Abstract
A recombinant norovirus, GII.P16-GII.4_Sydney2012, was first detected from nine patients with gastroenteritis in Kawasaki City, Japan, in 2016. The viral genome showed nucleotide sequence identities of 95.1% and 97.2% to the closest strains in the regions of 5′ terminus to ORF1 and ORF2 to 3′ terminus, respectively.
GENOME ANNOUNCEMENT
Norovirus is a major causative pathogen of acute gastroenteritis in humans of all age groups (1). The virus is classified into genogroups I to VII (GI to GVII) (2). Patients with gastroenteritis are typically infected by noroviruses GI and GII, which have 9 and 22 genotypes, respectively. Given the emergence of recombinant strains, norovirus experts recommend that genotyping for worldwide surveillance use two proteins: the RNA-dependent RNA polymerase (RdRp) gene in open reading frame 1 (ORF1) and the capsid viral protein 1 (VP1) gene in ORF2 (3).
A novel recombinant norovirus was detected in the diarrheal feces of nine patients in an outbreak in Kawasaki City, Japan, in 2016. The strain was assigned to GII.P16-GII.4_Sydney2012 by the norovirus genotyping tool (4). One strain was used for complete genome sequencing. Primers for amplifying the 5′ terminus-ORF1 fragments of GII.P16-GII.4 strain were based on the published sequence of GII.P16 (KJ407074). The fragment of the ORF2-3′ terminus was amplified as described previously (5, 6). The complete genome of the strain was sequenced using primers based on the closely related sequences of GII.P16 (KJ407074) and GII.4_Sydney2012 (AB972482). The 5′-terminal sequence was analyzed using the 5′ Full RACE Core Set (TaKaRa, Shiga, Japan).
Except for its poly(A) tail, the complete genome of GII.P16-GII.4_Sydney2012 was 7,560 bp in length. Its GC compositions were 48.5% and 48.8% in the the 5′ terminus-ORF1 and ORF2-3′ terminus sequences, respectively. The strain had nucleotide sequence identities of 95.1% to the closest Hu/GII/RUS/2012/GII.P16/Smolensk/S12-31 strain (KF895841) in the 5′ terminus-ORF1 and 97.2% to the closest Hu/GII/ITA/2013/GII.4_Sydney2012/PA13 strain (KF378731) in the ORF2-3′ terminus. The recombination breakpoint was predicted to be at nucleotide position 5088, which is in a sequence between ORF1 and ORF2 that is conserved on norovirus genomes (7).
To our knowledge, this is the first report of a complete genome sequence of norovirus GII.P16-GII.4_Sydney2012. Norovirus infection is caused mostly by the GII.4 genotype, followed by GII.2, GII.3, GII.6, and GII.17 (8–11). The most prevalent GII.4 contained GII.P4 and GII.Pe RdRp sequences, and GII.P16 strains with various VP1 genotypes have been detected in some countries (12–20). The amino acid identity was 95 to 100% among GII.P16 RdRp sequences, and these diverged phylogenetically into two clusters. GII.P16 showed an amino acid identity of 88 to 93% to GII.P4 and GII.Pe in the RdRp sequences. Some proteins within ORF1 are associated with the pathogenesis of norovirus (21, 22). Additionally, recent reports have shown that an interaction between the human norovirus GII RdRp and GII VP1 proteins, but not the murine norovirus VP1, enhanced host RIG-I-dependent interferon signaling activity via replicative RNA in a human cell line, whereas the GII VP2 downregulated the innate immune signaling (23, 24). Norovirus GII exhibits genetic diversity among the genotypes in the capsid sequence, which is crucial for host entry and the production of blocking antibodies, and also in the nonstructural polyprotein-coding sequence (25–28). Therefore, appropriate combinations of ORF1 and ORF2-ORF3 sequences may be associated with the enhancement of norovirus pathogenesis and infectivity, which leads to the prevalence of restricted genotypes.
Accession number(s).
The GenBank accession number for the norovirus Hu/GII/JP/2016/GII.P16-GII.4_Sydney2012/Kawasaki194 genome sequence is LC175468.
ACKNOWLEDGMENTS
We thank Gary C. Howard (Gladstone Institutes) for a critical review of the manuscript.
Footnotes
Citation Matsushima Y, Shimizu T, Ishikawa M, Komane A, Okabe N, Ryo A, Kimura H, Katayama K, Shimizu H. 2016. Complete genome sequence of a recombinant GII.P16-GII.4 norovirus detected in Kawasaki City, Japan, in 2016. Genome Announc 4(5):e01099-16. doi:10.1128/genomeA.01099-16.
REFERENCES
- 1.De Graaf M, van Beek J, Koopmans MP. 2016. Human norovirus transmission and evolution in a changing world. Nat Rev Microbiol 14:421–433. doi: 10.1038/nrmicro.2016.48. [DOI] [PubMed] [Google Scholar]
- 2.Vinjé J. 2015. Advances in laboratory methods for detection and typing of norovirus. J Clin Microbiol 53:373–381. doi: 10.1128/JCM.01535-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Kroneman A, Vega E, Vennema H, Vinjé J, White PA, Hansman G, Green K, Martella V, Katayama K, Koopmans M. 2013. Proposal for a unified norovirus nomenclature and genotyping. Arch Virol 158:2059–2068. doi: 10.1007/s00705-013-1708-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Kroneman A, Vennema H, Deforche K, v d Avoort H, Penaranda S, Oberste MS, Vinje J, Koopmans M. 2011. An automated genotyping tool for enteroviruses and noroviruses. J Clin Virol 51:121–125. doi: 10.1016/j.jcv.2011.03.006. [DOI] [PubMed] [Google Scholar]
- 5.Katayama K, Shirato-Horikoshi H, Kojima S, Kageyama T, Oka T, Hoshino F, Fukushi S, Shinohara M, Uchida K, Suzuki Y, Gojobori T, Takeda N. 2002. Phylogenetic analysis of the complete genome of 18 Norwalk-like viruses. Virology 299:225–239. doi: 10.1006/viro.2002.1568. [DOI] [PubMed] [Google Scholar]
- 6.Motomura K, Oka T, Yokoyama M, Nakamura H, Mori H, Ode H, Hansman GS, Katayama K, Kanda T, Tanaka T, Takeda N, Sato H, Norovirus Surveillance Group of Japan . 2008. Identification of monomorphic and divergent haplotypes in the 2006–2007 norovirus GII/4 epidemic population by genomewide tracing of evolutionary history. J Virol 82:11247–11262. doi: 10.1128/JVI.00897-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. 2015. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol 1:vev003. doi: 10.1093/ve/vev003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Centers for Disease Control and Prevention 2016. CaliciNet data. http://www.cdc.gov/norovirus/reporting/calicinet/data.html.
- 9.Infectious Disease Surveillance Center, National Institute of Infectious Diseases . 2014. Epidemiology of norovirus in Japan, 2010/11–2013/14 seasons. IASR 35:161–163. [Google Scholar]
- 10.Infectious Disease Surveillance Center, National Institute of Infectious Diseases . 2010. Norovirus epidemic in Japan during 2006/7–2009/10 seasons. IASR 31:312–314. [Google Scholar]
- 11.Matsushima Y, Ishikawa M, Shimizu T, Komane A, Kasuo S, Shinohara M, Nagasawa K, Kimura H, Ryo A, Okabe N, Haga K, Doan Y, Katayama K, Shimizu H. 2015. Genetic analyses of GII.17 norovirus strains in diarrheal disease outbreaks from December 2014 to March 2015 in Japan reveal a novel polymerase sequence and amino acid substitutions in the capsid region. Euro Surveill 20:pii21173. doi: 10.2807/1560-7917.ES2015.20.26.21173. [DOI] [PubMed] [Google Scholar]
- 12.Kim JS, Kim HS, Hyun J, Kim HS, Song W. 2015. Molecular epidemiology of human norovirus in Korea in 2013. BioMed Res Int 2015:468304. doi: 10.1155/2015/468304. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Mahar JE, Kirkwood CD. 2011. Characterization of norovirus strains in Australian children from 2006 to 2008: prevalence of recombinant strains. J Med Virol 83:2213–2219. doi: 10.1002/jmv.22215. [DOI] [PubMed] [Google Scholar]
- 14.Mans J, Murray TY, Nadan S, Netshikweta R, Page NA, Taylor MB. 2016. Norovirus diversity in children with gastroenteritis in South Africa from 2009 to 2013: GII.4 variants and recombinant strains predominate. Epidemiol Infect 144:907–916. doi: 10.1017/S0950268815002150. [DOI] [PubMed] [Google Scholar]
- 15.Mans J, Murray TY, Taylor MB. 2014. Novel norovirus recombinants detected in South Africa. Virol J 11:168. doi: 10.1186/1743-422X-11-168. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Medici MC, Tummolo F, Martella V, Giammanco GM, De Grazia S, Arcangeletti MC, De Conto F, Chezzi C, Calderaro A. 2014. Novel recombinant GII.P16_GII.13 and GII.P16_GII.3 norovirus strains in Italy. Virus Res 188:142–145. doi: 10.1016/j.virusres.2014.04.005. [DOI] [PubMed] [Google Scholar]
- 17.Nahar S, Afrad MH, Matthijnssens J, Rahman MZ, Momtaz Z, Yasmin R, Jubair M, Faruque AS, Choudhuri MS, Azim T, Rahman M. 2013. Novel intergenotype human norovirus recombinant GII.16/GII.3 in Bangladesh. Infect Genet Evol 20:325–329. doi: 10.1016/j.meegid.2013.09.021. [DOI] [PubMed] [Google Scholar]
- 18.Wang YH, Zhou DJ, Zhou X, Yang T, Ghosh S, Pang BB, Peng JS, Liu MQ, Hu Q, Kobayashi N. 2012. Molecular epidemiology of noroviruses in children and adults with acute gastroenteritis in Wuhan, China, 2007–2010. Arch Virol 157:2417–2424. doi: 10.1007/s00705-012-1437-1. [DOI] [PubMed] [Google Scholar]
- 19.Wu X, Han J, Chen L, Xu D, Shen Y, Zha Y, Zhu X, Ji L. 2015. Prevalence and genetic diversity of noroviruses in adults with acute gastroenteritis in Huzhou, China, 2013–2014. Arch Virol 160:1705–1713. doi: 10.1007/s00705-015-2440-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Zhirakovskaia EV, Tikunov AY, Bodnev SA, Klemesheva VV, Netesov SV, Tikunova NV. 2015. Molecular epidemiology of noroviruses associated with sporadic gastroenteritis in children in Novosibirsk, Russia, 2003–2012. J Med Virol 87:740–753. doi: 10.1002/jmv.24068. [DOI] [PubMed] [Google Scholar]
- 21.Ettayebi K, Hardy ME. 2003. Norwalk virus nonstructural protein p48 forms a complex with the SNARE regulator VAP-A and prevents cell surface expression of vesicular stomatitis virus G protein. J Virol 77:11790–11797. doi: 10.1128/JVI.77.21.11790-11797.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Sharp TM, Guix S, Katayama K, Crawford SE, Estes MK. 2010. Inhibition of cellular protein secretion by Norwalk virus nonstructural protein p22 requires a mimic of an endoplasmic reticulum export signal. PLoS One 5:e13130. doi: 10.1371/journal.pone.0013130. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Subba-Reddy CV, Goodfellow I, Kao CC. 2011. VPg-primed RNA synthesis of norovirus RNA-dependent RNA polymerases by using a novel cell-based assay. J Virol 85:13027–13037. doi: 10.1128/JVI.06191-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Subba-Reddy CV, Yunus MA, Goodfellow IG, Kao CC. 2012. Norovirus RNA synthesis is modulated by an interaction between the viral RNA-dependent RNA polymerase and the major capsid protein, VP1. J Virol 86:10138–10149. doi: 10.1128/JVI.01208-12. [DOI] [PMC free article] [PubMed] [Google Scholar] [Retracted]
- 25.Chakravarty S, Hutson AM, Estes MK, Prasad BV. 2005. Evolutionary trace residues in noroviruses: importance in receptor binding, antigenicity, virion assembly, and strain diversity. J Virol 79:554–568. doi: 10.1128/JVI.79.1.554-568.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Kobayashi M, Matsushima Y, Motoya T, Sakon N, Shigemoto N, Okamoto-Nakagawa R, Nishimura K, Yamashita Y, Kuroda M, Saruki N, Ryo A, Saraya T, Morita Y, Shirabe K, Ishikawa M, Takahashi T, Shinomiya H, Okabe N, Nagasawa K, Suzuki Y, Katayama K, Kimura H. 2016. Molecular evolution of the capsid gene in human norovirus genogroup II. Sci Rep 6:29400. doi: 10.1038/srep29400. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Tan M, Hegde RS, Jiang X. 2004. The P domain of norovirus capsid protein forms dimer and binds to histo-blood group antigen receptors. J Virol 78:6233–6242. doi: 10.1128/JVI.78.12.6233-6242.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Yun SI, Kim JK, Song BH, Jeong AY, Jee YM, Lee CH, Paik SY, Koo Y, Jeon I, Byun SJ, Lee YM. 2010. Complete genome sequence and phylogenetic analysis of a recombinant Korean norovirus, CBNU1, recovered from a 2006 outbreak. Virus Res 152:137–152. doi: 10.1016/j.virusres.2010.06.018. [DOI] [PubMed] [Google Scholar]
