1887

Abstract

Astro- and kobuviruses infect both humans and animals. Here, we report on the disease history, detection and genomic characterization of novel astro- and kobuviruses from fatal diarrhoea of two juvenile grey squirrels. The virus particles had enterovirus-like morphology and a diameter of 28–32 nm. Next-generation sequencing confirmed astro- and kobuviruses and sequence analysis revealed typical astrovirus and picornavirus genome organizations. The astrovirus ORF2 sequence clustered with a clade of unassigned astroviruses, with marmot and rodent mamastroviruses as closest relatives. For the kobuvirus, divergences greater than 49.4 % for P1 and 43.5 % in the non-structural proteins indicated a novel species. However, phylogenetic analysis of the 3D polymerase showed that it clustered with that of the newly classified ludopivirus A1, suggesting a previous recombination event in the evolution of the kobuvirus. Our data provide further insights into the diversity of astro- and kobuviruses and broaden the spectrum of viruses infecting grey squirrels.

Funding
This study was supported by the:
  • Not Applicable , Horizon 2020 , (Award 773830)
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001431
2020-05-27
2020-08-11
Loading full text...

Full text loading...

/deliver/fulltext/jgv/101/7/746.html?itemId=/content/journal/jgv/10.1099/jgv.0.001431&mimeType=html&fmt=ahah

References

  1. Cortez V, Meliopoulos VA, Karlsson EA, Hargest V, Johnson C et al. Astrovirus biology and pathogenesis. Annu Rev Virol 2017; 4:327–348 [CrossRef][PubMed]
    [Google Scholar]
  2. Johnson C, Hargest V, Cortez V, Meliopoulos V, Schultz-Cherry S. Astrovirus pathogenesis. Viruses 2017; 9:pii: E22 [CrossRef]
    [Google Scholar]
  3. Appleton H, Higgins PG. Viruses and gastroenteritis in infants. The Lancet 1975; 305:1297 [CrossRef]
    [Google Scholar]
  4. Vu DL, Cordey S, Brito F, Kaiser L. Novel human astroviruses: novel human diseases?. J Clin Virol 2016; 82:56–63 [CrossRef][PubMed]
    [Google Scholar]
  5. Snodgrass DR, Gray EW. Detection and transmission of 30 nm virus particles (astroviruses) in faeces of lambs with diarrhoea. Arch Virol 1977; 55:287–291 [CrossRef][PubMed]
    [Google Scholar]
  6. Woode GN, Bridger JC. Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. J Med Microbiol 1978; 11:441–452 [CrossRef][PubMed]
    [Google Scholar]
  7. De Benedictis P, Schultz-Cherry S, Burnham A, Cattoli G. Astrovirus infections in humans and animals – molecular biology, genetic diversity, and interspecies transmissions. Infect Genet Evol 2011; 11:1529–1544 [CrossRef]
    [Google Scholar]
  8. Li L, Diab S, McGraw S, Barr B, Traslavina R et al. Divergent astrovirus associated with neurologic disease in cattle. Emerg Infect Dis 2013; 19:1385–1392 [CrossRef]
    [Google Scholar]
  9. Bouzalas IG, Wüthrich D, Walland J, Drögemüller C, Zurbriggen A et al. Neurotropic astrovirus in cattle with nonsuppurative encephalitis in Europe. J Clin Microbiol 2014; 52:3318–3324 [CrossRef]
    [Google Scholar]
  10. Bouzalas IG, Wüthrich D, Selimovic-Hamza S, Drögemüller C, Bruggmann R et al. Full-Genome based molecular characterization of encephalitis-associated bovine astroviruses. Infect Genet Evol 2016; 44:162–168 [CrossRef]
    [Google Scholar]
  11. Schlottau K, Schulze C, Bilk S, Hanke D, Höper D et al. Detection of a novel bovine astrovirus in a cow with encephalitis. Transbound Emerg Dis 2016; 63:253–259 [CrossRef]
    [Google Scholar]
  12. Seuberlich T, Wüthrich D, Selimovic-Hamza S, Drögemüller C, Oevermann A et al. Identification of a second encephalitis-associated astrovirus in cattle. Emerg Microbes Infect 2016; 20:e71
    [Google Scholar]
  13. Blomström AL, Widén F, Hammer AS, Belák S, Berg M. Detection of a novel astrovirus in brain tissue of mink suffering from shaking mink syndrome by use of viral metagenomics. J Clin Microbiol 2010; 48:4392–4396 [CrossRef]
    [Google Scholar]
  14. Pfaff F, Schlottau K, Scholes S, Courtenay A, Hoffmann B et al. A novel astrovirus associated with encephalitis and ganglionitis in domestic sheep. Transbound Emerg Dis 2017; 64:677–682 [CrossRef]
    [Google Scholar]
  15. Boros Á, Albert M, Pankovics P, Bíró H, Pesavento PA et al. Outbreaks of neuroinvasive astrovirus associated with encephalomyelitis, weakness, and paralysis among weaned pigs, Hungary. Emerg Infect Dis 2017; 23:1982–1993 [CrossRef][PubMed]
    [Google Scholar]
  16. Gough RE, Collins MS, Borland E, Keymer LF. Astrovirus-like particles associated with hepatitis in ducklings. Vet Rec 1984; 114:279 [CrossRef][PubMed]
    [Google Scholar]
  17. Imada T, Yamaguchi S, Kawamura H. Pathogenicity for baby chicks of the G-4260 strain of the picornavirus "avian nephritis virus". Avian Dis 1979; 23:582–588 [CrossRef][PubMed]
    [Google Scholar]
  18. Mendez E, Arias CF. Astroviruses . In Knipe DM, Howley PM. (editors) Fields Virology 2013 pp 609–628
    [Google Scholar]
  19. Yamashita T, Kobayashi S, Sakac K, Nakata S, Chiba S et al. Isolation of cytopathic small round viruses with BS-C-l cells from patients with gastroenteritis. J Infect Dis 1991; 164:954–957 [CrossRef]
    [Google Scholar]
  20. Khamrin P, Maneekarn N, Okitsu S, Ushijima H. Epidemiology of human and animal kobuviruses. Virus Disease 2014; 25:195–200 [CrossRef]
    [Google Scholar]
  21. Yamashita T, Sugiyama M, Tsuzuki H, Sakae K, Suzuki Y et al. Application of a reverse transcription-PCR for identification and differentiation of Aichi virus, a new member of the picornavirus family associated with gastroenteritis in humans. J Clin Microbiol 2000; 38:2955–2961 [CrossRef]
    [Google Scholar]
  22. Ambert-Balay K, Lorrot M, Bon F, Giraudon H, Kaplon J et al. Prevalence and genetic diversity of Aichi virus strains in stool samples from community and hospitalized patients. J Clin Microbiol 2008; 46:1252–1258 [CrossRef]
    [Google Scholar]
  23. Yamashita T, Ito M, Kabashima Y, Tsuzuki H, Fujiura A et al. Isolation and characterization of a new species of kobuvirus associated with cattle. J Gen Virol 2003; 84:3069–3077 [CrossRef][PubMed]
    [Google Scholar]
  24. Smits SL, Raj VS, Oduber MD, Schapendonk CME, Bodewes R et al. Metagenomic analysis of the ferret fecal viral flora. PLoS One 2013; 8:e71595 [CrossRef]
    [Google Scholar]
  25. Reuter G, Boros Á, Pankovics P, Egyed L. Kobuvirus in domestic sheep, Hungary. Emerg Infect Dis 2010; 16:869–870 [CrossRef]
    [Google Scholar]
  26. Reuter G, Boros Á, Pankovics P. Kobuviruses - a comprehensive review. Rev Med Virol 2011; 21:32–41 [CrossRef]
    [Google Scholar]
  27. Reuter G, Nemes C, Boros Á, Kapusinszky B, Delwart E et al. Porcine kobuvirus in wild boars (Sus scrofa). Arch Virol 2013; 158:281–282 [CrossRef]
    [Google Scholar]
  28. Oem JK, Lee MH, Lee KK, An DJ. Novel Kobuvirus species identified from black goat with diarrhea. Vet Microbiol 2014; 172:563–567 [CrossRef][PubMed]
    [Google Scholar]
  29. Pankovics P, Boros Á, Kiss T, Reuter G. Identification and complete genome analysis of kobuvirus in faecal samples of European roller (Coracias garrulus): for the first time in a bird. Arch Virol 2015; 160:345–351 [CrossRef]
    [Google Scholar]
  30. Pankovics P, Boros Á, Bíró H, Horváth KB, Phan TG et al. Novel picornavirus in domestic rabbits (Oryctolagus cuniculus var. domestica). Infect Genet Evol 2016; 37:117–122 [CrossRef]
    [Google Scholar]
  31. Otomaru K, Naoi Y, Haga K, Omatsu T, Uto T et al. Detection of novel kobu-like viruses in Japanese black cattle in Japan. J Vet Med Sci 2016; 78:321–324 [CrossRef]
    [Google Scholar]
  32. Wu Z, Yang L, Ren X, He G, Zhang J et al. Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases. ISME J 2016; 10:609–620 [CrossRef]
    [Google Scholar]
  33. Yamashita T, Sakae K, Tsuzuki H, Suzuki Y, Ishikawa N et al. Complete nucleotide sequence and genetic organisation of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans. J Virol 1998; 72:8408–8412 [CrossRef]
    [Google Scholar]
  34. Everest DJ, Stidworthy MF, Milne EM, Meredith AL, Chantrey J et al. Retrospective detection by negative contrast electron microscopy of faecal viral particles in free-living wild red squirrels (Sciurus vulgaris) with suspected enteropathy in Great Britain. Vet Rec 2010; 167:1007–1010 [CrossRef]
    [Google Scholar]
  35. Dastjerdi A, Fooks AR, Johnson N. In: Rupprecht CE, Fooks AR, Abela-Ridder B (editors). Current laboratory techniques in rabies diagnosis, research and preventionCurrent laboratory techniques in rabies diagnosis, research and prevention Volume 1, 5th ed. 2014
    [Google Scholar]
  36. Dastjerdi A, Carr J, Ellis RJ, Steinbach F, Williamson S. Porcine epidemic diarrhea virus among farmed pigs, Ukraine. Emerg Infect Dis 2015; 21:2235–2237 [CrossRef]
    [Google Scholar]
  37. Boros Á, Pankovics P, Simmonds P, Kiss T, Phan TG et al. Genomic analysis of a novel picornavirus from a migratory waterfowl, greater white-fronted goose (Anser albifrons). Arch Virol 2018; 163:1087–1090 [CrossRef][PubMed]
    [Google Scholar]
  38. Simmonds P. Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J Virol 2006; 80:11124–11140 [CrossRef]
    [Google Scholar]
  39. Van Dung N, Anh PH, Van Cuong N, Hoa NT, Carrique-Mas J et al. Large-Scale screening and characterization of enteroviruses and kobuviruses infecting pigs in Vietnam. J Gen Virol 2016; 97:378–388 [CrossRef]
    [Google Scholar]
  40. Chen L, Zhu L, Zhou Y-cheng, Xu Z-wen, Guo W-zhu et al. Molecular and phylogenetic analysis of the porcine kobuvirus VP1 region using infected pigs from Sichuan Province, China. Virol J 2013; 10:281 [CrossRef][PubMed]
    [Google Scholar]
  41. Khamrin P, Maneekarn N, Hidaka S, Kishikawa S, Ushijima K et al. Molecular detection of kobuvirus sequences in stool samples collected from healthy pigs in Japan. Infect Genet Evol 2010; 10:950–954 [CrossRef]
    [Google Scholar]
  42. Boros Á, Pankovics P, Knowles NJ, Reuter G. Natural interspecies recombinant bovine/porcine enterovirus in sheep. J Gen Virol 2012; 93:1941–1951 [CrossRef]
    [Google Scholar]
  43. Duff JP, Scott AC, Keymer IF. Parapox infection of the grey squirrel. Vet Rec 1996; 138:400
    [Google Scholar]
  44. Everest DJ, Grierson SS, Stidworthy MF, Shuttleworth C. PCR detection of adenovirus in grey squirrels on Anglesey. Vet Rec 2009; 165:482 [CrossRef][PubMed]
    [Google Scholar]
  45. Everest DJ, Tolhurst-Cherriman DAR, Davies H, Dastjerdi A, Ashton A et al. Assessing a potential non-invasive method for viral diagnostic purposes in European squirrels. Hystrix, the Italian Journal of Mammalogy 2019
    [Google Scholar]
  46. Atkin JW, Radford AD, Coyne KP, Stavisky J, Chantrey J. Detection of squirrel poxvirus by nested and real-time PCR from red (Sciurus vulgaris) and grey (Sciurus carolinensis) squirrels. BMC Vet Res 2010; 6:33 [CrossRef]
    [Google Scholar]
  47. Wernike K, Wylezich C, Höper D, Schneider J, Lurz PWW et al. Widespread occurrence of squirrel adenovirus 1 in red and grey squirrels in Scotland detected by a novel real-time PCR assay. Virus Res 2018; 257:113–118 [CrossRef]
    [Google Scholar]
  48. Brooks F, Wood AR, Thomson J, Deane D, Everest DJ et al. Preliminary characterisation of Pentlands paramyxovirus-1, -2 and -3, three new paramyxoviruses of rodents. Vet Microbiol 2014; 170:391–397 [CrossRef]
    [Google Scholar]
  49. Hoff GL, Bigler WJ, Wellings FM, Lewis AL. Human enteroviruses and wildlife: isolation from gray squirrels. J Wildl Dis 1980; 16:131–133 [CrossRef][PubMed]
    [Google Scholar]
  50. Greenwood AG, Sanchez S. Serological evidence of murine pathogens in wild grey squirrels (Sciurus carolinensis) in North Wales. Vet Rec 2002; 150:543–546 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001431
Loading
/content/journal/jgv/10.1099/jgv.0.001431
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited this month 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