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Abstract

Species A rotaviruses (RVAs) are genetically diverse pathogens. These are the most evolutionarily adaptable organisms, with a multitude of mechanisms for evolutionary change. To date, full-genome classification has been proved to be an excellent tool for studying the evolution of unusual rotavirus strains. As limited data are available from Pune (Maharashtra), western India, the current study was undertaken with the aim of understanding the genetic diversity in three (G1P[6] G9P[4] and G9P[4]) unusual RVA strains circulating in Pune, India during 2013–2015. Full-genome analysis of these strains classified them as G1-P[6]-I1-R1-C1-M1-A1-N1-T1-E1-H1, G9-P[4]-I2-R2-C2-[M1-M2_R]-[A1-A2_R]-N2-T2-E6-H2 and G9-[P4-P6_R]-I1-R1-C1-M1-A1-N1-T1-E1-H1. Sequencing and phylogenetic analysis of the structural and non-structural genes of these unusual RVA strains showed nucleotide/amino acid identities of 82.3–98.5 %/77.3–99.8 % and 86.6–97.6 %/89.6–97.8 % between the strains of the study. Evidence of recombination events was found within the genes encoding VP3, VP4 and NSP1, which showed a combination of genetic information for genogroup 1 [M1/P[6]/A1] and genogroup 2 [M2/P[4]/A2] strains. This study will facilitate future investigations into the molecular pathogenesis of such RVAs as the exchange of whole or partial genetic material between rotaviruses through recombination contributes directly to their diversification, adaptation and evolution.

Funding
This study was supported by the:
  • Indian Council of Medical Research
    • Principle Award Recipient: Varanasi Gopalkrishna
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2019-09-25
2024-05-13
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References

  1. Estes MK, Greenberg HB. Rotaviruses. In Knipe DM. editor Fields Virology Philadelphia, PA: Wolters Kluwer Health/Lippincott, Williams and Wilkins; 2013 pp 1347–1401
    [Google Scholar]
  2. Tate JE, Burton AH, Boschi-Pinto C, Parashar UD. World Health Organization–Coordinated Global Rotavirus Surveillance Network Global, regional and national estimates of rotavirus mortality in children. Clin Infect Dis 2016; 62:S96–S105
    [Google Scholar]
  3. Jonesteller CL, Burnett E, Yen C, Tate JE, Parashar UD. Effectiveness of rotavirus vaccination: a systematic review of the first decade of global postlicensure data, 2006-2016. Clin Infect Dis 2017; 65:840–850 [View Article]
    [Google Scholar]
  4. Bányai K, Estes MK, Martella V, Parashar UD. Viral gastroenteritis. The Lancet 2018; 392:175–186 [View Article]
    [Google Scholar]
  5. Bhandari N, Rongsen-Chandola T, Bavdekar A, John J, Antony K et al. Efficacy of a monovalent human-bovine (116E) rotavirus vaccine in Indian infants: a randomised, double-blind, placebo-controlled trial. Lancet 2014; 383:2136–2143 [View Article]
    [Google Scholar]
  6. Kulkarni PS, Desai S, Tewari T, Kawade A, Goyal N et al. A randomized phase III clinical trial to assess the efficacy of a bovine-human reassortant pentavalent rotavirus vaccine in Indian infants. Vaccine 2017; 35:6228–6237 [View Article]
    [Google Scholar]
  7. Dennehy PH. Rotavirus vaccines: an overview. Clin Microbiol Rev 2008; 21:198–208 [View Article]
    [Google Scholar]
  8. Ramig RF. Genetics of the rotaviruses. Annu Rev Microbiol 1997; 51:225–255 [View Article]
    [Google Scholar]
  9. 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]
    [Google Scholar]
  10. 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]
    [Google Scholar]
  11. Desselberger U. Rotaviruses. Virus Res 2014; 190:75–96 [View Article]
    [Google Scholar]
  12. Woods RJ. Intrasegmental recombination does not contribute to the long-term evolution of group A rotavirus. Infect Genet Evol 2015; 32:354–360 [View Article]
    [Google Scholar]
  13. Ghosh S, Kobayashi N. Whole-genomic analysis of rotavirus strains: current status and future prospects. Future Microbiol 2011; 6:1049–1065 [View Article]
    [Google Scholar]
  14. 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]
    [Google Scholar]
  15. 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]
    [Google Scholar]
  16. Jere KC, Mlera L, Page NA, van Dijk AA, O'Neill HG et al. 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]
    [Google Scholar]
  17. 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]
    [Google Scholar]
  18. Phan TG, Okitsu S, Maneekarn N, Ushijima H. Evidence of intragenic recombination in G1 rotavirus VP7 genes. J Virol 2007a; 81:10188–10194 [View Article]
    [Google Scholar]
  19. Phan TG, Okitsu S, Maneekarn N, Ushijima H. Genetic heterogeneity, evolution and recombination in emerging G9 rotaviruses. Infect Genet Evol 2007b; 7:656–663 [View Article]
    [Google Scholar]
  20. Parra GI, Espínola EE, Amarilla AA, Stupka J, Martinez M et al. Diversity of group A rotavirus strains circulating in Paraguay from 2002 to 2005: detection of an atypical G1 in South America. J Clin Virol 2007; 40:135–141 [View Article]
    [Google Scholar]
  21. 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]
    [Google Scholar]
  22. Banerjee I, Iturriza-Gomara M, Rajendran P, Primrose B, Ramani S et al. Molecular characterization of G11P[25] and G3P[3] human rotavirus strains associated with asymptomatic infection in South India. J Med Virol 2007; 79:1768–1774 [View Article]
    [Google Scholar]
  23. Chitambar SD, Ranshing SS, Pradhan GN, Kalrao VR, Dhongde RK et al. Changing trends in circulating rotavirus strains in Pune, western India in 2009–2012: Emergence of a rare G9P[4] rotavirus strain. Vaccine 2014; 1432:A29–A32
    [Google Scholar]
  24. Mandal P, Mullick S, Nayak MK, Mukherjee A, Ganguly N et al. Complete genotyping of unusual species A rotavirus G12P[11] and G10P[14] isolates and evidence of frequent in vivo reassortment among the rotaviruses detected in children with diarrhea in Kolkata, India, during 2014. Arch Virol 2016; 161:2773–2785 [View Article]
    [Google Scholar]
  25. Mukherjee A, Mullick S, Deb AK, Panda S, Chawla-Sarkar M. First report of human rotavirus G8P[4] gastroenteritis in India: evidence of ruminants-to-human zoonotic transmission. J Med Virol 2013; 85:537–545 [View Article]
    [Google Scholar]
  26. Mukherjee A, Mullick S, Kobayashi N, Chawla-Sarkar M. The first identification of rare human group A rotavirus strain G3P[10] with severe infantile diarrhea in eastern India. Infect Genet Evol 2012; 12:1933–1937 [View Article]
    [Google Scholar]
  27. Rajendran P, Kang G. Molecular epidemiology of rotavirus in children and animals and characterization of an unusual G10P[15] strain associated with bovine diarrhea in south India. Vaccine 2014; 32:A89–A94 [View Article]
    [Google Scholar]
  28. Reesu R, Bhattacharya D, Chaaithanya IK, Muruganandam N, Bharadwaj AP et al. Emergence of an unusual genotype of rotavirus in Andaman and nicobar Islands, India. Intervirology 2013; 56:134–139 [View Article]
    [Google Scholar]
  29. Arora R, Chitambar SD. Full genomic analysis of Indian G1P[8] rotavirus strains. Infection, Genetics and Evolution 2011; 11:504–511 [View Article]
    [Google Scholar]
  30. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S et al. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 2013; 30:2725–2729 [View Article]
    [Google Scholar]
  31. 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
    [Google Scholar]
  32. Ruiz-Palacios GM, Pérez-Schael I, Velázquez FR, Abate H, Breuer T et al. Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N Engl J Med Overseas Ed 2006; 354:11–22 [View Article]
    [Google Scholar]
  33. Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M et al. Safety and efficacy of a pentavalent Human–Bovine (WC3) reassortant rotavirus vaccine. N Engl J Med Overseas Ed 2006; 354:23–33 [View Article]
    [Google Scholar]
  34. Afrad MH, Rahman MZ, Matthijnssens J, Das SK, Faruque ASG et al. High incidence of reassortant G9P[4] rotavirus strain in Bangladesh: fully heterotypic from vaccine strains. J Clin Virol 2013; 58:755–756 [View Article]
    [Google Scholar]
  35. Quaye O, McDonald S, Esona MD, Lyde FC, Mijatovic-Rustempasic S et al. Rotavirus G9P[4] in 3 countries in Latin America, 2009-2010. Emerg Infect Dis 2013; 19:1332–1333 [View Article]
    [Google Scholar]
  36. Lewis J, Roy S, Esona MD, Mijatovic-Rustempasic S, Hardy C et al. Full Genome Sequence of a Reassortant Human G9P[4] Rotavirus Strain. Genome Announc 2014; 2:e01284–14 [View Article]
    [Google Scholar]
  37. Yamamoto SP, Kaida A, Ono A, Kubo H, Iritani N. Detection and characterization of a human G9P[4] rotavirus strain in Japan. J Med Virol 2015; 87:1311–1318 [View Article]
    [Google Scholar]
  38. Pradhan GN, Walimbe AM, Chitambar SD. Molecular characterization of emerging G9P[4] rotavirus strains possessing a rare E6 NSP4 or T1 NSP3 genotype on a genogroup-2 backbone using a refined classification framework. J Gen Virol 2016; 97:3139–3153 [View Article]
    [Google Scholar]
  39. Doan YH, Suzuki Y, Fujii Y, Haga K, Fujimoto A et al. Complex reassortment events of unusual G9P[4] rotavirus strains in India between 2011 and 2013. Infect Genet Evol 2017; 54:417–428 [View Article]
    [Google Scholar]
  40. Ianiro G, Recanatini C, D’Errico MM, Monini M. Uncommon G9P[4] group A rotavirus strains causing dehydrating diarrhea in young children in Italy. Infection, Genetics and Evolution 2018; 64:57–64 [View Article]
    [Google Scholar]
  41. Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Bányai K et al. Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol 2009; 4:1303–1316 [View Article]
    [Google Scholar]
  42. Santos N, Hoshino Y. Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 2005; 15:29–56 [View Article]
    [Google Scholar]
  43. Adah MI, Wade A, Taniguchi K. Molecular epidemiology of rotaviruses in Nigeria: detection of unusual strains with G2P[6] and G8P[1] specificities. J Clin Microbiol 2001; 39:3969–3975 [View Article]
    [Google Scholar]
  44. Miles MG, Lewis KDC, Kang G, Parashar UD, Steele AD. A systematic review of rotavirus strain diversity in India, Bangladesh, and Pakistan. Vaccine 2012; 30:A131–A139 [View Article]
    [Google Scholar]
  45. Nordgren J, Nitiema LW, Sharma S, Ouermi D, Traore AS et al. Emergence of unusual G6P[6] rotaviruses in children, Burkina Faso, 2009-2010. Emerg Infect Dis 2012; 18:589–597 [View Article]
    [Google Scholar]
  46. Jain S, Thakur N, Vashistt J, Grover N, Krishnan T et al. Predominance of unusual rotavirus G1P[6] strain in North India: An evidence from hospitalized children and adult diarrheal patients. Infect Genet Evol 2016; 46:65–70 [View Article]
    [Google Scholar]
  47. Mukherjee A, Dutta D, Ghosh S, Bagchi P, Chattopadhyay S et al. Full genomic analysis of a human group A rotavirus G9P[6] strain from Eastern India provides evidence for porcine-to-human interspecies transmission. Arch Virol 2009; 154:733–746 [View Article]
    [Google Scholar]
  48. Nyaga MM, Jere KC, Peenze I, Mlera L, van Dijk AA et al. Sequence analysis of the whole genomes of five African human G9 rotavirus strains. Infect Genet Evol 2013; 16:62–77 [View Article]
    [Google Scholar]
  49. Nyaga MM, Tan Y, Seheri ML, Halpin RA, Akopov A et al. Whole-genome sequencing and analyses identify high genetic heterogeneity, diversity and endemicity of rotavirus genotype P[6] strains circulating in Africa. Infect Genet Evol 2018; 63:79–88 [View Article]
    [Google Scholar]
  50. Do LP, Nakagomi T, Nakagomi O. A rare G1P[6] super-short human rotavirus strain carrying an H2 genotype on the genetic background of a porcine rotavirus. Infect Genet Evol 2014; 21:334–350 [View Article]
    [Google Scholar]
  51. Ghosh S, Urushibara N, Chawla-Sarkar M, Krishnan T, Kobayashi N. Whole genomic analyses of asymptomatic human G1P[6], G2P[6] and G3P[6] rotavirus strains reveal intergenogroup reassortment events and genome segments of artiodactyl origin. Infect Genet Evol 2013; 16:165–173 [View Article]
    [Google Scholar]
  52. 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]
    [Google Scholar]
  53. 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]
    [Google Scholar]
  54. 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]
    [Google Scholar]
  55. Galli A, Bukh J. Comparative analysis of the molecular mechanisms of recombination in hepatitis C virus. Trends Microbiol 2014; 22:354–364 [View Article]
    [Google Scholar]
  56. Bentley K, Evans DJ. Mechanisms and consequences of positive-strand RNA virus recombination. J Gen Virol 2018; 99:1345–1356 [View Article]
    [Google Scholar]
  57. Su S, Wong G, Shi W, Liu J, Lai ACK et al. Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol 2016; 24:490–502 [View Article]
    [Google Scholar]
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