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Genomic diversity of group A rotaviruses from wild boars and domestic pigs in Japan: wide prevalence of NSP5 carrying the H2 genotype

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Abstract

Group A rotavirus (RVA) sequences were detected in 10.8% (23/212) and 20.7% (87/421) of fecal samples collected in 2017-2022 from wild boars and domestic pigs, using next-generation sequencing. Complete genome sequence analysis of one wild boar and 13 domestic pig RVAs revealed that six of them carried the rare H2 NSP5 genotype. Out of the 39 samples for which the NSP5 genotype could be determined, 23 (59.0%) were of genotype H2. H2 porcine RVAs consist exclusively of Japanese porcine RVAs and exhibit sequence diversity in each segment, suggesting that H2 porcine RVAs may have evolved through reassortment within the Japanese pig population.

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Fig. 1

Data availability

GenBank accession numbers are noted for the sequences used in this paper. Other information is not applicable.

References

  1. Dhama K, Chauhan RS, Mahendran M, Malik SV (2009) Rotavirus diarrhea in bovines and other domestic animals. Vet Res Commun 33:1–23. https://doi.org/10.1007/s11259-008-9070-x

    Article  CAS  PubMed  Google Scholar 

  2. Papp H, De LászlóJakabGaneshGrazia BFBS, MatthijnssensCiarletMartellaBányai JMVK (2013) Review of group A rotavirus strains reported in swine and cattle. Vet Microbiol 165:190–199. https://doi.org/10.1016/j.vetmic.2013.03.020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Vlasova AN, Amimo JO, Saif LJ (2017) Porcine rotaviruses: epidemiology, immune responses and control strategies. Viruses 9(3):48. https://doi.org/10.3390/v9030048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Vidal A, Martín-Valls GE, Tello M, Mateu E, Martín M, Darwich L (2019) Prevalence of enteric pathogens in diarrheic and non-diarrheic samples from pig farms with neonatal diarrhea in the North East of Spain. Vet Microbiol 237:108419. https://doi.org/10.1016/j.vetmic.2019.108419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gomara M, Maes P, Patton JT, Rahman M, Van Ranst M (2008) 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 82:3204–3219. https://doi.org/10.1128/JVI.02257-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Matthijnssens J, Ciarlet M, McDonald SM, Attoui H, Bányai K, Brister JR, Buesa J, Esona MD, Estes MK, Gentsch JR, Iturriza-Gómara M, Johne R, Kirkwood CD, Martella V, Mertens PP, Nakagomi O, Parreño V, Rahman M, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Patton JT, Desselberger U, Van Ranst M (2011) Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156:1397–1413. https://doi.org/10.1007/s00705-011-1006-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Miyazaki A, Kuga K, Suzuki T, Kohmoto M, Katsuda K, Tsunemitsu H (2011) Genetic diversity of group A rotaviruses associated with repeated outbreaks of diarrhea in a farrow-to-finish farm: identification of a porcine rotavirus strain bearing a novel VP7 genotype, G26. Vet Res 42(1):112. https://doi.org/10.1186/1297-9716-42-112

    Article  PubMed  PubMed Central  Google Scholar 

  8. Miyazaki A, Kuga K, Suzuki T, Tsunemitsu H (2012) Analysis of the excretion dynamics and genotypic characteristics of rotavirus A during the lives of pigs raised on farms for meat production. J Clin Microbiol 50:2009–2017. https://doi.org/10.1128/JCM.06815-11

    Article  PubMed  PubMed Central  Google Scholar 

  9. Miyazaki A, Kuga K, Suzuki T, Kohmoto M, Katsuda K, Tsunemitsu H (2013) Annual changes in predominant genotypes of rotavirus A detected in the feces of pigs in various developmental stages raised on a conventional farm. Vet Microbiol 163:162–166. https://doi.org/10.1016/j.vetmic.2012.11.044

    Article  CAS  PubMed  Google Scholar 

  10. Okadera K, Abe M, Ito N, Morikawa S, Yamasaki A, Masatani T, Nakagawa K, Yamaoka S, Sugiyama M (2013) Evidence of natural transmission of group A rotavirus between domestic pigs and wild boars (Sus scrofa) in Japan. Infect Genet Evol 20:54–60. https://doi.org/10.1016/j.meegid.2013.07.029

    Article  PubMed  Google Scholar 

  11. Teodoroff TA, Tsunemitsu H, Okamoto K, Katsuda K, Kohmoto M, Kawashima K, Nakagomi T, Nakagomi O (2005) Predominance of porcine rotavirus G9 in Japanese piglets with diarrhea: close relationship of their VP7 genes with those of recent human G9 strains. J Clin Microbiol 43:1377–1384. https://doi.org/10.1128/JCM.43.3.1377-1384.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Komoto S, Maeno Y, Tomita M, Matsuoka T, Ohfu M, Yodoshi T, Akeda H, Taniguchi K (2013) Whole genomic analysis of a porcine-like human G5P[6] rotavirus strain isolated from a child with diarrhoea and encephalopathy in Japan. J Gen Virol 94:1568–1575. https://doi.org/10.1099/vir.0.051011-0

    Article  CAS  PubMed  Google Scholar 

  13. Do LP, Nakagomi T, Nakagomi O (2014) A rare G1P[6] super-short human rotavirus strain carrying an H2 genotype on the genetic background of a porcine rotavirus. Infect Genet Evol 21:334–350. https://doi.org/10.1016/j.meegid.2013.11.027

    Article  CAS  PubMed  Google Scholar 

  14. Do LP, Nakagomi T, Otaki H, Agbemabiese CA, Nakagomi O, Tsunemitsu H (2016) Phylogenetic inference of the porcine Rotavirus A origin of the human G1 VP7 gene. Infect Genet Evol 40:205–213. https://doi.org/10.1016/j.meegid.2016.03.001

    Article  CAS  PubMed  Google Scholar 

  15. Fukuda Y, Araki K, Hara M, Yamashita Y, Adachi S, Honjo S, Togashi A, Hirakawa S, Fukumura S, Yamamoto M, Tsugawa T (2023) Sequence analysis of a feline- and porcine-origin G3P[9] rotavirus A strain in a child with acute gastroenteritis in Japan. Arch Virol 168:45. https://doi.org/10.1007/s00705-022-05685-3

    Article  CAS  PubMed  Google Scholar 

  16. Nagai M, Omatsu T, Aoki H, Otomaru K, Uto T, Koizumi M, Minami-Fukuda F, Takai H, Murakami T, Masuda T, Yamasato H, Shiokawa M, Tsuchiaka S, Naoi Y, Sano K, Okazaki S, Katayama Y, Oba M, Furuya T, Shirai J, Mizutani T (2015) Full genome analysis of bovine astrovirus from fecal samples of cattle in Japan: identification of possible interspecies transmission of bovine astrovirus. Arch Virol 160:2491–2501. https://doi.org/10.1007/s00705-015-2543-7

    Article  CAS  PubMed  Google Scholar 

  17. Gouvea V, Glass RI, Woods P, Taniguchi K, Clark HF, Forrester B, Fang ZY (1990) Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28:276–282. https://doi.org/10.1128/jcm.28.2.276-282.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Nagai M, Shimada S, Fujii Y, Moriyama H, Oba M, Katayama Y, Tsuchiaka S, Okazaki S, Omatsu T, Furuya T, Koyama S, Shirai J, Katayama K, Mizutani T (2015) H2 genotypes of G4P[6], G5P[7], and G9[23] porcine rotaviruses show super-short RNA electropherotypes. Vet Microbiol 176:250–256. https://doi.org/10.1016/j.vetmic.2015.02.002

    Article  CAS  PubMed  Google Scholar 

  19. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Park GN, Kim DI, Choe S, Shin J, An BH, Kim KS, Hyun BH, Lee JS, An DJ (2022) Genetic diversity of porcine group A rotavirus strains from pigs in South Korea. Viruses 14(11):2522. https://doi.org/10.3390/v14112522

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hull JJA, Qi M, Montmayeur AM, Kumar D, Velasquez DE, Moon SS, Magaña LC, Betrapally N, Ng TFF, Jiang B, Marthaler D (2020) Metagenomic sequencing generates the whole genomes of porcine rotavirus A, C, and H from the United States. PLoS ONE 15(12):e0244498. https://doi.org/10.1371/journal.pone.0244498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Fujii Y, Shimoike T, Takagi H, Murakami K, Todaka-Takai R, Park Y, Katayama K (2011) Amplification of all 11 RNA segments of group A rotaviruses based on reverse transcription polymerase chain reaction. Microbiol Immunol 56:630–638. https://doi.org/10.1111/j.1348-0421.2012.00479.x

    Article  CAS  Google Scholar 

  23. Ghosh S, Urushibara N, Kawaguchiya M, Shintani T, Kobayashi N (2013) The origin of two rare human P[10] rotavirus strains. Infect Genet Evol 13:292–300. https://doi.org/10.1016/j.meegid.2012.10.021

    Article  PubMed  Google Scholar 

  24. Heiman EM, McDonald SM, Barro M, Taraporewala ZF, Bar-Magen T, Patton JT (2008) Group A human rotavirus genomics: evidence that gene constellations are influenced by viral protein interactions. J Virol 82:11106–11116. https://doi.org/10.1128/JVI.01402-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Matsui SM, Mackow ER, Matsuno S, Paul PS, Greenberg HB (1990) Sequence analysis of gene 11 equivalents from “short” and “super short” strains of rotavirus. J Virol 64:120–124. https://doi.org/10.1128/JVI.64.1.120-124.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Hum CP, Dyall-Smith ML, Holmes IH (1989) The VP7 gene of a new G serotype of human rotavirus (B37) is similar to G3 proteins in the antigenic c region. Virology 170:55–61. https://doi.org/10.1016/0042-6822(89)90351-6

    Article  CAS  PubMed  Google Scholar 

  27. Guo D, Liu J, Lu Y, Sun Y, Yuan D, Jiang Q, Lin H, Li C, Si C, Qu L (2012) Full genomic analysis of rabbit rotavirus G3P[14] strain N5 in China: identification of a novel VP6 genotype. Infect Genet Evol 12:1567–1576. https://doi.org/10.1016/j.meegid.2012.06.010

    Article  CAS  PubMed  Google Scholar 

  28. Kojima K, Taniguchi K, Urasawa T, Urasawa S (1996) Sequence analysis of normal and rearranged NSP5 genes from human rotavirus strains isolated in nature: implications for the occurrence of the rearrangement at the step of plus strand synthesis. Virology 224:446–452. https://doi.org/10.1006/viro.1996.0551

    Article  CAS  PubMed  Google Scholar 

  29. Zeller M, Heylen E, De Coster S, Van Ranst M, Matthijnssens J (2012) Full genome characterization of a porcine-like human G9P[6] rotavirus strain isolated from an infant in Belgium. Infect Genet Evol 12:1492–1500. https://doi.org/10.1016/j.meegid.2012.03.002

    Article  CAS  PubMed  Google Scholar 

  30. Wu FT, Bányai K, Jiang B, Liu LT, Marton S, Huang YC, Huang LM, Liao MH, Hsiung CA (2017) Novel G9 rotavirus strains co-circulate in children and pigs, Taiwan. Sci Rep 18(7):40731. https://doi.org/10.1038/srep40731

    Article  CAS  Google Scholar 

  31. Bwogi J, Jere KC, Karamagi C, Byarugaba DK, Namuwulya P, Baliraine FN, Desselberger U, Iturriza-Gomara M (2017) Whole genome analysis of selected human and animal rotaviruses identified in Uganda from 2012 to 2014 reveals complex genome reassortment events between human, bovine, caprine and porcine strains. PLoS ONE 12(6):e0178855. https://doi.org/10.1371/journal.pone.0178855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by a Livestock Promotional Subsidy from the Japan Racing Association and JSPS KAKENHI (grant number 21K05947).

Funding

This study was funded by JSPS KAKENHI (Grant no. 21K05947) and Japan Racing Association.

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Authors and Affiliations

  1. School of Veterinary Medicine, Azabu University, Sagamihara, Kanagawa, 252-5201, Japan

    Shigeki Shizawa, Hiroho Ishida, Hironobu Murakami, Makoto Nagai & Mami Oba

  2. Ishikawa Nanbu Livestock Hygiene Service Center, Kanazawa, Ishikawa, 920-3101, Japan

    Fujiko Fukuda

  3. Global Pig Farm, Inc., Shibukawa, Gunma, 377-0052, Japan

    Yasuhiro Kikkawa

  4. Faculty of Bioresources and Environmental Science, Ishikawa Prefectural University, Nonoichi, Ishikawa, 921-8836, Japan

    Toru Oi

  5. Center for infectious Disease Epidemiology and Prevention Research, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-8509, Japan

    Hitoshi Takemae, Tetsuya Mizutani, Makoto Nagai & Mami Oba

  6. Faculty of Veterinary Medicine, Okayama University of Science, Imabari, Ehime, 794-0085, Japan

    Tsuneyuki Masuda

  7. Department of Microbiology and Infection Control, Faculty of Medicine, Osaka Medical and Pharmaceutical University, Osaka, 569-8686, Japan

    Shoichi Sakaguchi

Authors
  1. Shigeki Shizawa
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Corresponding author

Correspondence to Mami Oba.

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Research involving human participants and/or animals

The fecal samples that were used in this study were collected for pathological testing of wild boars and domestic pigs; therefore, no specific approval was needed.

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Shizawa, S., Fukuda, F., Kikkawa, Y. et al. Genomic diversity of group A rotaviruses from wild boars and domestic pigs in Japan: wide prevalence of NSP5 carrying the H2 genotype. Arch Virol 169, 63 (2024). https://doi.org/10.1007/s00705-023-05954-9

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