Sapovirus is a genus of caliciviruses that are known to cause enteric disease in humans and animals. There is considerable genetic diversity among the sapoviruses, which are classified into different genogroups based on phylogenetic analysis of the full-length capsid protein sequence. While several mammalian species, including humans, pigs, minks, and dogs, have been identified as animal hosts for sapoviruses, there were no reports of sapoviruses in bats in spite of their biological diversity. In this report, we present the results of a targeted surveillance study in different bat species in Hong Kong. Five of the 321 specimens from the bat species, Hipposideros pomona, were found to be positive for sapoviruses by RT-PCR. Complete or nearly full-length genome sequences of approximately 7.7 kb in length were obtained for three strains, which showed similar organization of the genome compared to other sapoviruses. Interestingly, they possess many genomic features atypical of most sapoviruses, like high G+C content and minimal CpG suppression. Phylogenetic analysis of the viral proteins suggested that the bat sapovirus descended from an ancestral sapovirus lineage and is most closely related to the porcine sapoviruses. Codon usage analysis showed that the bat sapovirus genome has greater codon usage bias relative to other sapovirus genomes. In summary, we report the discovery and genomic characterization of the first bat calicivirus, which appears to have evolved under different conditions after early divergence from other sapovirus lineages.
References
[1]
Smiley JR, Chang KO, Hayes J, Vinje J, Saif LJ (2002) Characterization of an enteropathogenic bovine calicivirus representing a potentially new calicivirus genus. Journal of virology 76: 10089–10098.
[2]
Di Martino B, Di Profio F, Martella V, Ceci C, Marsilio F (2011) Evidence for recombination in neboviruses. Veterinary microbiology 153: 367–372.
[3]
Kaplon J, Guenau E, Asdrubal P, Pothier P, Ambert-Balay K (2011) Possible novel nebovirus genotype in cattle, France. Emerging infectious diseases 17: 1120–1123.
[4]
Farkas T, Sestak K, Wei C, Jiang X (2008) Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae. Journal of virology 82: 5408–5416.
[5]
Farkas T, Dufour J, Jiang X, Sestak K (2010) Detection of norovirus-, sapovirus- and rhesus enteric calicivirus-specific antibodies in captive juvenile macaques. The Journal of general virology 91: 734–738.
[6]
L'Homme Y, Sansregret R, Plante-Fortier E, Lamontagne AM, Ouardani M, et al. (2009) Genomic characterization of swine caliciviruses representing a new genus of Caliciviridae. Virus genes 39: 66–75.
[7]
Wolf S, Reetz J, Otto P (2011) Genetic characterization of a novel calicivirus from a chicken. Archives of virology 156: 1143–1150.
[8]
Chiba S, Sakuma Y, Kogasaka R, Akihara M, Horino K, et al. (1979) An outbreak of gastroenteritis associated with calicivirus in an infant home. Journal of medical virology 4: 249–254.
[9]
Clarke IN, Lambden PR (2000) Organization and expression of calicivirus genes. The Journal of infectious diseases 181: Suppl 2S309–316.
[10]
Atmar RL, Estes MK (2001) Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clinical microbiology reviews 14: 15–37.
[11]
L'Homme Y, Brassard J, Ouardani M, Gagne MJ (2010) Characterization of novel porcine sapoviruses. Archives of virology 155: 839–846.
[12]
Bank-Wolf BR, Konig M, Thiel HJ (2010) Zoonotic aspects of infections with noroviruses and sapoviruses. Veterinary microbiology 140: 204–212.
[13]
Rockx B, De Wit M, Vennema H, Vinje J, De Bruin E, et al. (2002) Natural history of human calicivirus infection: a prospective cohort study. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America 35: 246–253.
[14]
Chiba S, Nakata S, Numata-Kinoshita K, Honma S (2000) Sapporo virus: history and recent findings. The Journal of infectious diseases 181: Suppl 2S303–308.
[15]
Percival S, Chalmers R, Embrey M, Hunter P, Sellwood J, et al. (2004) Norovirus and sapovirus. Microbiology of Waterborne Diseases. London: Academic Press. pp. 433–444.
[16]
Logan C, O'Sullivan N (2007) Detection of viral agents of gastroenteritis: Norovirus, Sapovirus and Astrovirus. Future Virology 3: 61–70.
[17]
Svraka S, Vennema H, van der Veer B, Hedlund KO, Thorhagen M, et al. (2010) Epidemiology and genotype analysis of emerging sapovirus-associated infections across Europe. Journal of clinical microbiology 48: 2191–2198.
[18]
Pang XL, Lee BE, Tyrrell GJ, Preiksaitis JK (2009) Epidemiology and genotype analysis of sapovirus associated with gastroenteritis outbreaks in Alberta, Canada: 2004–2007. The Journal of infectious diseases 199: 547–551.
[19]
Tam CC, Rodrigues LC, Viviani L, Dodds JP, Evans MR, et al. (2011) Longitudinal study of infectious intestinal disease in the UK (IID2 study): incidence in the community and presenting to general practice. Gut.
[20]
Khamrin P, Maneekarn N, Peerakome S, Tonusin S, Malasao R, et al. (2007) Genetic diversity of noroviruses and sapoviruses in children hospitalized with acute gastroenteritis in Chiang Mai, Thailand. Journal of medical virology 79: 1921–1926.
[21]
Monica B, Ramani S, Banerjee I, Primrose B, Iturriza-Gomara M, et al. (2007) Human caliciviruses in symptomatic and asymptomatic infections in children in Vellore, South India. Journal of medical virology 79: 544–551.
[22]
Martella V, Lorusso E, Decaro N, Elia G, Radogna A, et al. (2008) Detection and molecular characterization of a canine norovirus. Emerging infectious diseases 14: 1306–1308.
[23]
Li L, Pesavento PA, Shan T, Leutenegger CM, Wang C, et al. (2011) Viruses in diarrhoeic dogs include novel kobuviruses and sapoviruses. The Journal of general virology 92: 2534–2541.
[24]
Martella V, Campolo M, Lorusso E, Cavicchio P, Camero M, et al. (2007) Norovirus in captive lion cub (Panthera leo). Emerging infectious diseases 13: 1071–1073.
[25]
Scipioni A, Mauroy A, Vinje J, Thiry E (2008) Animal noroviruses. Veterinary journal 178: 32–45.
[26]
Guo M, Evermann JF, Saif LJ (2001) Detection and molecular characterization of cultivable caliciviruses from clinically normal mink and enteric caliciviruses associated with diarrhea in mink. Archives of virology 146: 479–493.
[27]
Li L, Shan T, Wang C, Cote C, Kolman J, et al. (2011) The fecal viral flora of California sea lions. Journal of virology 85: 9909–9917.
[28]
Wilson DE, Reeder DM (2005) Mammal species of the world : a taxonomic and geographic reference. Baltimore: Johns Hopkins University Press.
[29]
Lau SK, Woo PC, Lai KK, Huang Y, Yip CC, et al. (2011) Complete genome analysis of three novel picornaviruses from diverse bat species. Journal of virology 85: 8819–8828.
[30]
Lau SK, Poon RW, Wong BH, Wang M, Huang Y, et al. (2010) Coexistence of different genotypes in the same bat and serological characterization of Rousettus bat coronavirus HKU9 belonging to a novel Betacoronavirus subgroup. Journal of virology 84: 11385–11394.
[31]
Lau SK, Woo PC, Wong BH, Wong AY, Tsoi HW, et al. (2010) Identification and complete genome analysis of three novel paramyxoviruses, Tuhoko virus 1, 2 and 3, in fruit bats from China. Virology 404: 106–116.
[32]
Lau SK, Woo PC, Li KS, Huang Y, Wang M, et al. (2007) Complete genome sequence of bat coronavirus HKU2 from Chinese horseshoe bats revealed a much smaller spike gene with a different evolutionary lineage from the rest of the genome. Virology 367: 428–439.
[33]
Woo PC, Lau SK, Li KS, Poon RW, Wong BH, et al. (2006) Molecular diversity of coronaviruses in bats. Virology 351: 180–187.
[34]
Lau SK, Li KS, Huang Y, Shek CT, Tse H, et al. (2010) Ecoepidemiology and complete genome comparison of different strains of severe acute respiratory syndrome-related Rhinolophus bat coronavirus in China reveal bats as a reservoir for acute, self-limiting infection that allows recombination events. Journal of virology 84: 2808–2819.
[35]
Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, et al. (2005) Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 102: 14040–14045.
[36]
Wong S, Lau S, Woo P, Yuen KY (2007) Bats as a continuing source of emerging infections in humans. Reviews in medical virology 17: 67–91.
[37]
Oka T, Katayama K, Ogawa S, Hansman GS, Kageyama T, et al. (2005) Proteolytic processing of sapovirus ORF1 polyprotein. Journal of virology 79: 7283–7290.
[38]
Oka T, Yamamoto M, Katayama K, Hansman GS, Ogawa S, et al. (2006) Identification of the cleavage sites of sapovirus open reading frame 1 polyprotein. The Journal of general virology 87: 3329–3338.
[39]
Hansman GS, Oka T, Takeda N (2008) Sapovirus-like particles derived from polyprotein. Virus research 137: 261–265.
[40]
Rima BK, McFerran NV (1997) Dinucleotide and stop codon frequencies in single-stranded RNA viruses. The Journal of general virology 78(Pt 11): 2859–2870.
[41]
Karlin S, Doerfler W, Cardon LR (1994) Why is CpG suppressed in the genomes of virtually all small eukaryotic viruses but not in those of large eukaryotic viruses? Journal of virology 68: 2889–2897.
[42]
Berke T, Matson DO (2000) Reclassification of the Caliciviridae into distinct genera and exclusion of hepatitis E virus from the family on the basis of comparative phylogenetic analysis. Archives of virology 145: 1421–1436.
[43]
Kapoor A, Simmonds P, Lipkin WI, Zaidi S, Delwart E (2010) Use of nucleotide composition analysis to infer hosts for three novel picorna-like viruses. Journal of virology 84: 10322–10328.
[44]
Greenbaum BD, Rabadan R, Levine AJ (2009) Patterns of oligonucleotide sequences in viral and host cell RNA identify mediators of the host innate immune system. PloS one 4: e5969.
[45]
ElHefnawi M, Alaidi O, Mohamed N, Kamar M, El-Azab I, et al. (2011) Identification of novel conserved functional motifs across most Influenza A viral strains. Virology journal 8: 44.
[46]
Lobo FP, Mota BE, Pena SD, Azevedo V, Macedo AM, et al. (2009) Virus-host coevolution: common patterns of nucleotide motif usage in Flaviviridae and their hosts. PloS one 4: e6282.
[47]
Shackelton LA, Parrish CR, Holmes EC (2006) Evolutionary basis of codon usage and nucleotide composition bias in vertebrate DNA viruses. Journal of molecular evolution 62: 551–563.
[48]
Tse H, Cai JJ, Tsoi HW, Lam EP, Yuen KY (2010) Natural selection retains overrepresented out-of-frame stop codons against frameshift peptides in prokaryotes. BMC genomics 11: 491.
[49]
Kim KH, Bae JW (2011) Amplification Methods Bias Metagenomic Libraries of Uncultured Single-Stranded and Double-Stranded DNA Viruses. Applied and environmental microbiology 77: 7763–7768.
[50]
Woo PC, Lau SK, Lam CS, Lai KK, Huang Y, et al. (2009) Comparative analysis of complete genome sequences of three avian coronaviruses reveals a novel group 3c coronavirus. Journal of virology 83: 908–917.
[51]
Woo PC, Lau SK, Huang Y, Lam CS, Poon RW, et al. (2010) Comparative analysis of six genome sequences of three novel picornaviruses, turdiviruses 1, 2 and 3, in dead wild birds, and proposal of two novel genera, Orthoturdivirus and Paraturdivirus, in the family Picornaviridae. The Journal of general virology 91: 2433–2448.
[52]
Tse H, Chan WM, Tsoi HW, Fan RY, Lau CC, et al. (2011) Rediscovery and genomic characterization of bovine astroviruses. The Journal of general virology 92: 1888–1898.
[53]
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic acids research 32: 1792–1797.
[54]
Criscuolo A, Gribaldo S (2010) BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC evolutionary biology 10: 210.
[55]
Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic biology 52: 696–704.
[56]
Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27: 1164–1165.
[57]
Anisimova M, Gascuel O (2006) Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Systematic biology 55: 539–552.
[58]
Etherington GJ, Dicks J, Roberts IN (2005) Recombination Analysis Tool (RAT): a program for the high-throughput detection of recombination. Bioinformatics 21: 278–281.
[59]
Supek F, Vlahovicek K (2004) INCA: synonymous codon usage analysis and clustering by means of self-organizing map. Bioinformatics 20: 2329–2330.
[60]
Wright F (1990) The ‘effective number of codons’ used in a gene. Gene 87: 23–29.
[61]
Novembre JA (2002) Accounting for background nucleotide composition when measuring codon usage bias. Molecular biology and evolution 19: 1390–1394.
[62]
Cardon LR, Burge C, Clayton DA, Karlin S (1994) Pervasive CpG suppression in animal mitochondrial genomes. Proceedings of the National Academy of Sciences of the United States of America 91: 3799–3803.
