Analysis of codon usage bias in the VP1 gene of the human norovirus GII.2 genotype

Haoning Wang; Guanglin Cui; Xiaolong Wang; Minghai Zhang; Jimin Tan; Xingguang Li

doi:10.14715/cmb/2017.64.15.18

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Vol. 64 No. 15: Issue 15

Issue Published : January 1, 2019

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Analysis of codon usage bias in the VP1 gene of the human norovirus GII.2 genotype

https://doi.org/10.14715/cmb/2017.64.15.18

Haoning Wang

College of Wildlife Resource, Northeast Forestry University, 26 Hexing Road, Xiangfang Distract, Harbin 150040, Heilongjiang, China

Guanglin Cui

Key Clinical Laboratory of Henan Province, Department of Clinical Laboratory, First Affiliated Hospital of Zhengzhou University, Zhengzhou 450052, Henan, China

Xiaolong Wang

College of Wildlife Resource, Northeast Forestry University, 26 Hexing Road, Xiangfang Distract, Harbin 150040, Heilongjiang, China

Minghai Zhang

College of Wildlife Resource, Northeast Forestry University, 26 Hexing Road, Xiangfang Distract, Harbin 150040, Heilongjiang, China

Jimin Tan

Jiangsu Engineering Laboratory of Animal Immunology, Institute of Immunology and College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210095, China

Xingguang Li

Hubei Engineering Research Center of Viral Vector, Wuhan University of Bioengineering, Wuhan, 430415, China

Corresponding Author(s) : Haoning Wang

qr1305@163.com

Cellular and Molecular Biology, Vol. 64 No. 15: Issue 15
Article Published : December 31, 2018

Abstract

To investigate the codon usage patterns of all available VP1 gene sequences of the GII.2 genotype, to determine the factors that affect these patterns, and to provide comprehensive details of the characteristics and evolution of the gene. Complete 519 sequences of VP1 gene of the HuNoV GII.2 genotype with known sampling dates and geographic locations from 1971 - 2017 were retrieved from the GenBank nucleotide database of the National Center for Biotechnology Information (NCBI) and analyzed. The percentage composition of T, C, A, and G nucleotides were 24.80 ± 0.30, 26.61 ± 0.31, 25.84 ± 0.13, and 22.75 ± 0.17 %, respectively, with C and A relatively more abundant than T and G, and C the most abundant (p < 0.0001). The values of T3s (34.10 ± 0.90 %) and C3s (33.54 ± 0.90 %) were significantly higher than those of A3s (29.98 ± 0.43 %) and G3s (24.13 ± 0.51 %) (p < 0.0001). While T3s was highest among the four nucleotides, G3s was the lowest. Among the 18 most frequently employed synonymous codons, six optional codons ended with T, five ended with C, five ended with A and two ended with G. Codons ending with T were the most frequently used. The ENC ranged from 51.90 to 54.25 (mean = 52.38 ± 0.43) among the 519 VP1 gene sequences. There were significant correlations between ENC and C % and G % (p < 0.01). Codons containing CpG (1 and 2 or 2 and 3 codon positions) showed the lowest frequencies, while 30, 29, and 2 codons were above, below and on the mean line, respectively. The first four principal components accounted for 69.11 % of the total variation, with the first, second, third, and fourth principal axes contributing 37.90, 14.83, 9.61, and 6.77 %, respectively. The strains were not clustered by country of isolation or year of sampling. Gravy were significantly correlated with T3s, C3s, G3s, GC3s, and ENC (p < 0.01). Mutation pressure and natural selection contributed to the codon usage bias of the VP1 gene of the HuNoV GII.2 genotype. There was a correlation between GC12s and GC3s (R2 = 0.032; p < 0.0001). The relative neutrality was 3.20 %, while natural selection was 96.80 %. The VP1 gene exhibits low codon usage bias which is affected primarily by natural selection, followed by mutation pressure and translational selection.

Keywords

Human norovirus GII.2 genotype Codon usage bias Natural selection Mutation pressure.

Wang, H., Cui, G., Wang, X., Zhang, M., Tan, J., & Li, X. (2018). Analysis of codon usage bias in the VP1 gene of the human norovirus GII.2 genotype. Cellular and Molecular Biology, 64(15), 107–112. https://doi.org/10.14715/cmb/2017.64.15.18

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References

Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 2008; 14: 1224-1231.
Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, et al. Norwalk virus shedding after experimental human infection. Emerg Infect Dis 2008; 14: 1553-1557.
Ruvoen-Clouet N, Belliot G, Le Pendu J. Noroviruses and histo-blood groups: the impact of common host genetic polymorphisms on virus transmission and evolution. Rev Med Virol 2013; 23: 355-366.
Sakon N, Sadamasu K, Shinkai T, Hamajima Y, Yoshitomi H, Matsushima Y, et al. Foodborne Outbreaks Caused by Human Norovirus GII.P17-GII.17-Contaminated Nori, Japan, 2017. Emerg Infect Dis 2018; 24: 920-923.
Swartling L, Ljungman P, Remberger M, Sundin M, Tiveljung A, Mattsson J, et al. Norovirus causing severe gastrointestinal disease following allogeneic hematopoietic stem cell transplantation: A retrospective analysis. Transpl Infect Dis 2018; 20: 12847.
Dunkin N, Weng SC, Coulter CG, Jacangelo JG, Schwab KJ. Impacts of virus processing on human norovirus GI and GII persistence during disinfection of municipal secondary wastewater effluent. Water Res 2018; 134: 1-12.
Boonchan M, Guntapong R, Sripirom N, Ruchusatsawat K, Singchai P, Rungnobhakhun P, et al. The dynamics of norovirus genotypes and genetic analysis of a novel recombinant GII.P12-GII.3 among infants and children in Bangkok, Thailand between 2014 and 2016. Infect Genet Evol 2018; 60: 133-139.
Thongprachum A, Okitsu S, Khamrin P, Maneekarn N, Hayakawa S, Ushijima H. Emergence of norovirus GII.2 and its novel recombination during the gastroenteritis outbreak in Japanese children in mid-2016. Infection Genetics and Evolution 51:86-88.
Hardy ME. 2005. Norovirus protein structure and function. Fems Microbiol Letter 2017; 253: 1-8.
Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. Viral shape-shifting: norovirus evasion of the human immune system. Nat Rev Microbiol 2010; 8: 231-241.
Siqueira JAM, Sousa EC, Linhares AD, Gabbay YB. Molecular analysis of norovirus in specimens from children enrolled in a 1982-1986 study in Belem, Brazil: A community-based longitudinal study. J Med Virol 2017; 89: 1539-1549.
Comeron JM, Aguade M. An evaluation of measures of synonymous codon usage bias. J Mol Evol 1998; 47: 268-274.
Sorensen MA, Kurland CG, Pedersen S. Codon Usage Determines Translation Rate in Escherichia-Coli. J Mol Biol 1989; 207: 365-377.
Eyrewalker AC. An Analysis of Codon Usage in Mammals - Selection or Mutation Bias. J Mol Evol 1991; 33: 442-449.
Schachtel GA, Bucher P, Mocarski ES, Blaisdell BE, Karlin S. Evidence for Selective Evolution in Codon Usage in Conserved Amino-Acid Segments of Human Alphaherpesvirus Proteins. J Mol Evol 1991; 33: 483-494.
Seetharaman J, Srinivasan R. Analysis of Codon Usage - Positional Preference in Various Organisms. Indian J Biochem Biophys 1995; 32: 156-160.
Karlin S, Burge C. Dinucleotide Relative Abundance Extremes - a Genomic Signature. Trends Genet 1995; 11: 283-290.
Butt AM, Nasrullah I, Qamar R, Tong YG. Evolution of codon usage in Zika virus genomes is host and vector specific. Emerg Microbes Infect 2016; 5: 107.
Fuglsang A. Impact of bias discrepancy and amino acid usage on estimates of the effective number of codons used in a gene, and a test for selection on codon usage. Gene 2008; 410: 82-88.
Fu JG, Ai J, Qi X, Zhang J, Tang FY, Zhu YF. Emergence of two novel norovirus genotype II.4 variants associated with viral gastroenteritis in China. J Med Virol 2014; 86: 1226-1234.
Godoy P, Artigues A, Bartolome R, Dominguez A, Plasencia A. Norovirus gastroenteritis outbreak by person to person transmision in a nursing home. Med Clin 2006; 127: 538-541.
Pothier P, Kaiser L. Norovirus disease today. Clin Microbiol Infect 2014; 20: 16.
Koo HS, Lee MO, Ku PT, Hwang SJ, Park DJ, Baik HS. Molecular epidemiology of norovirus in asymptomatic food handlers in Busan, Korea, and emergence of genotype GII.17. J Microbiol 2016; 54: 686-694.
Kobayashi M, Matsushima Y, Motoya T, Sakon N, Shigemoto N, Okamoto-Nakagawa R, et al. Molecular evolution of the capsid gene in human norovirus genogroup II. Sci Rep 2016; 6: 29400.
Lee CC, Feng Y, Chen SY, Tsai CN, Lai MW, Chiu CH. Emerging Norovirus GII. 17 in Taiwan. Clin Infect Dis 2015; 61: 1762.
Li JS, Qin M, Dong XG, Yang JY, Yang XX, Wei XX, et al. Norovirus outbreaks in Fengtai District, Beijing, China, 2014. Arch Virol 2016; 161: 2855-2858.
Polo TD, Peiro JR, Mendes LCN, Ludwig LF, de Oliveira EF, Bucardo F, et al. Human norovirus infection in Latin America. J Clin Virol 2016; 78: 111-119.
Rocha-Pereira J, Van Dycke J, Neyts J. Norovirus genetic diversity and evolution: implications for antiviral therapy. Curr Opin Virol 2016; 20: 92-98.
Fretz R. How is Norovirus-assosiated gastroenteritis important? Wien Klin Wochenschr 2005; 117: 785-788.
Larsson MM, Rydell GEP, Rodriguez-Diaz J, Akerlind B, Hutson AM, Estes MK, et al. Antibody prevalence and titer to norovirus (genogroup II) correlate with secretor (FUT2) but not with ABO phenotype or Lewis (FUT3) genotype. J Infect Dis 2006; 194: 1422-1427.

References

Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 2008; 14: 1224-1231.

Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, et al. Norwalk virus shedding after experimental human infection. Emerg Infect Dis 2008; 14: 1553-1557.

Ruvoen-Clouet N, Belliot G, Le Pendu J. Noroviruses and histo-blood groups: the impact of common host genetic polymorphisms on virus transmission and evolution. Rev Med Virol 2013; 23: 355-366.

Sakon N, Sadamasu K, Shinkai T, Hamajima Y, Yoshitomi H, Matsushima Y, et al. Foodborne Outbreaks Caused by Human Norovirus GII.P17-GII.17-Contaminated Nori, Japan, 2017. Emerg Infect Dis 2018; 24: 920-923.

Swartling L, Ljungman P, Remberger M, Sundin M, Tiveljung A, Mattsson J, et al. Norovirus causing severe gastrointestinal disease following allogeneic hematopoietic stem cell transplantation: A retrospective analysis. Transpl Infect Dis 2018; 20: 12847.

Dunkin N, Weng SC, Coulter CG, Jacangelo JG, Schwab KJ. Impacts of virus processing on human norovirus GI and GII persistence during disinfection of municipal secondary wastewater effluent. Water Res 2018; 134: 1-12.

Boonchan M, Guntapong R, Sripirom N, Ruchusatsawat K, Singchai P, Rungnobhakhun P, et al. The dynamics of norovirus genotypes and genetic analysis of a novel recombinant GII.P12-GII.3 among infants and children in Bangkok, Thailand between 2014 and 2016. Infect Genet Evol 2018; 60: 133-139.

Thongprachum A, Okitsu S, Khamrin P, Maneekarn N, Hayakawa S, Ushijima H. Emergence of norovirus GII.2 and its novel recombination during the gastroenteritis outbreak in Japanese children in mid-2016. Infection Genetics and Evolution 51:86-88.

Hardy ME. 2005. Norovirus protein structure and function. Fems Microbiol Letter 2017; 253: 1-8.

Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. Viral shape-shifting: norovirus evasion of the human immune system. Nat Rev Microbiol 2010; 8: 231-241.

Siqueira JAM, Sousa EC, Linhares AD, Gabbay YB. Molecular analysis of norovirus in specimens from children enrolled in a 1982-1986 study in Belem, Brazil: A community-based longitudinal study. J Med Virol 2017; 89: 1539-1549.

Comeron JM, Aguade M. An evaluation of measures of synonymous codon usage bias. J Mol Evol 1998; 47: 268-274.

Sorensen MA, Kurland CG, Pedersen S. Codon Usage Determines Translation Rate in Escherichia-Coli. J Mol Biol 1989; 207: 365-377.

Eyrewalker AC. An Analysis of Codon Usage in Mammals - Selection or Mutation Bias. J Mol Evol 1991; 33: 442-449.

Schachtel GA, Bucher P, Mocarski ES, Blaisdell BE, Karlin S. Evidence for Selective Evolution in Codon Usage in Conserved Amino-Acid Segments of Human Alphaherpesvirus Proteins. J Mol Evol 1991; 33: 483-494.

Seetharaman J, Srinivasan R. Analysis of Codon Usage - Positional Preference in Various Organisms. Indian J Biochem Biophys 1995; 32: 156-160.

Karlin S, Burge C. Dinucleotide Relative Abundance Extremes - a Genomic Signature. Trends Genet 1995; 11: 283-290.

Butt AM, Nasrullah I, Qamar R, Tong YG. Evolution of codon usage in Zika virus genomes is host and vector specific. Emerg Microbes Infect 2016; 5: 107.

Fuglsang A. Impact of bias discrepancy and amino acid usage on estimates of the effective number of codons used in a gene, and a test for selection on codon usage. Gene 2008; 410: 82-88.

Fu JG, Ai J, Qi X, Zhang J, Tang FY, Zhu YF. Emergence of two novel norovirus genotype II.4 variants associated with viral gastroenteritis in China. J Med Virol 2014; 86: 1226-1234.

Godoy P, Artigues A, Bartolome R, Dominguez A, Plasencia A. Norovirus gastroenteritis outbreak by person to person transmision in a nursing home. Med Clin 2006; 127: 538-541.

Pothier P, Kaiser L. Norovirus disease today. Clin Microbiol Infect 2014; 20: 16.

Koo HS, Lee MO, Ku PT, Hwang SJ, Park DJ, Baik HS. Molecular epidemiology of norovirus in asymptomatic food handlers in Busan, Korea, and emergence of genotype GII.17. J Microbiol 2016; 54: 686-694.

Kobayashi M, Matsushima Y, Motoya T, Sakon N, Shigemoto N, Okamoto-Nakagawa R, et al. Molecular evolution of the capsid gene in human norovirus genogroup II. Sci Rep 2016; 6: 29400.

Lee CC, Feng Y, Chen SY, Tsai CN, Lai MW, Chiu CH. Emerging Norovirus GII. 17 in Taiwan. Clin Infect Dis 2015; 61: 1762.

Li JS, Qin M, Dong XG, Yang JY, Yang XX, Wei XX, et al. Norovirus outbreaks in Fengtai District, Beijing, China, 2014. Arch Virol 2016; 161: 2855-2858.

Polo TD, Peiro JR, Mendes LCN, Ludwig LF, de Oliveira EF, Bucardo F, et al. Human norovirus infection in Latin America. J Clin Virol 2016; 78: 111-119.

Rocha-Pereira J, Van Dycke J, Neyts J. Norovirus genetic diversity and evolution: implications for antiviral therapy. Curr Opin Virol 2016; 20: 92-98.

Fretz R. How is Norovirus-assosiated gastroenteritis important? Wien Klin Wochenschr 2005; 117: 785-788.

Larsson MM, Rydell GEP, Rodriguez-Diaz J, Akerlind B, Hutson AM, Estes MK, et al. Antibody prevalence and titer to norovirus (genogroup II) correlate with secretor (FUT2) but not with ABO phenotype or Lewis (FUT3) genotype. J Infect Dis 2006; 194: 1422-1427.

Author biographies is not available.