1887

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Volume 103, Issue 2

Genomic diversity and intragenic recombination of species C rotaviruses No Access

Abstract

Rotavirus C (RVC) is a major cause of diarrhoea in swine, cattle, and humans worldwide. RVC exhibits sequence diversity in all 11 genes, especially in VP4 and VP7, and all segment-based genotyping has been performed similar to rotavirus A. To date, recombination events have been reported in rotavirus A and B. However, there are no reports describing gene recombination of RVC, except for recombination in NSP3 between RVC and rotavirus H. In this study, nine porcine RVC strains identified in Japanese pigs were completely sequenced and analysed together with RVC sequences from the GenBank database. The analyses showed that sequences of the VP4, VP2, and NSP1 of several porcine RVC strains did not branch with any of those of the RVC strains in the GenBank database, suggesting new genotypes. Several homologous recombination events, between or within genotypes, were identified in the VP4, VP7, VP2, NSP1, and NSP3 genes. Of these, nine, one, and one intergenotypic recombination events in the VP4, VP2, and NSP3 genes, respectively, were supported with sufficient statistical values. Although these findings suggest occurrences of the intragenic recombination events in the RVC genome, potential sequence errors and poor sequence assemblies in the databases should be watched with care. The results in this study present data about the important recombination events of the RVCs, which influence evolution of the virus by aiding them to gain genetic diversity and plasticity, although further sequence data will be necessary to obtain more comprehensive understanding of such mechanisms.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): complete genome analyses , genotypes , intragenic recombination and rotavirus C
Funding
This study was supported by the:
  • JSPS KAKENHI (Award 18K05977 and 21K05947)
    • Principle Award Recipient: MakotoNagai
© 2022 The Authors
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/content/journal/jgv/10.1099/jgv.0.001703
2022-02-17
2024-04-19
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References

  1. Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Van Ranst M et al. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch Virol 2012; 157:1177–1182 [View Article] [PubMed]
     [Google Scholar]
  2. Mihalov-Kovács E, Gellért Á, Marton S, Farkas SL, Fehér E et al. Candidate new rotavirus species in sheltered dogs, Hungary. Emerg Infect Dis 2015; 21:660–663 [View Article] [PubMed]
     [Google Scholar]
  3. Bányai K, Kemenesi G, Budinski I, Földes F, Zana B et al. Candidate new rotavirus species in Schreiber’s bats, Serbia. Infect Genet Evol 2017; 48:19–26 [View Article] [PubMed]
     [Google Scholar]
  4. Estes MK, Greenberg HB. Rotaviruses. In Knipe DM, Howley PM. eds Fields Virology, 6th. edn Philadelphia: Lippincott, Williams & Wilkins; 2007 pp 1347–1395
     [Google Scholar]
  5. Saif LJ, Bohl EH, Theil KW, Cross RF, House JA. Rotavirus-like, calicivirus-like, and 23-nm virus-like particles associated with diarrhea in young pigs. J Clin Microbiol 1980; 12:105–111 [View Article] [PubMed]
     [Google Scholar]
  6. Kim Y, Chang KO, Straw B, Saif LJ. Characterization of group C rotaviruses associated with diarrhea outbreaks in feeder pigs. J Clin Microbiol 1999; 37:1484–1488 [View Article] [PubMed]
     [Google Scholar]
  7. Martella V, Bányai K, Lorusso E, Bellacicco AL, Decaro N et al. Prevalence of group C rotaviruses in weaning and post-weaning pigs with enteritis. Vet Microbiol 2007; 123:26–33 [View Article] [PubMed]
     [Google Scholar]
  8. Marthaler D, Rossow K, Culhane M, Collins J, Goyal S et al. Identification, phylogenetic analysis and classification of porcine group C rotavirus VP7 sequences from the United States and Canada. Virology 2013; 446:189–198 [View Article] [PubMed]
     [Google Scholar]
  9. Amimo JO, Vlasova AN, Saif LJ. Prevalence and genetic heterogeneity of porcine group C rotaviruses in nursing and weaned piglets in Ohio, USA and identification of a potential new VP4 genotype. Vet Microbiol 2013; 164:27–38 [View Article] [PubMed]
     [Google Scholar]
  10. Peñaranda ME, Cubitt WD, Sinarachatanant P, Taylor DN, Likanonsakul S et al. Group C rotavirus infections in patients with diarrhea in Thailand, Nepal, and England. J Infect Dis 1989; 160:392–397 [View Article] [PubMed]
     [Google Scholar]
  11. Matsumoto K, Hatano M, Kobayashi K, Hasegawa A, Yamazaki S et al. An outbreak of gastroenteritis associated with acute rotaviral infection in schoolchildren. J Infect Dis 1989; 160:611–615 [View Article] [PubMed]
     [Google Scholar]
  12. Kuzuya M, Fujii R, Hamano M, Yamada M, Shinozaki K et al. Survey of human group C rotaviruses in Japan during the winter of 1992 to 1993. J Clin Microbiol 1998; 36:6–10 [View Article] [PubMed]
     [Google Scholar]
  13. Oishi I, Yamazaki K, Minekawa Y. An occurrence of diarrheal cases associated with group C rotavirus in adults. Microbiol Immunol 1993; 37:505–509 [View Article] [PubMed]
     [Google Scholar]
  14. Hamano M, Kuzuya M, Fujii R, Ogura H, Mori T et al. Outbreak of acute gastroenteritis caused by human group C rotavirus in a primary school. Jpn J Infect Dis 1999; 52:170–171 [PubMed]
     [Google Scholar]
  15. Castello AA, Argüelles MH, Villegas GA, Olthoff A, Glikmann G. Incidence and prevalence of human group C rotavirus infections in Argentina. J Med Virol 2002; 67:106–112 [View Article] [PubMed]
     [Google Scholar]
  16. Schnagl RD, Boniface K, Cardwell P, McCarthy D, Ondracek C et al. Incidence of group C human rotavirus in central Australia and sequence variation of the VP7 and VP4 genes. J Clin Microbiol 2004; 42:2127–2133 [View Article] [PubMed]
     [Google Scholar]
  17. Rahman M, Banik S, Faruque ASG, Taniguchi K, Sack DA et al. Detection and characterization of human group C rotaviruses in Bangladesh. J Clin Microbiol 2005; 43:4460–4465 [View Article] [PubMed]
     [Google Scholar]
  18. Chang KO, Nielsen PR, Ward LA, Saif LJ. Dual infection of gnotobiotic calves with bovine strains of group A and porcine-like group C rotaviruses influences pathogenesis of the group C rotavirus. J Virol 1999; 73:9284–9293 [View Article] [PubMed]
     [Google Scholar]
  19. Mawatari T, Taneichi A, Kawagoe T, Hosokawa M, Togashi K et al. Detection of a bovine group C rotavirus from adult cows with diarrhea and reduced milk production. J Vet Med Sci 2004; 66:887–890 [View Article] [PubMed]
     [Google Scholar]
  20. Tsunemitsu H, Jiang B, Saif LJ. Detection of group C rotavirus antigens and antibodies in animals and humans by enzyme-linked immunosorbent assays. J Clin Microbiol 1992; 30:2129–2134 [View Article] [PubMed]
     [Google Scholar]
  21. Otto P, Schulze P, Herbst W. Demonstration of group C rotaviruses in fecal samples of diarrheic dogs in Germany. Arch Virol 1999; 144:2467–2473 [View Article] [PubMed]
     [Google Scholar]
  22. Torres-Medina A. Isolation of an atypical rotavirus causing diarrhea in neonatal ferrets. Lab Anim Sci 1987; 37:167–171 [PubMed]
     [Google Scholar]
  23. Xie XT, Macdonald RE, Tapscott B, Nagy E, Turner PV. Detection of Astrovirus, Rotavirus C, and Hepatitis E Viral RNA in Adult and Juvenile Farmed Mink (Neovison vison). Front Vet Sci 2018; 5:132 [View Article] [PubMed]
     [Google Scholar]
  24. Collins PJ, Martella V, O’Shea H. Detection and characterization of group C rotaviruses in asymptomatic piglets in Ireland. J Clin Microbiol 2008; 46:2973–2979 [View Article] [PubMed]
     [Google Scholar]
  25. Jeong Y-J, Matthijnssens J, Kim D-S, Kim J-Y, Alfajaro MM et al. Genetic diversity of the VP7, VP4 and VP6 genes of Korean porcine group C rotaviruses. Vet Microbiol 2015; 176:61–69 [View Article] [PubMed]
     [Google Scholar]
  26. Tsunemitsu H, Saif LJ, Jiang BM, Shimizu M, Hiro M et al. Isolation, characterization, and serial propagation of a bovine group C rotavirus in a monkey kidney cell line (MA104). J Clin Microbiol 1991; 29:2609–2613 [View Article] [PubMed]
     [Google Scholar]
  27. Tsunemitsu H, Jiang B, Saif LJ. Sequence comparison of the VP7 gene encoding the outer capsid glycoprotein among animal and human group C rotaviruses. Arch Virol 1996; 141:705–713 [View Article] [PubMed]
     [Google Scholar]
  28. Soma J, Tsunemitsu H, Miyamoto T, Suzuki G, Sasaki T et al. Whole-genome analysis of two bovine rotavirus C strains: Shintoku and Toyama. J Gen Virol 2013; 94:128–135 [View Article] [PubMed]
     [Google Scholar]
  29. Mawatari T, Hirano K, Tsunemitsu H, Suzuki T. Whole-genome analysis of bovine rotavirus species C isolates obtained in Yamagata, Japan, 2003-2010. J Gen Virol 2014; 95:1117–1125 [View Article] [PubMed]
     [Google Scholar]
  30. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T et al. Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol 2008; 82:3204–3219 [View Article] [PubMed]
     [Google Scholar]
  31. Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K et al. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 2008; 153:1621–1629 [View Article] [PubMed]
     [Google Scholar]
  32. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Bányai K et al. Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 2011; 156:1397–1413 [View Article] [PubMed]
     [Google Scholar]
  33. Suzuki T, Hasebe A. A provisional complete genome-based genotyping system for rotavirus species C from terrestrial mammals. J Gen Virol 2017; 98:2647–2662 [View Article] [PubMed]
     [Google Scholar]
  34. Wang Y, Porter EP, Lu N, Zhu C, Noll LW et al. Whole-genome classification of rotavirus C and genetic diversity of porcine strains in the USA. J Gen Virol 2021; 102: [View Article]
     [Google Scholar]
  35. Matthijnssens J, Van Ranst M. Genotype constellation and evolution of group A rotaviruses infecting humans. Curr Opin Virol 2012; 2:426–433 [View Article] [PubMed]
     [Google Scholar]
  36. Phan MVT, Anh PH, Cuong NV, Munnink BBO, van der Hoek L et al. Unbiased whole-genome deep sequencing of human and porcine stool samples reveals circulation of multiple groups of rotaviruses and a putative zoonotic infection. Virus Evol 2016; 2:vew027 [View Article] [PubMed]
     [Google Scholar]
  37. 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]
  38. Lukashev AN. Role of Recombination in Evolution of Enteroviruses. Rev Med Virol 2005; 15:157–167 [View Article] [PubMed]
     [Google Scholar]
  39. Pérez-Losada M, Arenas M, Galán JC, Palero F, González-Candelas F. Recombination in viruses: mechanisms, methods of study, and evolutionary consequences. Infection, Genetics and Evolution 2015; 30:296–307 [View Article]
     [Google Scholar]
  40. McDonald SM, Nelson MI, Turner PE, Patton JT. Reassortment in segmented RNA viruses: mechanisms and outcomes. Nat Rev Microbiol 2016; 14:448–460 [View Article] [PubMed]
     [Google Scholar]
  41. Simon-Loriere E, Holmes EC. Why do RNA viruses recombine?. Nat Rev Microbiol 2011; 9:617–626 [View Article] [PubMed]
     [Google Scholar]
  42. Suzuki Y, Gojobori T, Nakagomi O. Intragenic recombinations in rotaviruses. FEBS Lett 1998; 427:183–187 [View Article] [PubMed]
     [Google Scholar]
  43. Parra GI, Bok K, Martínez M, Gomez JA. Evidence of rotavirus intragenic recombination between two sublineages of the same genotype. J Gen Virol 2004; 85:1713–1716 [View Article] [PubMed]
     [Google Scholar]
  44. Phan TG, Okitsu S, Maneekarn N, Ushijima H. Genetic heterogeneity, evolution and recombination in emerging G9 rotaviruses. Infect Genet Evol 2007; 7:656–663 [View Article] [PubMed]
     [Google Scholar]
  45. Phan TG, Okitsu S, Maneekarn N, Ushijima H. Evidence of intragenic recombination in G1 rotavirus VP7 genes. J Virol 2007; 81:10188–10194 [View Article] [PubMed]
     [Google Scholar]
  46. Cao D, Barro M, Hoshino Y. Porcine rotavirus bearing an aberrant gene stemming from an intergenic recombination of the NSP2 and NSP5 genes is defective and interfering. J Virol 2008; 82:6073–6077 [View Article] [PubMed]
     [Google Scholar]
  47. Martínez-Laso J, Román A, Rodriguez M, Cervera I, Head J et al. Diversity of the G3 genes of human rotaviruses in isolates from Spain from 2004 to 2006: cross-species transmission and inter-genotype recombination generates alleles. J Gen Virol 2009; 90:935–943 [View Article] [PubMed]
     [Google Scholar]
  48. Donker NC, Boniface K, Kirkwood CD. Phylogenetic analysis of rotavirus A NSP2 gene sequences and evidence of intragenic recombination. Infect Genet Evol 2011; 11:1602–1607 [View Article] [PubMed]
     [Google Scholar]
  49. Jere KC, Mlera L, Page NA, van Dijk AA, O’Neill HG. Whole genome analysis of multiple rotavirus strains from a single stool specimen using sequence-independent amplification and 454® pyrosequencing reveals evidence of intergenotype genome segment recombination. Infect Genet Evol 2011; 11:2072–2082 [View Article] [PubMed]
     [Google Scholar]
  50. Esona MD, Roy S, Rungsrisuriyachai K, Sanchez J, Vasquez L et al. Characterization of a triple-recombinant, reassortant rotavirus strain from the Dominican Republic. J Gen Virol 2017; 98:134–142 [View Article] [PubMed]
     [Google Scholar]
  51. Jing Z, Zhang X, Shi H, Chen J, Shi D et al. A G3P[13] porcine group A rotavirus emerging in China is a reassortant and a natural recombinant in the VP4 gene. Transbound Emerg Dis 2018; 65:e317–e328 [View Article] [PubMed]
     [Google Scholar]
  52. Hoxie I, Dennehy JJ. Intragenic recombination influences rotavirus diversity and evolution. Virus Evol 2020; 6:vez059 [View Article]
     [Google Scholar]
  53. Phan T, Ide T, Komoto S, Khamrin P, Pham NTK et al. Genomic analysis of group A rotavirus G12P[8] including a new Japanese strain revealed evidence for intergenotypic recombination in VP7 and VP4 genes. Infect Genet Evol 2021; 87:104656 [View Article] [PubMed]
     [Google Scholar]
  54. Marthaler D, Suzuki T, Rossow K, Culhane M, Collins J et al. VP6 genetic diversity, reassortment, intragenic recombination and classification of rotavirus B in American and Japanese pigs. Vet Microbiol 2014; 172:359–366 [View Article] [PubMed]
     [Google Scholar]
  55. Suzuki T, Inoue D. Full genome-based genotyping system for rotavirus H and detection of potential gene recombination in nonstructural protein 3 between porcine rotavirus H and rotavirus C. J Gen Virol 2018; 99:1582–1589 [View Article] [PubMed]
     [Google Scholar]
  56. 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 [View Article] [PubMed]
     [Google Scholar]
  57. Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article] [PubMed]
     [Google Scholar]
  58. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
     [Google Scholar]
  59. 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 [View Article] [PubMed]
     [Google Scholar]
  60. 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 [View Article]
     [Google Scholar]
  61. Lorenz R, Bernhart SH, Höner Zu Siederdissen C, Tafer H, Flamm C et al. ViennaRNA Package 2.0. Algorithms Mol Biol 2011; 6:26 [View Article] [PubMed]
     [Google Scholar]
  62. Niira K, Ito M, Masuda T, Saitou T, Abe T et al. Whole genome sequences of Japanese porcine species C rotaviruses reveal a high diversity of genotypes of individual genes and will contribute to a comprehensive, generally accepted classification system. Infect Genet Evol 2016; 44:106–113 [View Article] [PubMed]
     [Google Scholar]
  63. Smith SC, Gribble J, Diller JR, Wiebe MA, Thoner TW et al. Reovirus RNA recombination is sequence directed and generates internally deleted defective genome segments during passage. J Virol 2021; 95:e02181-20 [View Article]
     [Google Scholar]
  64. Boni MF, de Jong MD, van Doorn HR, Holmes EC, Martin DP. Guidelines for identifying homologous recombination events in influenza A virus. PLoS One 2010; 5:e10434 [View Article]
     [Google Scholar]
  65. Lai MM. RNA recombination in animal and plant viruses. Microbiol Rev 1992; 56:61–79 [View Article] [PubMed]
     [Google Scholar]
  66. Nagy PD, Simon AE. New insights into the mechanisms of RNA recombination. Virology 1997; 235:1–9 [View Article] [PubMed]
     [Google Scholar]
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Genomic diversity and intragenic recombination of species C rotaviruses
J. Gen. Virol. 103, 001703 (2022); https://doi.org/10.1099/jgv.0.001703
/content/journal/jgv/10.1099/jgv.0.001703
/content/journal/jgv/10.1099/jgv.0.001703
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