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Journal of General Virology header logo Journal of General Virology

Volume 100, Issue 10

Updated classification of norovirus genogroups and genotypes Free

Abstract

Noroviruses are genetically diverse RNA viruses associated with acute gastroenteritis in mammalian hosts. Phylogenetically, they can be segregated into different genogroups as well as P (polymerase)-groups and further into genotypes and P-types based on amino acid diversity of the complete VP1 gene and nucleotide diversity of the RNA-dependent RNA polymerase (RdRp) region of ORF1, respectively. In recent years, several new noroviruses have been reported that warrant an update of the existing classification scheme. Using previously described 2× standard deviation (sd) criteria to group sequences into separate clusters, we expanded the number of genogroups to 10 (GI-GX) and the number of genotypes to 49 (9 GI, 27 GII, 3 GIII, 2 GIV, 2 GV, 2 GVI and 1 genotype each for GVII, GVIII, GIX [formerly GII.15] and GX). Viruses for which currently only one sequence is available in public databases were classified into tentative new genogroups (GNA1 and GNA2) and genotypes (GII.NA1, GII.NA2 and GIV.NA1) with their definitive assignment awaiting additional related sequences. Based on nucleotide diversity in the RdRp region, noroviruses can be divided into 60 P-types (14 GI, 37 GII, 2 GIII, 1 GIV, 2 GV, 2 GVI, 1 GVII and 1 GX), 2 tentative P-groups and 14 tentative P-types. Future classification and nomenclature updates will be based on complete genome sequences and will be coordinated and disseminated by the international norovirus classification-working group.

  • Received:
  • Accepted:
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Keyword(s): 2xSD criteria , acute gastroenteritis , classification , genogroup , genotype , Norovirus , P-group and P-type
© Microbiology Society

Erratum

An erratum has been published for this content:
Corrigendum: Updated classification of norovirus genogroups and genotypes
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2019-09-04
2024-12-26
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References

  1. Di Martino B, Di Profio F, Melegari I, Sarchese V, Cafiero MA et al. A novel feline norovirus in diarrheic cats. Infect Genet Evol 2016; 38:132–137 [View Article]
     [Google Scholar]
  2. Green K. Caliciviridae: The noroviruses. In Knipe DM, Howley PM. (editors) Fields virology Philadelphia, PA: Lippincott Williams & Wilkins; 2013 pp 586–608
     [Google Scholar]
  3. Karst SM, Wobus CE, Lay M, Davidson J, Virgin HW. Stat1-Dependent innate immunity to a Norwalk-like virus. Science 2003; 299:1575–1578 [View Article]
     [Google Scholar]
  4. Liu BL, Lambden PR, Günther H, Otto P, Elschner M et al. Molecular characterization of a bovine enteric calicivirus: relationship to the Norwalk-like viruses. J Virol 1999; 73:819–825
     [Google Scholar]
  5. Mesquita JR, Barclay L, Nascimento MSJ, Vinjé J. Novel norovirus in dogs with diarrhea. Emerg Infect Dis 2010; 16:980–982 [View Article]
     [Google Scholar]
  6. Shen Q, Zhang W, Yang S, Cui L, Hua X. Complete genome sequence of a new-genotype porcine norovirus isolated from piglets with diarrhea. J Virol 2012; 86:7015–7016 [View Article]
     [Google Scholar]
  7. Wang Q-H, Han MG, Cheetham S, Souza M, Funk JA et al. Porcine noroviruses related to human noroviruses. Emerg Infect Dis 2005; 11:1874–1881 [View Article]
     [Google Scholar]
  8. Wolf S, Williamson W, Hewitt J, Lin S, Rivera-Aban M et al. Molecular detection of norovirus in sheep and pigs in New Zealand farms. Vet Microbiol 2009; 133:184–189 [View Article]
     [Google Scholar]
  9. de Graaf M, Bodewes R, van Elk CE, van de Bildt M, Getu S et al. Norovirus infection in harbor porpoises. Emerg Infect Dis 2017; 23:87–91 [View Article]
     [Google Scholar]
  10. Shi M, Lin X-D, Chen X, Tian J-H, Chen L-J et al. The evolutionary history of vertebrate RNA viruses. Nature 2018; 556:197–202 [View Article]
     [Google Scholar]
  11. Teng JLL, Martelli P, Chan W-M, Lee HH, Hui S-W et al. Two novel noroviruses and a novel norovirus genogroup in California sea lions. J Gen Virol 2018; 99:777–782 [View Article]
     [Google Scholar]
  12. Wu Z, Yang L, Ren X, He G, Zhang J et al. Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases. Isme J 2016; 10:609–620 [View Article]
     [Google Scholar]
  13. Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis 2014; 14:725–730 [View Article]
     [Google Scholar]
  14. Bányai K, Estes MK, Martella V, Parashar UD. Viral gastroenteritis. The Lancet 2018; 392:175–186 [View Article]
     [Google Scholar]
  15. Lee S, Liu H, Wilen CB, Sychev ZE, Desai C et al. A secreted viral nonstructural protein determines intestinal norovirus pathogenesis. Cell Host Microbe 2019; 25:e845845–857 [View Article]
     [Google Scholar]
  16. Hutson AM, Atmar RL, Marcus DM, Estes MK. Norwalk virus-like particle hemagglutination by binding to H histo-blood group antigens. J Virol 2003; 77:405–415 [View Article]
     [Google Scholar]
  17. Vongpunsawad S, Venkataram Prasad BV, Estes MK. Norwalk virus minor capsid protein VP2 associates within the VP1 shell domain. J Virol 2013; 87:4818–4825 [View Article]
     [Google Scholar]
  18. Conley MJ, McElwee M, Azmi L, Gabrielsen M, Byron O et al. Calicivirus VP2 forms a portal-like assembly following receptor engagement. Nature 2019; 565:377–381 [View Article]
     [Google Scholar]
  19. Kroneman A, Vega E, Vennema H, Vinjé J, White PA et al. Proposal for a unified norovirus Nomenclature and genotyping. Arch Virol 2013; 158:2059–2068 [View Article]
     [Google Scholar]
  20. Ando T, Monroe SS, Gentsch JR, Jin Q, Lewis DC et al. Detection and differentiation of antigenically distinct small round-structured viruses (Norwalk-like viruses) by reverse transcription-PCR and southern hybridization. J Clin Microbiol 1995; 33:64–71
     [Google Scholar]
  21. Green SM, Lambden PR, Caul EO, Ashley CR, Clarke IN. Capsid diversity in small round-structured viruses: molecular characterization of an antigenically distinct human enteric calicivirus. Virus Res 1995; 37:271–283 [View Article]
     [Google Scholar]
  22. Nakayama M, Ueda Y, Kawamoto H, Han-jun Y, Saito K et al. Detection and sequencing of Norwalk-like viruses from stool samples in Japan using reverse transcription-polymerase chain reaction amplification. Microbiol Immunol 1996; 40:317–320 [View Article]
     [Google Scholar]
  23. Vinjé J, Koopmans MP. Molecular detection and epidemiology of small round-structured viruses in outbreaks of gastroenteritis in the Netherlands. J Infect Dis 1996; 174:610–615 [View Article]
     [Google Scholar]
  24. Vinjé J, Green J, Lewis DC, Gallimore CI, Brown DW et al. Genetic polymorphism across regions of the three open reading frames of "Norwalk-like viruses". Arch Virol 2000; 145:223–241 [View Article]
     [Google Scholar]
  25. Zheng DP, Ando T, Fankhauser RL, Beard RS, Glass RI et al. Norovirus classification and proposed strain nomenclature. Virology 2006; 346:312–323 [View Article]
     [Google Scholar]
  26. Kageyama T, Shinohara M, Uchida K, Fukushi S, Hoshino FB et al. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to norovirus in Japan. J Clin Microbiol 2004; 42:2988–2995 [View Article]
     [Google Scholar]
  27. Vinjé J. Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol 2015; 53:373–381 [View Article]
     [Google Scholar]
  28. de Graaf M, van Beek J, Koopmans MPG. Human norovirus transmission and evolution in a changing world. Nat Rev Microbiol 2016; 14:421–433 [View Article]
     [Google Scholar]
  29. Ford-Siltz L, Mullis L, Sanad Y, Tohma K, Lepore C et al. Genomics analyses of GIV and GVI noroviruses reveal the distinct clustering of human and animal viruses. Viruses 2019; 11:204 [View Article]
     [Google Scholar]
  30. Bull RA, White PA. Mechanisms of GII.4 norovirus evolution. Trends Microbiol 2011; 19:233–240 [View Article]
     [Google Scholar]
  31. Lim KL, Hewitt J, Sitabkhan A, Eden JS, Lun J et al. A multi-site study of norovirus molecular epidemiology in Australia and New Zealand, 2013-2014. PLoS One 2016; 11:e0145254 [View Article]
     [Google Scholar]
  32. Mahar JE, Bok K, Green KY, Kirkwood CD. The importance of intergenic recombination in norovirus GII.3 evolution. J Virol 2013; 87:3687–3698 [View Article]
     [Google Scholar]
  33. Mans J, Murray TY, Nadan S, Netshikweta R, Page NA et al. Norovirus diversity in children with gastroenteritis in South Africa from 2009 to 2013: GII.4 variants and recombinant strains predominate. Epidemiol Infect 2016; 144:907–916 [View Article]
     [Google Scholar]
  34. Mathijs E, Muylkens B, Mauroy A, Ziant D, Delwiche T et al. Experimental evidence of recombination in murine noroviruses. J Gen Virol 2010; 91:2723–2733 [View Article]
     [Google Scholar]
  35. Medici MC, Tummolo F, Martella V, Giammanco GM, De Grazia S et al. Novel recombinant GII.P16_GII.13 and GII.P16_GII.3 norovirus strains in Italy. Virus Res 2014; 188:142–145 [View Article]
     [Google Scholar]
  36. Zhang H, Cockrell SK, Kolawole AO, Rotem A, Serohijos AWR et al. Isolation and analysis of rare norovirus recombinants from coinfected mice using Drop-Based Microfluidics. J Virol 2015; 89:7722–7734 [View Article]
     [Google Scholar]
  37. Cannon JL, Barclay L, Collins NR, Wikswo ME, Castro CJ et al. Genetic and epidemiologic trends of norovirus outbreaks in the United States from 2013 to 2016 demonstrated emergence of novel GII.4 recombinant viruses. J Clin Microbiol 2017; 55:2208–2221 [View Article]
     [Google Scholar]
  38. Jothikumar N, Lowther JA, Henshilwood K, Lees DN, Hill VR et al. Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples. Appl Environ Microbiol 2005; 71:1870–1875 [View Article]
     [Google Scholar]
  39. Kageyama T, Kojima S, Shinohara M, Uchida K, Fukushi S et al. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol 2003; 41:1548–1557 [View Article]
     [Google Scholar]
  40. Degiuseppe JI, Gomes KA, Hadad MF, Parra GI, Stupka JA. Detection of novel GII.17 norovirus in Argentina, 2015. Infect Gen Evol 2017; 47:121–124 [View Article]
     [Google Scholar]
  41. Fioretti JM, Fumian TM, Rocha MS, Dos Santos IdeAL, Carvalho-Costa FA et al. Surveillance of noroviruses in Rio de Janeiro, Brazil: occurrence of new GIV genotype in clinical and wastewater samples. Food Environ Virol 2018; 10:1–6 [View Article]
     [Google Scholar]
  42. Kuroda M, Masuda T, Ito M, Naoi Y, Doan YH et al. Genetic diversity and intergenogroup recombination events of sapoviruses detected from feces of pigs in Japan. Infect Gen Evol 2017; 55:209–217 [View Article]
     [Google Scholar]
  43. Pietsch C, Ennuschat N, Härtel S, Liebert UG. Within-Host evolution of virus variants during chronic infection with novel GII.P26-GII.26 norovirus. J Clin Virol 2018; 108:96–102 [View Article]
     [Google Scholar]
  44. van Beek J, de Graaf M, Al-Hello H, Allen DJ, Ambert-Balay K et al. Molecular surveillance of norovirus, 2005-16: an epidemiological analysis of data collected from the NoroNet network. Lancet Infect Dis 2018; 18:545–553 [View Article]
     [Google Scholar]
  45. Chhabra P, Aswath K, Collins N, Ahmed T, Olórtegui MP et al. Near-Complete genome sequences of several new norovirus genogroup II genotypes. Genome Announc 2018; 6:e00007-18 [View Article]
     [Google Scholar]
  46. Kitajima M, Rachmadi AT, Iker BC, Haramoto E, Gerba CP. Genetically distinct genogroup IV norovirus strains identified in wastewater. Arch Virol 2016; 161:3521–3525 [View Article]
     [Google Scholar]
  47. Lizasoain A, Tort LFL, García M, Gómez MM, Leite JPG et al. Sewage surveillance reveals the presence of canine GVII norovirus and canine astrovirus in Uruguay. Arch Virol 2015; 160:2839–2843 [View Article]
     [Google Scholar]
  48. Tohma K, Saito M, Mayta H, Zimic M, Lepore CJ et al. Complete genome sequence of a nontypeable GII norovirus detected in Peru. Genome Announc 2018; 6:e00095-18 [View Article]
     [Google Scholar]
  49. Tse H, Lau SKP, Chan WM, Choi GKY, Woo PCY et al. Complete genome sequences of novel canine noroviruses in Hong Kong. J Virol 2012; 86:9531–9532 [View Article]
     [Google Scholar]
  50. Okada M, Ogawa T, Kaiho I, Shinozaki K. Genetic analysis of noroviruses in Chiba Prefecture, Japan, between 1999 and 2004. J Clin Microbiol 2005; 43:4391–4401 [View Article]
     [Google Scholar]
  51. Matsushima Y, Shimizu T, Ishikawa M, Komane A, Okabe N et al. Complete genome sequence of a recombinant GII.P16-GII.4 norovirus detected in Kawasaki City, Japan, in 2016. Genome Announc 2016; 4:e01099-16 [View Article]
     [Google Scholar]
  52. Bull RA, Tanaka MM, White PA. Norovirus recombination. J Gen Virol 2007; 88:3347–3359 [View Article]
     [Google Scholar]
  53. Ludwig-Begall LF, Mauroy A, Thiry E. Norovirus recombinants: recurrent in the field, recalcitrant in the lab - a scoping review of recombination and recombinant types of noroviruses. J Gen Virol 2018; 99:970–988 [View Article]
     [Google Scholar]
  54. Brown JR, Roy S, Ruis C, Yara Romero E, Shah D et al. Norovirus whole-genome sequencing by SureSelect _target enrichment: a robust and sensitive method. J Clin Microbiol 2016; 54:2530–2537 [View Article]
     [Google Scholar]
  55. Fonager J, Stegger M, Rasmussen LD, Poulsen MW, Rønn J et al. A universal primer-independent next-generation sequencing approach for investigations of norovirus outbreaks and novel variants. Sci Rep 2017; 7:813 [View Article]
     [Google Scholar]
  56. Parra GI, Squires RB, Karangwa CK, Johnson JA, Lepore CJ et al. Static and evolving norovirus genotypes: implications for epidemiology and immunity. PLoS Pathog 2017; 13:e1006136 [View Article]
     [Google Scholar]
  57. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 2018; 35:1547–1549 [View Article]
     [Google Scholar]
  58. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003; 52:696–704 [View Article]
     [Google Scholar]
  59. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article]
     [Google Scholar]
  60. Fourment M, Gibbs MJ. PATRISTIC: a program for calculating patristic distances and graphically comparing the components of genetic change. BMC Evol Biol 2006; 6:1 [View Article]
     [Google Scholar]
  61. Team R. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013. ISBN 20143-900051-07-0
     [Google Scholar]
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Updated classification of norovirus genogroups and genotypes
J. Gen. Virol. 100, 1393 (2019); https://doi.org/10.1099/jgv.0.001318
/content/journal/jgv/10.1099/jgv.0.001318
/content/journal/jgv/10.1099/jgv.0.001318
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