manifestations associated with parvovirus B19 infection. Clin Infect Dis 48:1713–1723 [View Article][PubMed]
    [Google Scholar]
  20. Ellis J. 2014; Porcine circovirus: a historical perspective. Vet Pathol 51:315–327 [View Article][PubMed]
    [Google Scholar]
  21. Fielding C.L., Higgins J.K., Higgins J.C., McIntosh S., Scott E., Giannitti F., Mete A., Pusterla N. 2015; Disease associated with equine coronavirus infection and high case fatality rate. J Vet Intern Med 29:307–310 [View Article][PubMed]
    [Google Scholar]
  22. Focosi D., Macera L., Pistello M., Maggi F. 2014; Torque teno virus viremia correlates with intensity of maintenance immunosuppression in adult orthotopic liver transplant. J Infect Dis 210:667–668 [View Article][PubMed]
    [Google Scholar]
  23. Ganesh B., Banyai K., Masachessi G., Mladenova Z., Nagashima S., Ghosh S., Nataraju S.M., Pativada M., Kumar R., Kobayashi N. 2011; Genogroup I picobirnavirus in diarrhoeic foals: can the horse serve as a natural reservoir for human infection?. Vet Res 42:52 [View Article][PubMed]
    [Google Scholar]
  24. Garigliany M.M., Hagen R.M., Frickmann H., May J., Schwarz N.G., Perse A., Jöst H., Börstler J., Shahhosseini N., other authors. 2014; Cyclovirus CyCV-VN species distribution is not limited to Vietnam and extends to Africa. Sci Rep 4:7552 [View Article][PubMed]
    [Google Scholar]
  25. Giannitti F., Diab S., Mete A., Stanton J.B., Fielding L., Crossley B., Sverlow K., Fish S., Mapes S., other authors. 2015; Necrotizing enteritis and hyperammonemic encephalopathy associated with equine coronavirus infection in equids. Vet Pathol (published ahead of print) http://vet.sagepub.com/content/early/2015/02/02/0300985814568683.abstract [View Article][PubMed]
    [Google Scholar]
  26. Gillman L., Sánchez A.M., Arbiza J. 2013; Picobirnavirus in captive animals from Uruguay: identification of new hosts. Intervirology 56:46–49 [View Article][PubMed]
    [Google Scholar]
  27. Johnson A.L. 2011; Update on infectious diseases affecting the equine nervous system. Vet Clin North Am Equine Pract 27:573–587 [View Article][PubMed]
    [Google Scholar]
  28. Kapoor A., Simmonds P., Gerold G., Qaisar N., Jain K., Henriquez J.A., Firth C., Hirschberg D.L., Rice C.M., other authors. 2011; Characterization of a canine homolog of hepatitis C virus. Proc Natl Acad Sci U S A 108:11608–11613 [View Article][PubMed]
    [Google Scholar]
  29. Labonté J.M., Suttle C.A. 2013; Previously unknown and highly divergent ssDNA viruses populate the oceans. ISME J 7:2169–2177 [View Article][PubMed]
    [Google Scholar]
  30. Li L., Kapoor A., Slikas B., Bamidele O.S., Wang C., Shaukat S., Masroor M.A., Wilson M.L., Ndjango J.B., 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]
  31. 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]
  32. 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]
  33. Li L., Deng X., Linsuwanon P., Bangsberg D., Bwana M.B., Hunt P., Martin J.N., Deeks S.G., Delwart E. 2013; AIDS alters the commensal plasma virome. J Virol 87:10912–10915 [View Article][PubMed]
    [Google Scholar]
  34. Li L., Deng X., Mee E.T., Collot-Teixeira S., Anderson R., Schepelmann S., Minor P.D., Delwart E. 2015; Comparing viral metagenomics methods using a highly multiplexed human viral pathogens reagent. J Virol Methods 213:139–146 [View Article][PubMed]
    [Google Scholar]
  35. Maclachlan N.J., Dubovi E.J., Fenner F. 2011 Fenner's Veterinary Virology, 4th edn. London: Academic Press;
    [Google Scholar]
  36. Malik Y.S., Kumar N., Sharma K., Dhama K., Shabbir M.Z., Ganesh B., Kobayashi N., Banyai K. 2014; Epidemiology, phylogeny, and evolution of emerging enteric Picobirnaviruses of animal origin and their relationship to human strains. BioMed Res Int 2014:780752 [View Article][PubMed]
    [Google Scholar]
  37. Mancuso R., Saresella M., Hernis A., Agostini S., Piancone F., Caputo D., Maggi F., Clerici M. 2013; Torque teno virus (TTV) in multiple sclerosis patients with different patterns of disease. J Med Virol 85:2176–2183[PubMed] [CrossRef]
    [Google Scholar]
  38. Masachessi G., Ganesh B., Martinez L.C., Giordano M.O., Barril P.A., Isa M.B., Paván G.V., Mateos C.A., Nates S.V. 2015; Maintenance of picobirnavirus (PBV) infection in an adult orangutan (Pongo pygmaeus) and genetic diversity of excreted viral strains during a three-year period. Infect Genet Evol 29:196–202 [View Article][PubMed]
    [Google Scholar]
  39. Mei M., Zhu L., Wang Y., Xu Z., Zhao L., Peng X., Wu Y., Li S., Guo W. 2011; Histopathological investigation in porcine infected with torque teno sus virus type 2 by inoculation. Virol J 8:545 [View Article][PubMed]
    [Google Scholar]
  40. Mi Z., Yuan X., Pei G., Wang W., An X., Zhang Z., Huang Y., Peng F., Li S., other authors. 2014; High-throughput sequencing exclusively identified a novel Torque teno virus genotype in serum of a patient with fatal fever. Virol Sin 29:112–118 [View Article][PubMed]
    [Google Scholar]
  41. Ng T.F., Suedmeyer W.K., Wheeler E., Gulland F., Breitbart M. 2009; Novel anellovirus discovered from a mortality event of captive California sea lions. J Gen Virol 90:1256–1261 [View Article][PubMed]
    [Google Scholar]
  42. Ng T.F., Mesquita J.R., Nascimento M.S., Kondov N.O., Wong W., Reuter G., Knowles N.J., Vega E., Esona M.D., other authors. 2014; Feline fecal virome reveals novel and prevalent enteric viruses. Vet Microbiol 171:102–111 [View Article][PubMed]
    [Google Scholar]
  43. Ni J., Qiao C., Han X., Han T., Kang W., Zi Z., Cao Z., Zhai X., Cai X. 2014; Identification and genomic characterization of a novel porcine parvovirus (PPV6) in china. Virol J 11:203 [View Article][PubMed]
    [Google Scholar]
  44. Nishiyama S., Dutia B.M., Stewart J.P., Meredith A.L., Shaw D.J., Simmonds P., Sharp C.P. 2014; Identification of novel anelloviruses with broad diversity in UK rodents. J Gen Virol 95:1544–1553 [View Article][PubMed]
    [Google Scholar]
  45. Nishizawa T., Okamoto H., Konishi K., Yoshizawa H., Miyakawa Y., Mayumi M. 1997; A novel DNA virus (TTV) associated with elevated transaminase levels in posttransfusion hepatitis of unknown etiology. Biochem Biophys Res Commun 241:92–97 [View Article][PubMed]
    [Google Scholar]
  46. Okamoto H. 2009a; History of discoveries and pathogenicity of TT viruses. Curr Top Microbiol Immunol 331:1–20[PubMed]
    [Google Scholar]
  47. Okamoto H. 2009b; TT viruses in animals. Curr Top Microbiol Immunol 331:35–52[PubMed]
    [Google Scholar]
  48. Onmaz A.C., Beutel R.G., Schneeberg K., Pavaloiu A.N., Komarek A., van den Hoven R. 2013; Vectors and vector-borne diseases of horses. Vet Res Commun 37:65–81 [View Article][PubMed]
    [Google Scholar]
  49. Padilla-Rodriguez M., Rosario K., Breitbart M. 2013; Novel cyclovirus discovered in the Florida woods cockroach Eurycotis floridana (Walker). Arch Virol 158:1389–1392 [View Article][PubMed]
    [Google Scholar]
  50. Pereira H.G., Flewett T.H., Candeias J.A., Barth O.M. 1988; A virus with a bisegmented double-stranded RNA genome in rat (Oryzomys nigripes) intestines. J Gen Virol 69:2749–2754 [View Article][PubMed]
    [Google Scholar]
  51. Phan T.G., Luchsinger V., Avendaño L.F., Deng X., Delwart E. 2014; Cyclovirus in nasopharyngeal aspirates of Chilean children with respiratory infections. J Gen Virol 95:922–927 [View Article][PubMed]
    [Google Scholar]
  52. Pollicino T., Raffa G., Squadrito G., Costantino L., Cacciola I., Brancatelli S., Alafaci C., Florio M.G., Raimondo G. 2003; TT virus has a ubiquitous diffusion in human body tissues: analyses of paired serum and tissue samples. J Viral Hepat 10:95–102 [View Article][PubMed]
    [Google Scholar]
  53. Prakash S., Jain A., Seth A., Singh A.K., Jain B. 2015; Complete genome sequences of two isolates of human parvovirus 4 from patients with acute encephalitis syndrome. Genome Announc 3:e01472–e01414 [View Article][PubMed]
    [Google Scholar]
  54. 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]
  55. 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][PubMed]
    [Google Scholar]
  56. Scheel T.K., Simmonds P., Kapoor A. 2015; Surveying the global virome: identification and characterization of HCV-related animal hepaciviruses. Antiviral Res 115:83–93 [View Article][PubMed]
    [Google Scholar]
  57. Shan T., Li L., Simmonds P., Wang C., Moeser A., Delwart E. 2011; The fecal virome of pigs on a high-density farm. J Virol 85:11697–11708 [View Article][PubMed]
    [Google Scholar]
  58. Slater J. 2013; From glanders to Hendra virus: 125 years of equine infectious diseases. Vet Rec 173:186–189 [View Article][PubMed]
    [Google Scholar]
  59. Smits S.L., Poon L.L., van Leeuwen M., Lau P.N., Perera H.K., Peiris J.S., Simon J.H., Osterhaus A.D. 2011; Genogroup I and II picobirnaviruses in respiratory tracts of pigs. Emerg Infect Dis 17:2328–2330 [View Article][PubMed]
    [Google Scholar]
  60. Smits S.L., van Leeuwen M., Schapendonk C.M., Schürch A.C., Bodewes R., Haagmans B.L., Osterhaus A.D. 2012; Picobirnaviruses in the human respiratory tract. Emerg Infect Dis 18:1539–1540 [View Article][PubMed]
    [Google Scholar]
  61. Smits S.L., Zijlstra E.E., van Hellemond J.J., Schapendonk C.M., Bodewes R., Schürch A.C., Haagmans B.L., Osterhaus A.D. 2013; Novel cyclovirus in human cerebrospinal fluid, Malawi, 2010–2011. Emerg Infect Dis 19:1511–1513 [View Article][PubMed]
    [Google Scholar]
  62. Smits S.L., Schapendonk C.M., van Beek J., Vennema H., Schürch A.C., Schipper D., Bodewes R., Haagmans B.L., Osterhaus A.D., Koopmans M.P. 2014; New viruses in idiopathic human diarrhea cases, the Netherlands. Emerg Infect Dis 20:1218–1222 [View Article][PubMed]
    [Google Scholar]
  63. Sukhumsirichart W., Attasart P., Boonsaeng V., Panyim S. 2006; Complete nucleotide sequence and genomic organization of hepatopancreatic parvovirus (HPV) of Penaeus monodon . Virology 346:266–277 [View Article][PubMed]
    [Google Scholar]
  64. Tan V., van Doorn H.R., Nghia H.D., Chau T.T., Tu T.P., de Vries M., Canuti M., Deijs M., Jebbink M.F., other authors. 2013; Identification of a new cyclovirus in cerebrospinal fluid of patients with acute central nervous system infections. MBio 4:e00231–e00213 [View Article][PubMed]
    [Google Scholar]
  65. Telford E.A., Watson M.S., Aird H.C., Perry J., Davison A.J. 1995; The DNA sequence of equine herpesvirus 2. J Mol Biol 249:520–528 [View Article][PubMed]
    [Google Scholar]
  66. Toplu N., Og˘uzog˘lu T.C., Ural K., Albayrak H., Ozan E., Ertürk A., Epikmen E.T. 2015; West Nile Virus infection in horses: detection by immunohistochemistry, in situ hybridization, and ELISA. Vet Pathol [View Article][PubMed] [View Article][PubMed] [Epub ahead of print].
    [Google Scholar]
  67. Verma H., Mor S.K., Erber J., Goyal S.M. 2015; Prevalence and complete genome characterization of turkey picobirnaviruses. Infect Genet Evol 30:134–139 [View Article][PubMed]
    [Google Scholar]
  68. 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 [View Article][PubMed]
    [Google Scholar]
  69. Woo P.C., Lau S.K., Teng J.L., Tsang A.K., Joseph M., Wong E.Y., Tang Y., Sivakumar S., Bai R., other authors. 2014; Metagenomic analysis of viromes of dromedary camel fecal samples reveals large number and high diversity of circoviruses and picobirnaviruses. Virology 471-473:117–125 [View Article][PubMed]
    [Google Scholar]
  70. Xiao C.T., Giménez-Lirola L.G., Jiang Y.H., Halbur P.G., Opriessnig T. 2013; Characterization of a novel porcine parvovirus tentatively designated PPV5. PLoS One 8:e65312 [View Article][PubMed]
    [Google Scholar]
  71. Young J.C., Chehoud C., Bittinger K., Bailey A., Diamond J.M., Cantu E., Haas A.R., Abbas A., Frye L., other authors. 2015; Viral metagenomics reveal blooms of anelloviruses in the respiratory tract of lung transplant recipients. Am J Transplant 15:200–209 [View Article][PubMed]
    [Google Scholar]
  72. Yu X., Li B., Fu Y., Jiang D., Ghabrial S.A., Li G., Peng Y., Xie J., Cheng J., 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]
  73. Zhang W., Li L., Deng X., Kapusinszky B., Delwart E. 2014; What is for dinner? Viral metagenomics of US store bought beef, pork, and chicken. Virology 468-470:303–310 [View Article]
    [Google Scholar]
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