1887

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Volume 103, Issue 9

Molecular evolution and genetic characteristics of G3P[3] group A canine rotavirus isolated in Wuhan, China No Access

Abstract

Rotaviruses can infect multiple animal species and have the potential for cross-recombination based on the segmented genome characteristics. To study the intra-host recombination and zoonotic potential of group A canine rotavirus (CRV), 438 samples were collected from domestic dogs in six animal hospitals and from stray dogs from October 2019 to May 2021 in Wuhan, China. Seven of the samples were positive (7/438) for group A CRV from which a CRV strain was successfully isolated in MA-104 cells. The genotype of the isolated strain was characterized by whole-genome sequencing showing that the genotype was group A CRV . According to the Rotavirus Classification Working Group (RCWG), the genomic constellation of the isolated CRV was G3-P[3]-I3-R3-C3-M3-A9-N2-T3-E3-H6, which belongs to the AU-1-like group with gene segments of AU-1-like and Cat 97-like strains. Based on the phylogenetic analysis of the 11 gene segments, we found that the different segments of the isolated group A CRV were closely related to several reassortment rotaviruses from different animal sources and bat strains. Based on the analysis of the molecular evolution and genetic characteristics, we concluded that the isolated strain might be a reassortment strain. These data further enrich our understanding of rotavirus molecular evolution and genetic characteristics in China.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): canine rotavirus , G3P[3] , phylogenetic analysis and reassortment
Funding
This study was supported by the:
  • the Fundamental Research Funds for the Central Universities (Award 2662019YJ005)
    • Principle Award Recipient: JiangYunbo
© 2022 The Authors
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/content/journal/jgv/10.1099/jgv.0.001784
2022-09-20
2024-04-18
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References

  1. Desselberger U. Rotaviruses. Virus Res 2014; 190:75–96 [View Article] [PubMed]
     [Google Scholar]
  2. Yan N, Tang C, Kan R, Feng F, Yue H. Genome analysis of a G9P[23] group a rotavirus isolated from a dog with diarrhea in China. Infect Genet Evol 2019; 70:67–71 [View Article] [PubMed]
     [Google Scholar]
  3. Charoenkul K, Janetanakit T, Bunpapong N, Boonyapisitsopa S, Tangwangvivat R et al. Molecular characterization identifies intra-host recombination and zoonotic potential of canine rotavirus among dogs from Thailand. Transbound Emerg Dis 2021; 68:1240–1252 [View Article] [PubMed]
     [Google Scholar]
  4. Rolsma MD, Kuhlenschmidt TB, Gelberg HB, Kuhlenschmidt MS. Structure and function of a ganglioside receptor for porcine rotavirus. J Virol 1998; 72:9079–9091 [View Article] [PubMed]
     [Google Scholar]
  5. Malherbe H, Harwin R. The cytopathic effects of vervet monkey viruses. S Afr Med J 1963; 37:407–411 [PubMed]
     [Google Scholar]
  6. Mebus CA, Underdahl NR, Rhodes MB, Twiehaus MJ. Further studies on neonatal calf diarrhea virus. Proc Annu Meet U S Anim Health Assoc 1969; 73:97–99 [PubMed]
     [Google Scholar]
  7. Dhama K, Chauhan RS, Mahendran M, Malik SVS. Rotavirus diarrhea in bovines and other domestic animals. Vet Res Commun 2009; 33:1–23 [View Article] [PubMed]
     [Google Scholar]
  8. Kindler E, Trojnar E, Heckel G, Otto PH, Johne R. Analysis of rotavirus species diversity and evolution including the newly determined full-length genome sequences of rotavirus F and G. Infect Genet Evol 2013; 14:58–67 [View Article] [PubMed]
     [Google Scholar]
  9. Estes MK, Greenberg HB. Rotaviruses. Fields Virology. Philadelphia, PA: Lippincott Williams and Wilkins; 2013
  10. Ward RL, McNeal MM. VP6: a candidate rotavirus vaccine. J Infect Dis 2010; 202 (Suppl. 1):S101–S107 [View Article] [PubMed]
     [Google Scholar]
  11. Stipp DT, Alfieri AF, Lorenzetti E, da Silva Medeiros TN, Possatti F et al. VP6 gene diversity in 11 Brazilian strains of porcine group C rotavirus. Virus Genes 2015; 50:142–146 [View Article] [PubMed]
     [Google Scholar]
  12. Simsek C, Corman VM, Everling HU, Lukashev AN, Rasche A et al. At least seven distinct rotavirus genotype constellations in bats with evidence of reassortment and zoonotic transmissions. mBio 2021; 12:e02755-20 [View Article] [PubMed]
     [Google Scholar]
  13. Chen H, Song L, Li G, Chen W, Zhao S et al. Human rotavirus strain Wa downregulates NHE1 and NHE6 expressions in rotavirus-infected Caco-2 cells. Virus Genes 2017; 53:367–376 [View Article] [PubMed]
     [Google Scholar]
  14. 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]
  15. Dóró R, Farkas SL, Martella V, Bányai K. Zoonotic transmission of rotavirus: surveillance and control. Expert Rev Anti Infect Ther 2015; 13:1337–1350 [View Article] [PubMed]
     [Google Scholar]
  16. Martella V, Pratelli A, Elia G, Decaro N, Tempesta M et al. Isolation and genetic characterization of two G3P5A[3] canine rotavirus strains in Italy. J Virol Methods 2001; 96:43–49 [View Article] [PubMed]
     [Google Scholar]
  17. Yamamoto D, Kawaguchiya M, Ghosh S, Ichikawa M, Numazaki K et al. Detection and full genomic analysis of G6P[9] human rotavirus in Japan. Virus Genes 2011; 43:215–223 [View Article] [PubMed]
     [Google Scholar]
  18. Gauchan P, Sasaki E, Nakagomi T, Do LP, Doan YH et al. Whole genotype constellation of prototype feline rotavirus strains FRV-1 and FRV64 and their phylogenetic relationships with feline-like human rotavirus strains. J Gen Virol 2015; 96:338–350 [View Article] [PubMed]
     [Google Scholar]
  19. Tsugawa T, Hoshino Y. Whole genome sequence and phylogenetic analyses reveal human rotavirus G3P[3] strains Ro1845 and HCR3A are examples of direct virion transmission of canine/feline rotaviruses to humans. Virology 2008; 380:344–353 [View Article] [PubMed]
     [Google Scholar]
  20. Tacharoenmuang R, Guntapong R, Upachai S, Singchai P, Fukuda S et al. Full genome-based characterization of G4P[6] rotavirus strains from diarrheic patients in Thailand: evidence for independent porcine-to-human interspecies transmission events. Virus Genes 2021; 57:338–357 [View Article] [PubMed]
     [Google Scholar]
  21. Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 2019; 20:1160–1166 [View Article] [PubMed]
     [Google Scholar]
  22. Khamrin P, Maneekarn N, Peerakome S, Yagyu F, Okitsu S et al. Molecular characterization of a rare G3P[3] human rotavirus reassortant strain reveals evidence for multiple human-animal interspecies transmissions. J Med Virol 2006; 78:986–994 [View Article] [PubMed]
     [Google Scholar]
  23. Tsugawa T, Fujii Y, Akane Y, Honjo S, Kondo K et al. Molecular characterization of the first human G15 rotavirus strain of zoonotic origin from the bovine species. J Gen Virol 2021; 102:4–9 [View Article] [PubMed]
     [Google Scholar]
  24. Rahman M, Matthijnssens J, Yang X, Delbeke T, Arijs I et al. Evolutionary history and global spread of the emerging G12 human rotaviruses. J Virol 2007; 81:2382–2390 [View Article] [PubMed]
     [Google Scholar]
  25. Mosallanejad B, Shapouri MRS, Avizeh R, Pourmahdi M. Antigenic detection of Canine rotavirus group A in diarrheic dogs in Ahvaz district, southwestern Iran. Comp Clin Path 2015; 24:899–902 [View Article] [PubMed]
     [Google Scholar]
  26. Van Borm S, Vanneste K, Fu Q, Maes D, Schoos A et al. Increased viral read counts and metagenomic full genome characterization of porcine astrovirus 4 and posavirus 1 in sows in a swine farm with unexplained neonatal piglet diarrhea. Virus Genes 2020; 56:696–704 [View Article] [PubMed]
     [Google Scholar]
  27. Malasao R, Saito M, Suzuki A, Imagawa T, Nukiwa-Soma N et al. Human G3P[4] rotavirus obtained in Japan, 2013, possibly emerged through a human-equine rotavirus reassortment event. Virus Genes 2015; 50:129–133 [View Article] [PubMed]
     [Google Scholar]
  28. Pratelli A, Tempesta M, Greco G, Martella V, Buonavoglia C. Development of a nested PCR assay for the detection of canine coronavirus. J Virol Methods 1999; 80:11–15 [View Article] [PubMed]
     [Google Scholar]
  29. Ennima I, Sebbar G, Harif B, Amzazi S, Loutfi C et al. Isolation and identification of group a rotaviruses among neonatal diarrheic calves, Morocco. BMC Res Notes 2016; 9:261 [View Article] [PubMed]
     [Google Scholar]
  30. Ma H, Zhang M, Wu M, Ghonaim AH, Fan S et al. Isolation and genetic characteristics of a neurotropic teschovirus variant belonging to genotype 1 in northeast China. Arch Virol 2021; 166:1355–1370 [View Article] [PubMed]
     [Google Scholar]
  31. Zhang M-J, Liu D-J, Liu X-L, Ge X-Y, Jongkaewwattana A et al. Genomic characterization and pathogenicity of porcine deltacoronavirus strain CHN-HG-2017 from China. Arch Virol 2019; 164:413–425 [View Article] [PubMed]
     [Google Scholar]
  32. 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]
  33. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 2015; 32:268–274 [View Article] [PubMed]
     [Google Scholar]
  34. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
     [Google Scholar]
  35. Geletu US, Usmael MA, Bari FD. Rotavirus in calves and its zoonotic importance. Vet Med Int 2021; 2021:6639701 [View Article] [PubMed]
     [Google Scholar]
  36. Yeşilbağ K, Yilmaz Z, Ozkul A, Pratelli A. Aetiological role of viruses in puppies with diarrhoea. Vet Rec 2007; 161:169–170 [View Article] [PubMed]
     [Google Scholar]
  37. Ortega AF, Martínez-Castañeda JS, Bautista-Gómez LG, Muñoz RF, Hernández IQ. Identification of co-infection by rotavirus and parvovirus in dogs with gastroenteritis in Mexico. Braz J Microbiol 2017; 48:769–773 [View Article] [PubMed]
     [Google Scholar]
  38. Sashina TA, Morozova OV, Epifanova NV, Kashnikov AU, Leonov AV et al. Molecular monitoring of the rotavirus (Reoviridae: Sedoreovirinae: Rotavirus: Rotavirus A) strains circulating in Nizhny Novgorod (2012-2020): detection of the strains with the new genetic features. Vopr Virusol 2021; 66:140–151 [View Article] [PubMed]
     [Google Scholar]
  39. 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]
  40. Hoa-Tran TN, Nakagomi T, Vu HM, Kataoka C, Nguyen TTT et al. Whole genome characterization of feline-like G3P[8] reassortant rotavirus A strains bearing the DS-1-like backbone genes detected in Vietnam, 2016. Infect Genet Evol 2019; 73:1–6 [View Article] [PubMed]
     [Google Scholar]
  41. Okitsu S, Hikita T, Thongprachum A, Khamrin P, Takanashi S et al. Detection and molecular characterization of two rare G8P[14] and G3P[3] rotavirus strains collected from children with acute gastroenteritis in Japan. Infect Genet Evol 2018; 62:95–108 [View Article] [PubMed]
     [Google Scholar]
  42. Du H, Xiong P, Ji F, Lin X, Wang S et al. Genetic diversity and molecular epidemiological characterization of group A rotaviruses in raw sewage in Jinan by next generation sequencing. Infect Genet Evol 2021; 91:104814 [View Article] [PubMed]
     [Google Scholar]
  43. Sasaki M, Orba Y, Sasaki S, Gonzalez G, Ishii A et al. Multi-reassortant G3P[3] group A rotavirus in a horseshoe bat in Zambia. J Gen Virol 2016; 97:2488–2493 [View Article] [PubMed]
     [Google Scholar]
  44. Matthijnssens J, De Grazia S, Piessens J, Heylen E, Zeller M et al. Multiple reassortment and interspecies transmission events contribute to the diversity of feline, canine and feline/canine-like human group A rotavirus strains. Infect Genet Evol 2011; 11:1396–1406 [View Article] [PubMed]
     [Google Scholar]
  45. Martella V, Potgieter AC, Lorusso E, De Grazia S, Giammanco GM et al. A feline rotavirus G3P[9] carries traces of multiple reassortment events and resembles rare human G3P[9] rotaviruses. J Gen Virol 2011; 92:1214–1221 [View Article] [PubMed]
     [Google Scholar]
  46. Nyaga MM, Stucker KM, Esona MD, Jere KC, Mwinyi B et al. Whole-genome analyses of DS-1-like human G2P[4] and G8P[4] rotavirus strains from Eastern, Western and Southern Africa. Virus Genes 2014; 49:196–207 [View Article] [PubMed]
     [Google Scholar]
  47. Fujii Y, Doan YH, Suzuki Y, Nakagomi T, Nakagomi O et al. Study of complete genome sequences of rotavirus A epidemics and evolution in Japan in 2012-2014. Front Microbiol 2019; 10:38 [View Article] [PubMed]
     [Google Scholar]
  48. Wang Y-H, Pang B-B, Ghosh S, Zhou X, Shintani T et al. Molecular epidemiology and genetic evolution of the whole genome of G3P[8] human rotavirus in Wuhan, China, from 2000 through 2013. PLoS One 2014; 9:e88850 [View Article] [PubMed]
     [Google Scholar]
  49. Phan T, Ide T, Komoto S, Khamrin P, Okitsu S et al. Unusual mono-reassortant of A Wa-like G1P[8] species A rotavirus containing DS-1-like (genotype 2) NSP4 gene. Virus Genes 2020; 56:638–641 [View Article] [PubMed]
     [Google Scholar]
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Molecular evolution and genetic characteristics of G3P[3] group A canine rotavirus isolated in Wuhan, China
J. Gen. Virol. 103, 001784 (2022); https://doi.org/10.1099/jgv.0.001784
/content/journal/jgv/10.1099/jgv.0.001784
/content/journal/jgv/10.1099/jgv.0.001784
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