1887

Abstract

The genetic diversity of enterovirus G (EV-G) was investigated in the wild-boar population in Japan. EV-G-specific reverse transcription PCR demonstrated 30 (37.5 %) positives out of 80 faecal samples. Of these, viral protein 1 (VP1) fragments of 20 samples were classified into G1 (3 samples), G4 (1 sample), G6 (2 samples), G8 (4 samples), G11 (1 sample), G12 (7 samples), G14 (1 sample) and G17 (1 sample), among which 11 samples had a papain-like cysteine protease (PL-CP) sequence, believed to be the first discoveries in G1 (2 samples) or G17 (1 sample) wild-boar EV-Gs, and in G8 (2 samples) or G12 (6 samples) EV-Gs from any animals. Sequences of the non-structural protein regions were similar among EV-Gs possessing the PL-CP sequence (PL-CP EV-Gs) regardless of genotype or origin, suggesting the existence of a common ancestor for these strains. Interestingly, for the two G8 and two G12 samples, the genome sequences contained two versions, with or without the PL-CP sequence, together with the homologous 2C/PL-CP and PL-CP/3A junction sequences, which may explain how the recombination and deletion of the PL-CP sequences occured in the PL-CP EV-G genomes. These findings shed light on the genetic plasticity and evolution of EV-G.

Funding
This study was supported by the:
  • Makoto Nagai , Japan Society for the Promotion of Science , (Award 18K05977)
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/content/journal/jgv/10.1099/jgv.0.001446
2020-06-17
2020-09-22
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References

  1. Lulla V, Dinan AM, Hosmillo M, Chaudhry Y, Sherry L et al. An upstream protein-coding region in enteroviruses modulates virus infection in gut epithelial cells. Nat Microbiol 2019; 4:280–292 [CrossRef][PubMed]
    [Google Scholar]
  2. Knowles NJ, Hovi T, Hyypiä T, King AMQ, Lindberg AM et al. Picornaviridae. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. (editors) Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses London, San Diego CA: Elsevier; 2012
    [Google Scholar]
  3. Brown BA, Maher K, Flemister MR, Naraghi-Arani P, Uddin M et al. Resolving ambiguities in genetic typing of human enterovirus species C clinical isolates and identification of enterovirus 96, 99 and 102. J Gen Virol 2009; 90:1713–1723 [CrossRef][PubMed]
    [Google Scholar]
  4. Tapparel C, Siegrist F, Petty TJ, Kaiser L. Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 2013; 14:282–293 [CrossRef][PubMed]
    [Google Scholar]
  5. Van Dung N, Anh PH, Van Cuong N, Hoa NT, Carrique-Mas J et al. Prevalence, genetic diversity and recombination of species G enteroviruses infecting pigs in Vietnam. J Gen Virol 2014; 95:549–556 [CrossRef][PubMed]
    [Google Scholar]
  6. 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][PubMed]
    [Google Scholar]
  7. Vilar MJ, Peralta B, García-Bocanegra I, Simon-Grifé M, Bensaid A et al. Distribution and genetic characterization of Enterovirus G and Sapelovirus A in six Spanish swine herds. Virus Res 2016; 215:42–49 [CrossRef][PubMed]
    [Google Scholar]
  8. Bunke J, Receveur K, Oeser AC, Fickenscher H, Zell R et al. High genetic diversity of porcine enterovirus G in Schleswig-Holstein, Germany. Arch Virol 2018; 163:489–493 [CrossRef][PubMed]
    [Google Scholar]
  9. Anbalagan S, Hesse RA, Hause BM. First identification and characterization of porcine enterovirus G in the United States. PLoS One 2014; 9:e97517 [CrossRef]
    [Google Scholar]
  10. Donin DG, de Arruda Leme R, Alfieri AF, Alberton GC, Alfieri AA. First report of porcine teschovirus (PTV), porcine sapelovirus (PSV) and enterovirus G (EV-G) in pig herds of Brazil. Trop Anim Health Prod 2014; 46:523–528 [CrossRef][PubMed]
    [Google Scholar]
  11. Lu L, Van Dung N, Bryant JE, Carrique-Mas J, Van Cuong N et al. Evolution and phylogeographic dissemination of endemic porcine picornaviruses in Vietnam. Virus Evol 2016; 2:vew001 [CrossRef][PubMed]
    [Google Scholar]
  12. Yang S, Wang Y, Shen Q, Zhang W, Hua X. Prevalence of porcine enterovirus 9 in pigs in middle and eastern China. Virol J 2013; 10:99 [CrossRef][PubMed]
    [Google Scholar]
  13. Knowles NJ. The association of group III porcine enteroviruses with epithelial tissue. Vet Rec 1988; 122:441–442 [CrossRef][PubMed]
    [Google Scholar]
  14. Knowles NJ. Porcine enteric picornaviruses. In Straw BE, Zimmermann JJ, D'Allaire SD, Taylor DJ. eds Diseases of Swine, 9th edn. Ames, IA: Blackwell Publishing; 2006 pp 337–345
    [Google Scholar]
  15. Knutson TP, Velayudhan BT, Marthaler DG. A porcine enterovirus G associated with enteric disease contains a novel papain-like cysteine protease. J Gen Virol 2017; 98:1305–1310 [CrossRef][PubMed]
    [Google Scholar]
  16. Shang P, Misra S, Hause B, Fang Y. A naturally occurring recombinant enterovirus expresses a torovirus deubiquitinase. J Virol 2017; 91:e00450-17 [CrossRef][PubMed]
    [Google Scholar]
  17. Conceição-Neto N, Theuns S, Cui T, Zeller M, Yinda CK et al. Identification of an enterovirus recombinant with a torovirus-like gene insertion during a diarrhea outbreak in fattening pigs. Virus Evol 2017; 3:vex024 [CrossRef][PubMed]
    [Google Scholar]
  18. Wang Y, Zhang W, Liu Z, Fu X, Yuan J et al. Full-length and defective enterovirus G genomes with distinct torovirus protease insertions are highly prevalent on a Chinese pig farm. Arch Virol 2018; 163:2471–2476 [CrossRef][PubMed]
    [Google Scholar]
  19. Lee S, Lee C. First detection of novel enterovirus G recombining a torovirus papain-like protease gene associated with diarrhoea in swine in South Korea. Transbound Emerg Dis 2019; 66:1023–1028 [CrossRef][PubMed]
    [Google Scholar]
  20. Tsuchiaka S, Naoi Y, Imai R, Masuda T, Ito M et al. Genetic diversity and recombination of enterovirus G strains in Japanese pigs: high prevalence of strains carrying a papain-like cysteine protease sequence in the enterovirus G population. PLoS One 2018; 13:e0190819 [CrossRef][PubMed]
    [Google Scholar]
  21. Imai R, Nagai M, Oba M, Sakaguchi S, Ujike M et al. A novel defective recombinant porcine enterovirus G virus carrying a porcine torovirus papain-like cysteine protease gene and a putative anti-apoptosis gene in place of viral structural protein genes. Infect Genet Evol 2019; 75:103975 [CrossRef][PubMed]
    [Google Scholar]
  22. Beld M, Minnaar R, Weel J, Sol C, Damen M et al. Highly sensitive assay for detection of enterovirus in clinical specimens by reverse transcription-PCR with an armored RNA internal control. J Clin Microbiol 2004; 42:3059–3064 [CrossRef][PubMed]
    [Google Scholar]
  23. Nagai M, Omatsu T, Aoki H, Otomaru K, Uto T et al. Full genome analysis of bovine astrovirus from fecal samples of cattle in Japan: identification of possible interspecies transmission of bovine astrovirus. Arch Virol 2015; 160:2491–2501 [CrossRef][PubMed]
    [Google Scholar]
  24. Oka T, Doan YH, Shimoike T, Haga K, Takizawa T. First complete genome sequences of genogroup V, genotype 3 porcine sapoviruses: common 5'-terminal genomic feature of sapoviruses. Virus Genes 2017; 53:848–855 [CrossRef][PubMed]
    [Google Scholar]
  25. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [CrossRef][PubMed]
    [Google Scholar]
  26. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [CrossRef][PubMed]
    [Google Scholar]
  27. Lole KS, Bollinger RC, Paranjape RS, Gadkari D, Kulkarni SS et al. Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 1999; 73:152–160 [CrossRef][PubMed]
    [Google Scholar]
  28. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 2015; 1:vev003 [CrossRef][PubMed]
    [Google Scholar]
  29. Meier R, Ryser-Degiorgis M. Wild boar and infectious diseases: evaluation of the current risk to human and domestic animal health in Switzerland: a review. Schweiz Arch Tierheilkd 2018; 160:443–460 [CrossRef][PubMed]
    [Google Scholar]
  30. Meng XJ, Lindsay DS, Sriranganathan N. Wild boars as sources for infectious diseases in livestock and humans. Philos Trans R Soc Lond B Biol Sci 2009; 364:2697–2707 [CrossRef][PubMed]
    [Google Scholar]
  31. Ohdachi SD, Ishibashi Y, Iwasa MA, Saitoh T. The Wild Mammals of Japan 544 Kyoto: Shoukadoh Book Sellers; 2009
    [Google Scholar]
  32. Yamazaki Y, Adachi F, Sawamura A. Multiple origins and admixture of recently expanding Japanese wild boar (Sus scrofa leucomystax) populations in Toyama Prefecture of Japan. Zoolog Sci 2016; 33:38–43 [CrossRef][PubMed]
    [Google Scholar]
  33. Boros Á, Pankovics P, Knowles NJ, Reuter G. Natural interspecies recombinant bovine/porcine enterovirus in sheep. J Gen Virol 2012; 93:1941–1951 [CrossRef][PubMed]
    [Google Scholar]
  34. Prodělalová J. The survey of porcine teschoviruses, sapeloviruses and enteroviruses B infecting domestic pigs and wild boars in the Czech Republic between 2005 and 2011. Infect Genet Evol 2012; 12:1447–1451 [CrossRef][PubMed]
    [Google Scholar]
  35. Moutelíková R, Dufková L, Kamler J, Drimaj J, Plhal R et al. Epidemiological survey of enteric viruses in wild boars in the Czech Republic: first evidence of close relationship between wild boar and human rotavirus A strains. Vet Microbiol 2016; 193:28–35 [CrossRef][PubMed]
    [Google Scholar]
  36. Hicks AL, Duffy S. Genus-specific substitution rate variability among picornaviruses. J Virol 2011; 85:7942–7947 [CrossRef][PubMed]
    [Google Scholar]
  37. Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE et al. Recombination in circulating enteroviruses. J Virol 2003; 77:10423–10431 [CrossRef][PubMed]
    [Google Scholar]
  38. Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE et al. Recombination in circulating Human enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 2005; 86:3281–3290 [CrossRef]
    [Google Scholar]
  39. Lukashev AN, Shumilina EY, Belalov IS, Ivanova OE, Eremeeva TP et al. Recombination strategies and evolutionary dynamics of the Human enterovirus A global gene pool. J Gen Virol 2014; 95:868–873 [CrossRef][PubMed]
    [Google Scholar]
  40. Savolainen-Kopra C, Blomqvist S. Mechanisms of genetic variation in polioviruses. Rev Med Virol 2010; 20:358–371 [CrossRef][PubMed]
    [Google Scholar]
  41. Simmonds P, Welch J. Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 2006; 80:483–493 [CrossRef][PubMed]
    [Google Scholar]
  42. Nagy PD, Bujarski JJ. Efficient system of homologous RNA recombination in brome mosaic virus: sequence and structure requirements and accuracy of crossovers. J Virol 1995; 69:131–140 [CrossRef][PubMed]
    [Google Scholar]
  43. Banner LR, Lai MM. Random nature of coronavirus RNA recombination in the absence of selection pressure. Virology 1991; 185:441–445 [CrossRef][PubMed]
    [Google Scholar]
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