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Volume 63, Issue 9

Complete genome analysis of a rare group A rotavirus, G11P[25], isolated from a child in Mumbai, India, reveals interspecies transmission and reassortment with human rotavirus strains Free

Abstract

Hospital-based rotavirus surveillance was carried out in Mumbai during 2005–2009. An isolate (B08299) with a rare genotype combination (G11P[25]) was detected. The present study was undertaken to characterize the complete genome of the isolate. B08299 exhibited a G11–P[25]–I12–R1–C1–M1–A1–N1–T1–E1–H1 genotype constellation. Phylogenetic analysis of the 11 gene segments of B08299 revealed that the VP2 and NSP5 genes of B08299 had a human origin, while the VP6 gene represented an I12 genotype of obscure origin. The remaining six genes formed a lineage distinct from human and porcine rotaviruses within genotype 1. Analysis of the structural and non-structural genes suggested that B08299 has evolved by gene reassortment. Our findings provide further evidence that interspecies transmission is an important mechanism involved in the evolution and genetic diversity of human rotaviruses in nature.

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© 2014 The Authors
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2014-09-01
2024-04-25
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References

  1. Adah M. I., Wade A., Taniguchi K. 2001; Molecular epidemiology of rotaviruses in Nigeria: detection of unusual strains with G2P[6] and G8P[1] specificities. J Clin Microbiol 39:3969–3975 [View Article][PubMed]
     [Google Scholar]
  2. Araújo I. T., Ferreira M. S., Fialho A. M., Assis R. M., Cruz C. M., Rocha M., Leite J. P. 2001; Rotavirus genotypes P[4]G9, P[6]G9, and P[8]G9 in hospitalized children with acute gastroenteritis in Rio de Janeiro, Brazil. J Clin Microbiol 39:1999–2001 [View Article][PubMed]
     [Google Scholar]
  3. Awachat P. S., Kelkar S. D. 2005; Unexpected detection of simian SA11–human reassortant strains of rotavirus G3P[8] genotype from diarrhea epidemic among tribal children of western India. J Med Virol 77:128–135 [View Article][PubMed]
     [Google Scholar]
  4. Banerjee I., Iturriza-Gómara M., Rajendran P., Primrose B., Ramani S., Gray J. J., Brown D. W., Kang G. 2007; Molecular characterization of G11P[25] and G3P[3] human rotavirus strains associated with asymptomatic infection in South India. J Med Virol 79:1768–1774 [View Article][PubMed]
     [Google Scholar]
  5. Bányai K., Esona M. D., Kerin T. K., Hull J. J., Mijatovic S., Vásconez N., Torres C., de Filippis A. M., Foytich K. R., Gentsch J. R. 2009; Molecular characterization of a rare, human–porcine reassortant rotavirus strain, G11P[6], from Ecuador. Arch Virol 154:1823–1829 [View Article][PubMed]
     [Google Scholar]
  6. Bok K., Castagnaro N., Borsa A., Nates S., Espul C., Fay O., Fabri A., Grinstein S., Miceli I. other authors 2001; Surveillance for rotavirus in Argentina. J Med Virol 65:190–198 [View Article][PubMed]
     [Google Scholar]
  7. Castello A. A., Argüelles M. H., Rota R. P., Olthoff A., Jiang B., Glass R. I., Gentsch J. R., Glikmann G. 2006; Molecular epidemiology of group A rotavirus diarrhea among children in Buenos Aires, Argentina, from 1999 to 2003 and emergence of the infrequent genotype G12. J Clin Microbiol 44:2046–2050 [View Article][PubMed]
     [Google Scholar]
  8. Chitambar S. D., Arora R., Chhabra P. 2009; Molecular characterization of a rare G1P[19] rotavirus strain from India: evidence of reassortment between human and porcine rotavirus strains. J Med Microbiol 58:1611–1615 [View Article][PubMed]
     [Google Scholar]
  9. Ciarlet M., Hidalgo M., Gorziglia M., Liprandi F. 1994; Characterization of neutralization epitopes on the VP7 surface protein of serotype G11 porcine rotaviruses. J Gen Virol 75:1867–1873 [View Article][PubMed]
     [Google Scholar]
  10. Cooney M. A., Gorrell R. J., Palombo E. A. 2001; Characterisation and phylogenetic analysis of the VP7 proteins of serotype G6 and G8 human rotaviruses. J Med Microbiol 50:462–467[PubMed]
     [Google Scholar]
  11. Cunliffe N. A., Woods P. A., Leite J. P., Das B. K., Ramachandran M., Bhan M. K., Hart C. A., Glass R. I., Gentsch J. R. 1997; Sequence analysis of NSP4 gene of human rotavirus allows classification into two main genetic groups. J Med Virol 53:41–50 [View Article][PubMed]
     [Google Scholar]
  12. Cunliffe N. A., Gondwe J. S., Graham S. M., Thindwa B. D., Dove W., Broadhead R. L., Molyneux M. E., Hart C. A. 2001; Rotavirus strain diversity in Blantyre, Malawi, from 1997 to 1999. J Clin Microbiol 39:836–843 [View Article][PubMed]
     [Google Scholar]
  13. Das S., Varghese V., Chaudhury S., Barman P., Mahapatra S., Kojima K., Bhattacharya S. K., Krishnan T., Ratho R. K. other authors 2003; Emergence of novel human group A rotavirus G12 strains in India. J Clin Microbiol 41:2760–2762 [View Article][PubMed]
     [Google Scholar]
  14. Duan Z. J., Li D. D., Zhang Q., Liu N., Huang C. P., Jiang X., Jiang B., Glass R., Steele D. other authors 2007; Novel human rotavirus of genotype G5P[6] identified in a stool specimen from a Chinese girl with diarrhea. J Clin Microbiol 45:1614–1617 [View Article][PubMed]
     [Google Scholar]
  15. Estes M. K., Kapikian A. Z. 2007; Rotaviruses. In Fields Virology, 5th edn. vol. 2 pp. 1917–1974 Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Straus S. E. Philadelphia: Lippincott Williams & Wilkins;
     [Google Scholar]
  16. Gentsch J. R., Glass R. I., Woods P., Gouvea V., Gorziglia M., Flores J., Das B. K., Bhan M. K. 1992; Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol 30:1365–1373[PubMed]
     [Google Scholar]
  17. Ghosh S., Kobayashi N. 2011; Whole-genomic analysis of rotavirus strains: current status and future prospects. Future Microbiol 6:1049–1065 [View Article][PubMed]
     [Google Scholar]
  18. Ghosh S., Varghese V., Samajdar S., Sinha M., Naik T. N., Kobayashi N. 2007; Evidence for bovine origin of VP4 and VP7 genes of human group A rotavirus G6P[14] and G10P[14] strains. J Clin Microbiol 45:2751–2753 [View Article][PubMed]
     [Google Scholar]
  19. Gouvea V., Glass R. I., Woods P., Taniguchi K., Clark H. F., Forrester B., Fang Z. Y. 1990; Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol 28:276–282[PubMed]
     [Google Scholar]
  20. 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 [View Article][PubMed]
     [Google Scholar]
  21. Hong S. K., Lee S. G., Lee S. A., Kang J. H., Lee J. H., Kim J. H., Kim D. S., Kim H. M., Jang Y. T. other authors 2007; Characterization of a G11,P[4] strain of human rotavirus isolated in South Korea. J Clin Microbiol 45:3759–3761 [View Article][PubMed]
     [Google Scholar]
  22. Iturriza-Gómara M., Green J., Brown D. W., Desselberger U., Gray J. J. 1999; Comparison of specific and random priming in the reverse transcriptase polymerase chain reaction for genotyping group A rotaviruses. J Virol Methods 78:93–103 [View Article][PubMed]
     [Google Scholar]
  23. Iturriza Gómara M., Kang G., Mammen A., Jana A. K., Abraham M., Desselberger U., Brown D., Gray J. 2004; Characterization of G10P[11] rotaviruses causing acute gastroenteritis in neonates and infants in Vellore, India. J Clin Microbiol 42:2541–2547 [View Article][PubMed]
     [Google Scholar]
  24. Jenkins G. M., Rambaut A., Pybus O. G., Holmes E. C. 2002; Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54:156–165 [View Article][PubMed]
     [Google Scholar]
  25. Jere K. C., Esona M. D., Ali Y. H., Peenze I., Roy S., Bowen M. D., Saeed I. K., Khalafalla A. I., Nyaga M. M. other authors 2014; Novel NSP1 genotype characterised in an African camel G8P[11] rotavirus strain. Infect Genet Evol 21:58–66 [View Article][PubMed]
     [Google Scholar]
  26. Kang G., Arora R., Chitambar S. D., Deshpande J., Gupte M. D., Kulkarni M., Naik T. N., Mukherji D., Venkatasubramaniam S. other authors 2009; Multicenter, hospital-based surveillance of rotavirus disease and strains among Indian children aged <5 years. J Infect Dis 200:Suppl. 1S147–S153 [View Article][PubMed]
     [Google Scholar]
  27. Khamrin P., Maneekarn N., Peerakome S., Tonusin S., Phan T. G., Okitsu S., Ushijima H. 2007; Molecular characterization of rare G3P[9] rotavirus strains isolated from children hospitalized with acute gastroenteritis. J Med Virol 79:843–851 [View Article][PubMed]
     [Google Scholar]
  28. Kimura M. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 [View Article][PubMed]
     [Google Scholar]
  29. Kusumakar A. L., Savita, Malik Y. S., Minakshi, Prasad G. 2010; Genomic diversity among group A rotaviruses from diarrheic children, piglets, buffalo and cow calves of Madhya Pradesh. Indian J Microbiol 50:83–88 [View Article][PubMed]
     [Google Scholar]
  30. Maes P., Matthijnssens J., Rahman M., Van Ranst M. 2009; RotaC: a web-based tool for the complete genome classification of group A rotaviruses. BMC Microbiol 9:238 [View Article][PubMed]
     [Google Scholar]
  31. Matthijnssens J., Rahman M., Martella V., Xuelei Y., De Vos S., De Leener K., Ciarlet M., Buonavoglia C., Van Ranst M. 2006; Full genomic analysis of human rotavirus strain B4106 and lapine rotavirus strain 30/96 provides evidence for interspecies transmission. J Virol 80:3801–3810 [View Article][PubMed]
     [Google Scholar]
  32. Matthijnssens J., Ciarlet M., Rahman M., Attoui H., Bányai K., Estes M. K., Gentsch J. R., Iturriza-Gómara M., Kirkwood C. D. other authors 2008a; Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol 153:1621–1629 [View Article][PubMed]
     [Google Scholar]
  33. Matthijnssens J., Rahman M., Van Ranst M. 2008b; Two out of the 11 genes of an unusual human G6P[6] rotavirus isolate are of bovine origin. J Gen Virol 89:2630–2635 [View Article][PubMed]
     [Google Scholar]
  34. Matthijnssens J., Rahman M., Ciarlet M., Zeller M., Heylen E., Nakagomi T., Uchida R., Hassan Z., Azim T. other authors 2010a; Reassortment of human rotavirus gene segments into G11 rotavirus strains. Emerg Infect Dis 16:625–630 [View Article][PubMed]
     [Google Scholar]
  35. Matthijnssens J., Heylen E., Zeller M., Rahman M., Lemey P., Van Ranst M. 2010b; Phylodynamic analyses of rotavirus genotypes G9 and G12 underscore their potential for swift global spread. Mol Biol Evol 27:2431–2436 [View Article][PubMed]
     [Google Scholar]
  36. Matthijnssens J., Ciarlet M., McDonald S. M., Attoui H., Bányai K., Brister J. R., Buesa J., Esona M. D., Estes M. K. other authors 2011; Uniformity of rotavirus strain nomenclature proposed by the Rotavirus Classification Working Group (RCWG). Arch Virol 156:1397–1413 [View Article][PubMed]
     [Google Scholar]
  37. Mukherjee A., Dutta D., Ghosh S., Bagchi P., Chattopadhyay S., Nagashima S., Kobayashi N., Dutta P., Krishnan T. other authors 2009; 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 154:733–746 [View Article][PubMed]
     [Google Scholar]
  38. Mukherjee A., Ghosh S., Bagchi P., Dutta D., Chattopadhyay S., Kobayashi N., Chawla-Sarkar M. 2011; Full genomic analyses of human rotavirus G4P[4], G4P[6], G9P[19] and G10P[6] strains from north-eastern India: evidence for interspecies transmission and complex reassortment events. Clin Microbiol Infect 17:1343–1346[PubMed] [CrossRef]
     [Google Scholar]
  39. Mukherjee A., Mullick S., Deb A. K., Panda S., Chawla-Sarkar M. 2013; First report of human rotavirus G8P[4] gastroenteritis in India: evidence of ruminants-to-human zoonotic transmission. J Med Virol 85:537–545 [View Article][PubMed]
     [Google Scholar]
  40. Mullick S., Mukherjee A., Ghosh S., Pazhani G. P., Sur D., Manna B., Nataro J. P., Levine M. M., Ramamurthy T., Chawla-Sarkar M. 2013; Genomic analysis of human rotavirus strains G6P[14] and G11P[25] isolated from Kolkata in 2009 reveals interspecies transmission and complex reassortment events. Infect Genet Evol 14:15–21 [View Article][PubMed]
     [Google Scholar]
  41. Palombo E. A. 2002; Genetic analysis of group A rotaviruses: evidence for interspecies transmission of rotavirus genes. Virus Genes 24:11–20 [View Article][PubMed]
     [Google Scholar]
  42. Papp H., Al-Mutairi L. Z., Chehadeh W., Farkas S. L., Lengyel G., Jakab F., Martella V., Szűcs G., Bányai K. 2012; Novel NSP4 genotype in a camel G10P[15] rotavirus strain. Acta Microbiol Immunol Hung 59:411–421 [View Article][PubMed]
     [Google Scholar]
  43. Paul S. K., Kobayashi N., Nagashima S., Ishino M., Watanabe S., Alam M. M., Ahmed M. U., Hossain M. A., Naik T. N. 2008; Phylogenetic analysis of rotaviruses with genotypes G1, G2, G9 and G12 in Bangladesh: evidence for a close relationship between rotaviruses from children and adults. Arch Virol 153:1999–2012 [View Article][PubMed]
     [Google Scholar]
  44. Phan T. G., Okitsu S., Maneekarn N., Ushijima H. 2007; Genetic heterogeneity, evolution and recombination in emerging G9 rotaviruses. Infect Genet Evol 7:656–663 [View Article][PubMed]
     [Google Scholar]
  45. Rahman M., Matthijnssens J., Nahar S., Podder G., Sack D. A., Azim T., Van Ranst M. 2005; Characterization of a novel P[25],G11 human group a rotavirus. J Clin Microbiol 43:3208–3212 [View Article][PubMed]
     [Google Scholar]
  46. Rahman M., Matthijnssens J., Yang X., Delbeke T., Arijs I., Taniguchi K., Iturriza-Gómara M., Iftekharuddin N., Azim T., Van Ranst M. 2007; Evolutionary history and global spread of the emerging g12 human rotaviruses. J Virol 81:2382–2390 [View Article][PubMed]
     [Google Scholar]
  47. Ramachandran M., Das B. K., Vij A., Kumar R., Bhambal S. S., Kesari N., Rawat H., Bahl L., Thakur S. other authors 1996; Unusual diversity of human rotavirus G and P genotypes in India. J Clin Microbiol 34:436–439[PubMed]
     [Google Scholar]
  48. Ruiz A. M., López I. V., López S., Espejo R. T., Arias C. F. 1988; Molecular and antigenic characterization of porcine rotavirus YM, a possible new rotavirus serotype. J Virol 62:4331–4336[PubMed]
     [Google Scholar]
  49. Saitou N., Nei M. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425[PubMed]
     [Google Scholar]
  50. Santos N., Hoshino Y. 2005; Global distribution of rotavirus serotypes/genotypes and its implication for the development and implementation of an effective rotavirus vaccine. Rev Med Virol 15:29–56 [View Article][PubMed]
     [Google Scholar]
  51. Santos N., Lima R. C., Pereira C. F., Gouvea V. 1998; Detection of rotavirus types G8 and G10 among Brazilian children with diarrhea. J Clin Microbiol 36:2727–2729[PubMed]
     [Google Scholar]
  52. Tamura K., Dudley J., Nei M., Kumar S. 2007; MEGA4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
     [Google Scholar]
  53. Taniguchi K., Nishikawa K., Urasawa T., Urasawa S., Midthun K., Kapikian A. Z., Gorziglia M. 1989; Complete nucleotide sequence of the gene encoding VP4 of a human rotavirus (strain K8) which has unique VP4 neutralization epitopes. J Virol 63:4101–4106[PubMed]
     [Google Scholar]
  54. Than V. T., Park J. H., Chung I. S., Kim J. B., Kim W. 2013; Whole-genome sequence analysis of a Korean G11P[25] rotavirus strain identifies several porcine-human reassortant events. Arch Virol 158:2385–2393 [View Article][PubMed]
     [Google Scholar]
  55. Trojnar E., Sachsenröder J., Twardziok S., Reetz J., Otto P. H., Johne R. 2013; Identification of an avian group A rotavirus containing a novel VP4 gene with a close relationship to those of mammalian rotaviruses. J Gen Virol 94:136–142 [View Article][PubMed]
     [Google Scholar]
  56. Uchida R., Pandey B. D., Sherchand J. B., Ahmed K., Yokoo M., Nakagomi T., Cuevas L. E., Cunliffe N. A., Hart C. A., Nakagomi O. 2006; Molecular epidemiology of rotavirus diarrhea among children and adults in Nepal: detection of G12 strains with P[6] or P[8] and a G11P[25] strain. J Clin Microbiol 44:3499–3505 [View Article][PubMed]
     [Google Scholar]
  57. Varghese V., Das S., Singh N. B., Kojima K., Bhattacharya S. K., Krishnan T., Kobayashi N., Naik T. N. 2004; Molecular characterization of a human rotavirus reveals porcine characteristics in most of the genes including VP6 and NSP4. Arch Virol 149:155–172 [View Article][PubMed]
     [Google Scholar]
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Complete genome analysis of a rare group A rotavirus, G11P[25], isolated from a child in Mumbai, India, reveals interspecies transmission and reassortment with human rotavirus strains
J. Med. Microbiol. 63, 1220 (2014); https://doi.org/10.1099/jmm.0.070524-0
/content/journal/jmm/10.1099/jmm.0.070524-0
/content/journal/jmm/10.1099/jmm.0.070524-0
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