1887

Abstract

This study reports the metagenomic detection and complete genome characterization of a novel turkey picornavirus from faecal samples of healthy (1/3) and affected (6/8) commercial turkeys with enteric and/or stunting syndrome in Hungary. The virus was detected at seven of the eight farms examined. The turkey/M176-TuASV/2011/HUN genome (KC465954) was genetically different from the currently known picornaviruses of turkey origin (megriviruses and galliviruses), and showed distant phylogenetic relationship and common genomic features (e.g. uncleaved VP0 and three predicted and unrelated 2A polypeptides) to duck hepatitis A virus (DHAV) of the genus . The complete genome analysis revealed multiple distinct genome features like the presence of two in-tandem aphthovirus 2A-like sequence repeats with DxExNPG/P ‘ribosome-skipping’ sites (76 %, 23/30 amino acids identical), with the first aphthovirus 2A-like sequence being located at the end of the VP1 capsid protein (VP1/2A1 ‘ribosome-skipping’ site). The phylogenetic analyses, low sequence identity (33, 32 and 36 % amino acid identity in P1, P2 and P3 regions) to DHAV, and the type II-like internal ribosome entry site suggests that this turkey picornavirus is related to, but distinct from the genus and it could be the founding member of a novel sister-clade genus. This is the third, taxonomically highly distinct picornavirus clade identified from turkeys exhibiting varied symptoms.

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2013-07-01
2019-10-21
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References

  1. Barbknecht M.. ( 2009; ). Characterization of a unclassified virus and survey for its presence in Wisconsin bluegill populations . . MSc thesis;, University of Wisconsin–La Crosse;.
  2. Bazan J. F., Fletterick R. J.. ( 1988; ). Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: structural and functional implications. . Proc Natl Acad Sci U S A 85:, 7872–7876. [CrossRef] [PubMed]
    [Google Scholar]
  3. Belsham G. J.. ( 2009; ). Divergent picornavirus IRES elements. . Virus Res 139:, 183–192. [CrossRef] [PubMed]
    [Google Scholar]
  4. Blom N., Hansen J., Brunak S., Blaas D.. ( 1996; ). Cleavage site analysis in picornaviral polyproteins: discovering cellular targets by neural networks. . Protein Sci 5:, 2203–2216. [CrossRef] [PubMed]
    [Google Scholar]
  5. Boros A., Pankovics P., Simmonds P., Reuter G.. ( 2011; ). Novel positive-sense, single-stranded RNA (+ssRNA) virus with di-cistronic genome from intestinal content of freshwater carp (Cyprinus carpio). . PLoS ONE 6:, e29145. [CrossRef] [PubMed]
    [Google Scholar]
  6. Boros A., Nemes C., Pankovics P., Kapusinszky B., Delwart E., Reuter G.. ( 2012a; ). Identification and complete genome characterization of a novel picornavirus in turkey (Meleagris gallopavo). . J Gen Virol 93:, 2171–2182. [CrossRef] [PubMed]
    [Google Scholar]
  7. Boros A., Pankovics P., Knowles N. J., Reuter G.. ( 2012b; ). Natural interspecies recombinant bovine/porcine enterovirus in sheep. . J Gen Virol 93:, 1941–1951. [CrossRef] [PubMed]
    [Google Scholar]
  8. Day J. M., Ballard L. L., Duke M. V., Scheffler B. E., Zsak L.. ( 2010; ). Metagenomic analysis of the turkey gut RNA virus community. . Virol J 7:, 313. [CrossRef] [PubMed]
    [Google Scholar]
  9. Ding C., Zhang D.. ( 2007; ). Molecular analysis of duck hepatitis virus type 1. . Virology 361:, 9–17. [CrossRef] [PubMed]
    [Google Scholar]
  10. Doherty M., Todd D., McFerran N., Hoey E. M.. ( 1999; ). Sequence analysis of a porcine enterovirus serotype 1 isolate: relationships with other picornaviruses. . J Gen Virol 80:, 1929–1941.[PubMed]
    [Google Scholar]
  11. Farkas T., Fey B., Hargitt E. III, Parcells M., Ladman B., Murgia M., Saif Y.. ( 2012; ). Molecular detection of novel picornaviruses in chickens and turkeys. . Virus Genes 44:, 262–272. [CrossRef] [PubMed]
    [Google Scholar]
  12. Fu Y., Pan M., Wang X., Xu Y., Yang H., Zhang D.. ( 2008; ). Molecular detection and typing of duck hepatitis A virus directly from clinical specimens. . Vet Microbiol 131:, 247–257. [CrossRef] [PubMed]
    [Google Scholar]
  13. Ghazi F., Hughes P. J., Hyypiä T., Stanway G.. ( 1998; ). Molecular analysis of human parechovirus type 2 (formerly echovirus 23). . J Gen Virol 79:, 2641–2650.[PubMed]
    [Google Scholar]
  14. Gorbalenya A. E., Donchenko A. P., Blinov V. M., Koonin E. V.. ( 1989; ). Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases: a distinct protein superfamily with a common structural fold. . FEBS Lett 243:, 103–114. [CrossRef] [PubMed]
    [Google Scholar]
  15. Gorbalenya A. E., Koonin E. V., Wolf Y. I.. ( 1990; ). A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. . FEBS Lett 262:, 145–148. [CrossRef] [PubMed]
    [Google Scholar]
  16. Honkavuori K. S., Shivaprasad H. L., Briese T., Street C., Hirschberg D. L., Hutchison S. K., Lipkin W. I.. ( 2011; ). Novel picornavirus in Turkey poults with hepatitis, California, USA. . Emerg Infect Dis 17:, 480–487. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hughes P. J., Stanway G.. ( 2000; ). The 2A proteins of three diverse picornaviruses are related to each other and to the H-rev107 family of proteins involved in the control of cell proliferation. . J Gen Virol 81:, 201–207.[PubMed]
    [Google Scholar]
  18. Johansson S., Niklasson B., Maizel J., Gorbalenya A. E., Lindberg A. M.. ( 2002; ). Molecular analysis of three Ljungan virus isolates reveals a new, close-to-root lineage of the Picornaviridae with a cluster of two unrelated 2A proteins. . J Virol 76:, 8920–8930. [CrossRef] [PubMed]
    [Google Scholar]
  19. Johansson E. S., Niklasson B., Tesh R. B., Shafren D. R., Travassos da Rosa A. P., Lindberg A. M.. ( 2003; ). Molecular characterization of M1146, an American isolate of Ljungan virus (LV) reveals the presence of a new LV genotype. . J Gen Virol 84:, 837–844. [CrossRef] [PubMed]
    [Google Scholar]
  20. Kapoor A., Victoria J., Simmonds P., Slikas E., Chieochansin T., Naeem A., Shaukat S., Sharif S., Alam M. M.. & other authors ( 2008a; ). A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. . Proc Natl Acad Sci U S A 105:, 20482–20487. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kapoor A., Victoria J., Simmonds P., Wang C., Shafer R. W., Nims R., Nielsen O., Delwart E.. ( 2008b; ). A highly divergent picornavirus in a marine mammal. . J Virol 82:, 311–320. [CrossRef] [PubMed]
    [Google Scholar]
  22. Kim M. C., Kwon Y. K., Joh S. J., Kim S. J., Tolf C. J., Kim J. H., Sung H. W., Lindberg A. M., Kwon J. H.. ( 2007; ). Recent Korean isolates of duck hepatitis virus reveal the presence of a new geno- and serotype when compared to duck hepatitis virus type 1 type strains. . Arch Virol 152:, 2059–2072. [CrossRef] [PubMed]
    [Google Scholar]
  23. Knowles N. J., Hovi T., Hyypiä T., King A. M. Q., Lindberg A. M., Pallansch M. A., Palmenberg A. C., Simmonds P., Skern T.. & other authors ( 2012; ). Picornaviridae. . In Virus Taxonomy. Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses, pp. 855–880. Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J... San Diego:: Elsevier;.
    [Google Scholar]
  24. Kofstad T., Jonassen C. M.. ( 2011; ). Screening of feral and wood pigeons for viruses harbouring a conserved mobile viral element: characterization of novel astroviruses and picornaviruses. . PLoS ONE 6:, e25964. [CrossRef] [PubMed]
    [Google Scholar]
  25. Marchler-Bauer A., Lu S., Anderson J. B., Chitsaz F., Derbyshire M. K., DeWeese-Scott C., Fong J. H., Geer L. Y., Geer R. C.. & other authors ( 2011; ). CDD: a conserved domain database for the functional annotation of proteins. . Nucleic Acids Res 39: (Database issue), D225–D229. [CrossRef] [PubMed]
    [Google Scholar]
  26. 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. [CrossRef] [PubMed]
    [Google Scholar]
  27. Nicholas K. B., Nicholas H. B.. ( 1997; ). GeneDoc: a tool for editing and annotating multiple sequence alignments. National Resource for Biomedical Supercomputing. http://www.nrbsc.org. Accessed 02 Dec 2011.
  28. OIE ( 2010; ). Duck virus hepatitis. . In Manual of Diagnostic Tests & Vaccines for Terrestrial Animals, , 7th edn., Chapter 2.3.8. Paris:: OIE (Office International des Epizooties);. http://www.oie.int/manual-of-diagnostic-tests-and-vaccines-for-terrestrial-animals/. Accessed 07 Jan. 2013.
    [Google Scholar]
  29. Pankovics P., Boros A., Reuter G.. ( 2012; ). Novel picornavirus in domesticated common quail (Coturnix coturnix) in Hungary. . Arch Virol 157:, 525–530. [CrossRef] [PubMed]
    [Google Scholar]
  30. Pantin-Jackwood M. J., Spackman E., Day J. M., Rives D.. ( 2007; ). Periodic monitoring of commercial turkeys for enteric viruses indicates continuous presence of astrovirus and rotavirus on the farms. . Avian Dis 51:, 674–680. [CrossRef] [PubMed]
    [Google Scholar]
  31. Pantin-Jackwood M. J., Day J. M., Jackwood M. W., Spackman E.. ( 2008; ). Enteric viruses detected by molecular methods in commercial chicken and turkey flocks in the United States between 2005 and 2006. . Avian Dis 52:, 235–244. [CrossRef] [PubMed]
    [Google Scholar]
  32. Racaniello V.. (2007). Picornaviridae: the viruses and their replication. . In Fields Virology, , 5th edn., pp. 795–838. Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Riozman B., Straus S. E... Philadelphia, PA:: Lippincott Williams & Wilkins;.
    [Google Scholar]
  33. Reuter G., Farkas T., Berke T., Jiang X., Matson D. O., Szücs G.. ( 2002; ). Molecular epidemiology of human calicivirus gastroenteritis outbreaks in Hungary, 1998 to 2000. . J Med Virol 68:, 390–398. [CrossRef] [PubMed]
    [Google Scholar]
  34. 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]
  35. Reuter G., Pankovics P., Knowles N. J., Boros A.. ( 2012; ). Two closely related novel picornaviruses in cattle and sheep in Hungary from 2008 to 2009, proposed as members of a new genus in the family Picornaviridae . . J Virol 86:, 13295–13302. [CrossRef] [PubMed]
    [Google Scholar]
  36. Rohll J. B., Moon D. H., Evans D. J., Almond J. W.. ( 1995; ). The 3′ untranslated region of picornavirus RNA: features required for efficient genome replication. . J Virol 69:, 7835–7844.[PubMed]
    [Google Scholar]
  37. Sauvage V., Ar Gouilh M., Cheval J., Muth E., Pariente K., Burguiere A., Caro V., Manuguerra J. C., Eloit M.. ( 2012; ). A member of a new Picornaviridae genus is shed in pig feces. . J Virol 86:, 10036–10046. [CrossRef] [PubMed]
    [Google Scholar]
  38. Semler B. L., Ertel K. J.. ( 2008; ). Picornaviruses: molecular biology. . In Encyclopedia of virology, , 3rd edn., pp. 129–140. Edited by Mahy B. W. J., Van Regenmortel M. H. V... Oxford:: Academic Press;. [CrossRef]
    [Google Scholar]
  39. Sharma P., Yan F., Doronina V. A., Escuin-Ordinas H., Ryan M. D., Brown J. D.. ( 2012; ). 2A peptides provide distinct solutions to driving stop-carry on translational recoding. . Nucleic Acids Res 40:, 3143–3151. [CrossRef] [PubMed]
    [Google Scholar]
  40. Sweeney T. R., Dhote V., Yu Y., Hellen C. U.. ( 2012; ). A distinct class of internal ribosomal entry site in members of the Kobuvirus and proposed Salivirus and Paraturdivirus genera of the Picornaviridae . . J Virol 86:, 1468–1486. [CrossRef] [PubMed]
    [Google Scholar]
  41. 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. [CrossRef] [PubMed]
    [Google Scholar]
  42. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G.. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. . Nucleic Acids Res 25:, 4876–4882. [CrossRef] [PubMed]
    [Google Scholar]
  43. Tseng C. H., Tsai H. J.. ( 2007; ). Molecular characterization of a new serotype of duck hepatitis virus. . Virus Res 126:, 19–31. [CrossRef] [PubMed]
    [Google Scholar]
  44. Tseng C. H., Knowles N. J., Tsai H. J.. ( 2007; ). Molecular analysis of duck hepatitis virus type 1 indicates that it should be assigned to a new genus. . Virus Res 123:, 190–203. [CrossRef] [PubMed]
    [Google Scholar]
  45. 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]
  46. Wang X., Zhang J., Lu J., Yi F., Liu C., Hu Y.. ( 2004; ). Sequence analysis and genomic organization of a new insect picorna-like virus, Ectropis obliqua picorna-like virus, isolated from Ectropis obliqua . . J Gen Virol 85:, 1145–1151. [CrossRef] [PubMed]
    [Google Scholar]
  47. Williams C. H., Panayiotou M., Girling G. D., Peard C. I., Oikarinen S., Hyöty H., Stanway G.. ( 2009; ). Evolution and conservation in human parechovirus genomes. . J Gen Virol 90:, 1702–1712. [CrossRef] [PubMed]
    [Google Scholar]
  48. Woo P. C., Lau S. K., Yuen K. Y.. ( 2006; ). Infectious diseases emerging from Chinese wet-markets: zoonotic origins of severe respiratory viral infections. . Curr Opin Infect Dis 19:, 401–407. [CrossRef] [PubMed]
    [Google Scholar]
  49. Woo P. C., Lau S. K., Huang Y., Lam C. S., Poon R. W., Tsoi H. W., Lee P., Tse H., Chan A. S.. & other authors ( 2010; ). Comparative analysis of six genome sequences of three novel picornaviruses, turdiviruses 1, 2 and 3, in dead wild birds, and proposal of two novel genera, Orthoturdivirus and Paraturdivirus, in the family Picornaviridae . . J Gen Virol 91:, 2433–2448. [CrossRef] [PubMed]
    [Google Scholar]
  50. Woo P. C., Lau S. K., Choi G. K., Huang Y., Teng J. L., Tsoi H. W., Tse H., Yeung M. L., Chan K. H.. & other authors ( 2012; ). Natural occurrence and characterization of two internal ribosome entry site elements in a novel virus, canine picodicistrovirus, in the picornavirus-like superfamily. . J Virol 86:, 2797–2808. [CrossRef] [PubMed]
    [Google Scholar]
  51. Wu C. Y., Lo C. F., Huang C. J., Yu H. T., Wang C. H.. ( 2002; ). The complete genome sequence of Perina nuda picorna-like virus, an insect-infecting RNA virus with a genome organization similar to that of the mammalian picornaviruses. . Virology 294:, 312–323. [CrossRef] [PubMed]
    [Google Scholar]
  52. Yu Y., Abaeva I. S., Marintchev A., Pestova T. V., Hellen C. U. T.. ( 2011; ). Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. . Nucleic Acids Res 39:, 4851–4865. [CrossRef] [PubMed]
    [Google Scholar]
  53. Zuker M.. ( 2003; ). Mfold web server for nucleic acid folding and hybridization prediction. . Nucleic Acids Res 31:, 3406–3415. [CrossRef] [PubMed]
    [Google Scholar]
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