1887

Abstract

(PSVs) are widely distributed in pig populations; however, little information on their evolutionary history and the mechanisms driving their divergence is available. Therefore, in the present study, 241 fecal samples and 91 intestinal contents collected from pigs at 26 farms in Hunan, China, were tested for the presence of PSVs. The overall PSV positivity rate was 46.39 %, with a particularly high infection rate detected in nursery and fattening pigs. A total of 29 PSV strains (PSV-HuNs) were isolated, with these showing high genetic diversity based on phylogenetic and pairwise distance analyses of the capsid-protein gene sequences. Incongruence between phylognetic trees of the capsid-protein and 3CD regions indicated frequent recombination within the PSV-HuNs, and a putative recombinant hotspot near the 3′ end of the P1 region was identified. Our results suggested that recombination played an important role in driving PSV genetic diversity and evolution.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000951
2017-11-01
2024-12-03
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/11/2738.html?itemId=/content/journal/jgv/10.1099/jgv.0.000951&mimeType=html&fmt=ahah

References

  1. ICTV 2016; International Committee on Taxonomy of Viruses. http://ictvonline.org/virusTaxonomy.asp (accessed 17.7.18)
  2. Krumbholz A, Dauber M, Henke A, Birch-Hirschfeld E, Knowles NJ et al. Sequencing of porcine enterovirus groups II and III reveals unique features of both virus groups. J Virol 2002; 76:5813–5821 [View Article][PubMed]
    [Google Scholar]
  3. Chen J, Chen F, Zhou Q, Li W, Song Y et al. Complete genome sequence of a novel porcine Sapelovirus strain YC2011 isolated from piglets with diarrhea. J Virol 2012; 86:10898 [View Article][PubMed]
    [Google Scholar]
  4. Son KY, Kim DS, Kwon J, Choi JS, Kang MI et al. Full-length genomic analysis of Korean porcine Sapelovirus strains. PLoS One 2014; 9:e107860 [View Article][PubMed]
    [Google Scholar]
  5. Donin DG, Leme Rdea, Alfieri AF, Alberton GC, Alfieri AA. Molecular survey of porcine teschovirus, porcine sapelovirus, and enterovirus G in captive wild boars (Sus scrofa scrofa) of Paraná state, Brazil. Pesq Vet Bras 2015; 35:403–408 [View Article]
    [Google Scholar]
  6. Cano-Gómez C, García-Casado MA, Soriguer R, Palero F, Jiménez-Clavero MA. Teschoviruses and sapeloviruses in faecal samples from wild boar in Spain. Vet Microbiol 2013; 165:115–122 [View Article][PubMed]
    [Google Scholar]
  7. 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 [View Article][PubMed]
    [Google Scholar]
  8. 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 [View Article][PubMed]
    [Google Scholar]
  9. Arruda PH, Arruda BL, Schwartz KJ, Vannucci F, Resende T et al. Detection of a novel sapelovirus in central nervous tissue of pigs with polioencephalomyelitis in the USA. Transbound Emerg Dis 2017; 64:311–315 [View Article][PubMed]
    [Google Scholar]
  10. Schock A, Gurrala R, Fuller H, Foyle L, Dauber M et al. Investigation into an outbreak of encephalomyelitis caused by a neuroinvasive porcine sapelovirus in the United Kingdom. Vet Microbiol 2014; 172:381–389 [View Article][PubMed]
    [Google Scholar]
  11. Lan D, Ji W, Yang S, Cui L, Yang Z et al. Isolation and characterization of the first Chinese porcine sapelovirus strain. Arch Virol 2011; 156:1567–1574 [View Article][PubMed]
    [Google Scholar]
  12. 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 [View Article][PubMed]
    [Google Scholar]
  13. Abe M, Ito N, Sakai K, Kaku Y, Oba M et al. A novel sapelovirus-like virus isolation from wild boar. Virus Genes 2011; 43:243–248 [View Article][PubMed]
    [Google Scholar]
  14. Chen Q, Zheng Y, Guo B, Zhang J, Yoon KJ et al. Complete genome sequence of porcine sapelovirus strain USA/IA33375/2015 identified in the United States. Genome Announc 2016; 4:e01055-16 [View Article][PubMed]
    [Google Scholar]
  15. Ray PK, Desingu PA, Kumari S, John JK, Sethi M et al. Porcine sapelovirus among diarrhoeic piglets in India. Transbound Emerg Dis 2017 [View Article][PubMed]
    [Google Scholar]
  16. Son KY, Kim DS, Matthijnssens J, Kwon HJ, Park JG et al. Molecular epidemiology of Korean porcine sapeloviruses. Arch Virol 2014; 159:1175–1180 [View Article][PubMed]
    [Google Scholar]
  17. Yang T, Li R, Peng W, Ge M, Luo B et al. First isolation and genetic characteristics of porcine sapeloviruses in Hunan, China. Arch Virol 2017; 162:1589–1597 [View Article][PubMed]
    [Google Scholar]
  18. Bak GY, Kang MI, Son KY, Park JG, Kim DS et al. Occurrence and molecular characterization of Sapelovirus A in diarrhea and non-diarrhea feces of different age group pigs in one Korean pig farm. J Vet Med Sci 2017; 78:1911–1914 [View Article][PubMed]
    [Google Scholar]
  19. Racaniello VR. Picornaviridae: the viruses and their replication. In Knipe DMHP, Lamb RAMM. (editors) Fields Virology, 6th ed. 2001 pp. 455–457
    [Google Scholar]
  20. Maclachlan N, Dubovi J. Picornaviridae. In Fenner’s Veterinary Virology, 5th ed. 2017 pp. 478–481
    [Google Scholar]
  21. Horsington JJ, Gilkerson JR, Hartley CA. Mapping B-cell epitopes in equine rhinitis B viruses and identification of a neutralising site in the VP1 C-terminus. Vet Microbiol 2012; 155:128–136 [View Article][PubMed]
    [Google Scholar]
  22. Kriegshäuser G, Wutz G, Lea S, Stuart D, Skern T et al. Model of the equine rhinitis A virus capsid: identification of a major neutralizing immunogenic site. J Gen Virol 2003; 84:2365–2373 [View Article][PubMed]
    [Google Scholar]
  23. Mateu MG. Antibody recognition of picornaviruses and escape from neutralization: a structural view. Virus Res 1995; 38:1–24 [View Article][PubMed]
    [Google Scholar]
  24. Pulli T, Roivainen M, Hovi T, Hyypiä T. Induction of neutralizing antibodies by synthetic peptides representing the C terminus of coxsackievirus A9 capsid protein VP1. J Gen Virol 1998; 79:2249–2253 [View Article][PubMed]
    [Google Scholar]
  25. Foo DG, Alonso S, Phoon MC, Ramachandran NP, Chow VT et al. Identification of neutralizing linear epitopes from the VP1 capsid protein of Enterovirus 71 using synthetic peptides. Virus Res 2007; 125:61–68 [View Article][PubMed]
    [Google Scholar]
  26. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article][PubMed]
    [Google Scholar]
  27. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012; 29:1969–1973 [View Article][PubMed]
    [Google Scholar]
  28. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9:772 [View Article][PubMed]
    [Google Scholar]
  29. Hu L, Zhang Y, Hong M, Zhu S, Yan D et al. Phylogenetic evidence for multiple intertypic recombinations in enterovirus B81 strains isolated in Tibet, China. Sci Rep 2014; 4:6035 [View Article][PubMed]
    [Google Scholar]
  30. Junttila N, Lévêque N, Magnius LO, Kabue JP, Muyembe-Tamfum JJ et al. Complete coding regions of the prototypes enterovirus B93 and C95: phylogenetic analyses of the P1 and P3 regions of EV-B and EV-C strains. J Med Virol 2015; 87:485–497 [View Article][PubMed]
    [Google Scholar]
  31. Zell R, Dauber M, Krumbholz A, Henke A, Birch-Hirschfeld E et al. Porcine teschoviruses comprise at least eleven distinct serotypes: molecular and evolutionary aspects. J Virol 2001; 75:1620–1631 [View Article][PubMed]
    [Google Scholar]
  32. das B, Mohapatra JK, Pande V, Subramaniam S, Sanyal A. Evolution of foot-and-mouth disease virus serotype A capsid coding (P1) region on a timescale of three decades in an endemic context. Infect Genet Evol 2016; 41:36–46 [View Article][PubMed]
    [Google Scholar]
  33. Oberste MS, Maher K, Kilpatrick DR, Pallansch MA. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 1999; 73:1941–1948[PubMed]
    [Google Scholar]
  34. Subramaniam S, Mohapatra JK, Das B, Sharma GK, Biswal JK et al. Capsid coding region diversity of re-emerging lineage C foot-and-mouth disease virus serotype Asia1 from India. Arch Virol 2015; 160:1751–1759 [View Article][PubMed]
    [Google Scholar]
  35. Sozzi E, Barbieri I, Lavazza A, Lelli D, Moreno A et al. Molecular characterization and phylogenetic analysis of VP1 of porcine enteric picornaviruses isolates in Italy. Transbound Emerg Dis 2010; 57:434–442 [View Article][PubMed]
    [Google Scholar]
  36. Santti J, Hyypiä T, Kinnunen L, Salminen M. Evidence of recombination among enteroviruses. J Virol 1999; 73:8741–8749[PubMed]
    [Google Scholar]
  37. Belalov IS, Isaeva OV, Lukashev AN. Recombination in hepatitis A virus: evidence for reproductive isolation of genotypes. J Gen Virol 2011; 92:860–872 [View Article][PubMed]
    [Google Scholar]
  38. Jamal SM, Ferrari G, Ahmed S, Normann P, Belsham GJ. Molecular characterization of serotype Asia-1 foot-and-mouth disease viruses in Pakistan and Afghanistan; emergence of a new genetic Group and evidence for a novel recombinant virus. Infect Genet Evol 2011; 11:2049–2062 [View Article][PubMed]
    [Google Scholar]
  39. Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE et al. Recombination in circulating enteroviruses. J Virol 2003; 77:10423–10431 [View Article][PubMed]
    [Google Scholar]
  40. 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 [View Article][PubMed]
    [Google Scholar]
  41. Oberste MS, Peñaranda S, Pallansch MA. RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J Virol 2004; 78:2948–2955 [View Article][PubMed]
    [Google Scholar]
  42. Lindberg AM, Andersson P, Savolainen C, Mulders MN, Hovi T. Evolution of the genome of Human enterovirus B: incongruence between phylogenies of the VP1 and 3CD regions indicates frequent recombination within the species. J Gen Virol 2003; 84:1223–1235 [View Article][PubMed]
    [Google Scholar]
  43. Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol 2015; 1:v3 [View Article][PubMed]
    [Google Scholar]
  44. 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[PubMed]
    [Google Scholar]
  45. Dimmock NJ, Easton AJ, Leppard KN. The evolution of viruses. Introduction to Modern Virology, 7th ed. John Wiley & Sons; 2016 pp. 39–43
    [Google Scholar]
  46. Lukashev AN. Recombination among picornaviruses. Rev Med Virol 2010; 20:327–337 [View Article][PubMed]
    [Google Scholar]
  47. Simmonds P. Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J Virol 2006; 80:11124–11140 [View Article][PubMed]
    [Google Scholar]
  48. Tosh C, Hemadri D, Sanyal A. Evidence of recombination in the capsid-coding region of type A foot-and-mouth disease virus. J Gen Virol 2002; 83:2455–2460 [View Article][PubMed]
    [Google Scholar]
  49. 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 [View Article][PubMed]
    [Google Scholar]
  50. Wang B, Tian ZJ, Gong DQ, Li DY, Wang Y et al. Isolation of serotype 2 porcine teschovirus in China: evidence of natural recombination. Vet Microbiol 2010; 146:138–143 [View Article][PubMed]
    [Google Scholar]
  51. Holmblat B, Jégouic S, Muslin C, Blondel B, Joffret ML et al. Nonhomologous recombination between defective poliovirus and coxsackievirus genomes suggests a new model of genetic plasticity for picornaviruses. MBio 2014; 5:e01119-14e01119-19 [View Article][PubMed]
    [Google Scholar]
/content/journal/jgv/10.1099/jgv.0.000951
Loading
/content/journal/jgv/10.1099/jgv.0.000951
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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