Genomic analysis of putative novel serotypes of Tibet orbivirus isolated in Japan

Abstract

Tibet orbivirus (TIBOV) was initially isolated in Tibet in 2009 and subsequently in Guangdong, Hunan, and Yunnan, China. We document the first isolation of TIBOV outside of China: two TIBOV isolates from Culicoides collected in 2009 and 2010 in Kagoshima, Japan. Their complete genome sequences were also determined. Our results suggest that the two virus isolates are of novel serotypes, evident by variability within genome segment 2 encoding VP2. These new putative TIBOV serotypes will help with future virus surveillance and with the evaluation of its potential to cause disease in domestic ruminants.

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References

  1. 1.

    Attoui H, Mertens PPC, Becnel J et al (2011) Order reoviridae. In: King AMQ, Adams MJ, Lefkowitz EJ, Carstens EB (eds) Virus taxonomy: IXth report of the international committee on taxonomy of viruses. Elsevier, London, pp 541–637

    Google Scholar 

  2. 2.

    Maclachlan NJ, Zientara S, Wilson WC et al (2019) Bluetongue and epizootic hemorrhagic disease viruses: recent developments with these globally re-emerging arboviral infections of ruminants. Curr Opin Virol 34:56–62. https://doi.org/10.1016/j.coviro.2018.12.005

    Article  PubMed  Google Scholar 

  3. 3.

    Dennis SJ, Meyers AE, Hitzeroth II, Rybicki EP (2019) African horse sickness: a review of current understanding and vaccine development. Viruses 11:844. https://doi.org/10.3390/v11090844

    CAS  Article  PubMed Central  Google Scholar 

  4. 4.

    Belhouchet M, Jaafar FM, Firth AE et al (2011) Detection of a fourth orbivirus non-structural protein. PLoS ONE 6:e25697. https://doi.org/10.1371/journal.pone.0025697

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Belaganahalli MN, Maan S, Maan NS et al (2015) Genetic characterization of the tick-borne orbiviruses. Viruses 7:2185–2209. https://doi.org/10.3390/v7052185

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. 6.

    White JR, Boyd V, Brangwyn JK et al (2004) Characterisation and monitoring of neutralisation-resistant VP2 phenotypes in BTV-1 isolates from northern Australia collected over a twenty-year period. Vet Ital 40:508–512

    CAS  PubMed  Google Scholar 

  7. 7.

    Heidner HW, Rossitto PV, MacLachlan NJ (1990) Identification of four distinct neutralizing epitopes on bluetongue virus serotype 10 using neutralizing monoclonal antibodies and neutralization-escape variants. Virology 176:658–661. https://doi.org/10.1016/0042-6822(90)90041-O

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Russell BL, Parbhoo N, Gildenhuys S (2018) Analysis of conserved, computationally predicted epitope regions for VP5 and VP7 across three orbiviruses. Bioinform Biol Insights 12:1177932218755348. https://doi.org/10.1177/1177932218755348

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Luo L, Sabara MI (2005) Production of a recombinant major inner capsid protein for serological detection of epizootic hemorrhagic disease virus. Clin Diagn Lab Immunol 12:904–909. https://doi.org/10.1128/CDLI.12.8.904-909.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Wilson WC, Ma HC, Venter EH et al (2000) Phylogenetic relationships of bluetongue viruses based on gene S7. Virus Res. 67:141–151. https://doi.org/10.1016/s0168-1702(00)00138-6

    CAS  Article  PubMed  Google Scholar 

  11. 11.

    Maan S, Maan NS, Ross-smith N et al (2008) Sequence analysis of bluetongue virus serotype 8 from the Netherlands 2006 and comparison to other European strains. Virology 377:308–318. https://doi.org/10.1016/j.virol.2008.04.028

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Li M, Zheng Y, Zhao G et al (2014) Tibet orbivirus, a novel orbivirus species isolated from Anopheles maculatus mosquitoes in Tibet, China. PLoS ONE 9:e88738. https://doi.org/10.1371/journal.pone.0088738

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Lei W, Guo X, Fu S et al (2015) Isolation of Tibet orbivirus, TIBOV, from Culicoides collected in Yunnan, China. PLoS ONE 10:e0136257. https://doi.org/10.1371/journal.pone.0136257

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  14. 14.

    Cao Y, Fu S, Song S et al (2019) Isolation and genome phylogenetic analysis of arthropod-borne viruses, including Akabane virus, from mosquitoes collected in Hunan province, China. Vector Borne Zoonotic Dis 19:62–72. https://doi.org/10.1089/vbz.2018.2267

    Article  PubMed  Google Scholar 

  15. 15.

    Wang J, Li H, He Y et al (2017) Isolation of Tibet orbivirus from Culicoides and associated infections in livestock in Yunnan, China. Virol J 14:105. https://doi.org/10.1186/s12985-017-0774-9

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. 16.

    Kato T, Yanase T, Suzuki M et al (2016) Monitoring for bovine arboviruses in the most southwestern islands in Japan between 1994 and 2014. BMC Vet Res 12:125. https://doi.org/10.1186/s12917-016-0747-z

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Murota K, Suda Y, Shirafuji H et al (2020) Identification and characterization of a novel orbivirus, Yonaguni orbivirus, isolated from cattle in the westernmost island of Japan. Arch Virol 165:2903–2908. https://doi.org/10.1007/s00705-020-04803-3

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Li Z, Yu M, Zhang H et al (2005) Improved rapid amplification of cDNA ends (RACE) for mapping both the 5′ and 3′ terminal sequences of paramyxovirus genomes. J Virol Methods 130:154–156. https://doi.org/10.1016/j.jviromet.2005.06.022

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Attoui H, Billoir F, Cantaloube JF et al (2000) Strategies for the sequence determination of viral dsRNA genomes. J Virol Methods 89:147–158. https://doi.org/10.1016/S0166-0934(00)00212-3

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Lemoine F, Damien C, Lefort V et al (2019) NGPhylogeny.fr: new generation phylogenetic services for non-specialists. Nucleic Acids Res 47:W260–W265. https://doi.org/10.1093/nar/gkz303

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    CAS  Article  Google Scholar 

  22. 22.

    Sievers F, Higgins DG (2014) Clustal omega, accurate alignment of very large numbers of sequences. Methods Mol Biol 1079:105–116. https://doi.org/10.1007/978-1-62703-646-7_6

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Xing S, Guo X, Zhang X et al (2017) A novel mosquito-borne reassortant orbivirus isolated from Xishuangbanna, China. Virol Sin 32:159–162. https://doi.org/10.1007/s12250-016-3886-2

    Article  PubMed  Google Scholar 

  24. 24.

    Wu D, Tan Q, Zhang H et al (2020) Genomic and biological features of a novel orbivirus isolated from mosquitoes, in China. Virus Res 285:197990. https://doi.org/10.1016/j.virusres.2020.197990

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Anthony SJ, Maan S, Maan N et al (2009) Genetic and phylogenetic analysis of the outer-coat proteins VP2 and VP5 of epizootic haemorrhagic disease virus (EHDV): comparison of genetic and serological data to characterise the EHDV serogroup. Virus Res 145:200–221. https://doi.org/10.1016/j.virusres.2009.07.012

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Maan S, Maan NS, Nomikou K et al (2011) Complete genome characterisation of a novel 26th bluetongue virus serotype from Kuwait. PLoS ONE 6:e26147. https://doi.org/10.1371/journal.pone.0026147

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Huismans H, van Staden V, Fick WC et al (2004) A comparison of different orbivirus proteins that could affect virulence and pathogenesis. Vet Ital 40:417–425

    CAS  PubMed  Google Scholar 

  28. 28.

    Otuka A (2013) Migration of rice planthoppers and their vectored re-emerging and novel rice viruses in East Asia. Front Microbiol 4:309. https://doi.org/10.3389/fmicb.2013.00309

    Article  PubMed  PubMed Central  Google Scholar 

  29. 29.

    Hayama Y, Moriguchi S, Yanase T et al (2016) Epidemiological analysis of bovine ephemeral fever in 2012–2013 in the subtropical islands of Japan. BMC Vet Res 12:47. https://doi.org/10.1186/s12917-016-0673-0

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Kurogi H, Akiba K, Inaba Y, Matumoto M (1987) Isolation of akabane virus from the biting midge Culicoides oxystoma in Japan. Vet Microbiol 15:243–248. https://doi.org/10.1016/0378-1135(87)90078-2

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Kurogi H, Suzuki T, Akashi H et al (1989) Isolation and preliminary characterization of an orbivirus of the Palyam serogroup from biting midge Culicoides oxystoma in Japan. Vet Microbiol 19:1–11. https://doi.org/10.1016/0378-1135(89)90086-2

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Yanase T, Kato T, Kubo T et al (2005) Isolation of bovine arboviruses from Culicoides biting midges (Diptera: Ceratopogonidae) in southern Japan: 1985–2002. J Med Entomol 42:63–67. https://doi.org/10.1093/JMEDENT/42.1.63

    CAS  Article  PubMed  Google Scholar 

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Funding

This study was conducted under the research project “Development of the Management Technologies for the Risk of Introduction of Livestock Infectious Diseases and Their Wildlife-borne Spreads in Japan (JP J008617. 18065101)” funded by the Ministry of Agriculture, Forestry and Fisheries of Japan.

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Correspondence to Tohru Yanase.

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Suda, Y., Murota, K., Shirafuji, H. et al. Genomic analysis of putative novel serotypes of Tibet orbivirus isolated in Japan. Arch Virol (2021). https://doi.org/10.1007/s00705-021-04966-7

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