Abstract
Among the tick-borne orbiviruses (genus Orbivirus, family Reoviridae), 36 serotypes are currently classified within a single virus species, Great Island virus. In this study, we report the first characterization of a tick-borne orbivirus isolated from the tick Ixodes turdus in Japan, which we identified as a new member of the species Great Island virus. The virus isolate, designated Muko virus (MUV), replicated and induced cytopathic effects in BHK-21, Vero E6, and CCL-141 cells and caused high mortality in suckling mice after intracerebral inoculation. Full genome sequence analysis showed that MUV shared the greatest phylogenetic similarity with Tribeč virus in terms of the amino acid sequences of all viral proteins except for outer capsid protein 1 (OC1; VP4 of MUV). Analysis of genome segment 9 in MUV detected an uninterrupted open reading frame that overlaps with VP6 (Hel), which putatively encodes a molecular and functional equivalent of NS4 from Great Island virus. Our study provides new insights into the geographic distribution, genetic diversity, and evolutionary history of the members of the species Great Island virus.
Similar content being viewed by others
References
Attoui H, Mertens PPC, Becnel J, Belaganahalli S, Bergoin M, Brussaard CP, Chappell JD, Ciarlet M, del Vas M, Dermody TS, Dormitzer PR, Duncan R, Fang Q, Graham R, Guglielmi KM, Harding RM, Hillman B, Makkay A, Marzachi C, Matthijnssens J, Milne RG, Mohd Jaafar F, Mori H, Noordeloos AA, Omura T, Patton JT, Rao S, Maan M, Stoltz D, Suzuki N, Upadhyaya NM, Wei C, Zhou H (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
Roy P, Noad R (2006) Bluetongue virus assembly and morphogenesis. Curr Top Microbiol Immunol 309:87–116
Limn CK, Staeuber N, Monastyrskaya K, Gouet P, Roy P (2000) Functional Dissection of the major structural protein of Bluetongue virus: identification of key residues within VP7 essential for capsid assembly. J Virol 74:8658–8669
Limn CK, Roy P (2003) Intermolecular interactions in a two-layered viral capsid that requires a complex symmetry mismatch. J Virol 77:11114–11124
Owens RJ, Limn CK, Roy P (2004) Role of an arbovirus nonstructural protein in cellular pathogenesis and virus release. J Virol 78:6649–6656
Hubalek Z, Rudolf I (2012) Tick-borne viruses in Europe. Parasitol Res 111:9–36
Gorman BM, Taylor J, Walker PJ (1983) Orbiviruses. Springer, US, pp 287–357
Nuttall PA (1984) Tick-borne viruses in seabird colonies. Seabird 7:31–41
Main AJ, Downs WG, Shope RE, Wallis RC (1976) Avian arboviruses of the Witless Bay seabird Sanctuary, Newfoundland, Canada. J Wildl Dis 12:182–194
Moss SR, Ayres CM, Nuttall PA (1988) The Great Island subgroup of tick-borne orbiviruses represents a single gene pool. J Gen Virol 69:2721–2727
Nunn MA, Barton TR, Wanless S, Hails RS, Harris MP, Nuttall PA (2006) Tick-borne Great Island Virus: (II) Impact of age-related acquired immunity on transmission in a natural seabird host. Parasitology 132:241–253
Belhouchet M, Mohd Jaafar F, Tesh R, Grimes J, Maan S, Mertens PP, Attoui H (2010) Complete sequence of Great Island virus and comparison with the T2 and outer-capsid proteins of Kemerovo, Lipovnik and Tribec viruses (genus Orbivirus, family Reoviridae). J Gen Virol 91:2985–2993
Gresikova M, Nosek J, Kozuch O, Ernek E, Lichard M (1965) Study on the ecology of Tribec virus. Acta Virol 9:83–88
Libikova H, Tesarova J, Rajcani J (1970) Experimental infection of monkeys with Kemerovo virus. Acta Virol 14:64–69
Ernek E, Kozuch O, Gresikova M (1966) Isolation of Tribec virus from the blood of sentinel pastured goats in Tribec region (Slovakia). Acta Virol 10:367–368
Libikova H, Heinz F, Ujhazyova D, Stunzner D (1978) Orbiviruses of the Kemerovo complex and neurological diseases. Med Microbiol Immunol 166:255–263
Libikova H, Mayer V, Kozuch O, Rehacek J, Ernek E, Albrecht P (1964) Isolation from ixodes persulcatus ticks of cytopathic agents (Kemerovo virus) differing from tick-borne encephalitis virus and some of their properties. Acta Virol 8:289–301
Libikova H, Ernek E, Albrecht P (1965) Pathogenicity and pathogenesis of Kemerovo virus and Kemerovo virus-like viruses in some laboratory and domestic mammals. Acta Virol 9:423–430
Belhouchet M, Mohd JF, Firth AE, Grimes JM, Mertens PP, Attoui H (2011) Detection of a fourth orbivirus non-structural protein. PLoS One 6:e25697
Dilcher M, Hasib L, Lechner M, Wieseke N, Middendorf M, Marz M, Koch A, Spiegel M, Dobler G, Hufert FT, Weidmann M (2012) Genetic characterization of Tribec virus and Kemerovo virus, two tick-transmitted human-pathogenic Orbiviruses. Virology 423:68–76
Ejiri H, Kuwata R, Tsuda Y, Sasaki T, Kobayashi M, Sato Y, Sawabe K, Isawa H (2014) First isolation and characterization of a mosquito-borne orbivirus belonging to the species Umatilla virus in East Asia. Arch Virol 159:2675–2685
Castillo A, Cottet L, Castro M, Sepulveda F (2011) Rapid isolation of mycoviral double-stranded RNA from Botrytis cinerea and Saccharomyces cerevisiae. Virol J 8:38
Attoui H, Billoir F, Cantaloube JF, Biagini P, de Micco P, de Lamballerie X (2000) Strategies for the sequence determination of viral dsRNA genomes. J Virol Methods 89:147–158
Palacios G, Cowled C, Bussetti AV, Savji N, Weir R, Wick I, Travassos da Rosa A, Calisher CH, Tesh RB, Boyle D, Lipkin WI (2011) Rapid molecular strategy for orbivirus detection and characterization. J Clin Microbiol 49:2314–2317
Gumm ID, Newman JF (1982) The preparation of purified bluetongue virus group antigen for use as a diagnostic reagent. Arch Virol 72:83–93
Belaganahalli MN, Maan S, Maan NS, Tesh R, Attoui H, Mertens PP (2011) Umatilla virus genome sequencing and phylogenetic analysis: identification of stretch lagoon orbivirus as a new member of the Umatilla virus species. PLoS One 6:e23605
Attoui H, Stirling JM, Munderloh UG, Billoir F, Brookes SM, Burroughs JN, de Micco P, Mertens PP, de Lamballerie X (2001) Complete sequence characterization of the genome of the St Croix River virus, a new orbivirus isolated from cells of Ixodes scapularis. J Gen Virol 82:795–804
Brown SE, Morrison HG, Buckley SM, Shope RE, Knudson DL (1988) Genetic relatedness of the Kemerovo serogroup viruses: I. RNA–RNA blot hybridization and gene reassortment in vitro of the Kemerovo serocomplex. Acta Virol 32:369–378
Brown SE, Morrison HG, Knudson DL (1989) Genetic relatedness of the kemerovo serogroup viruses: II. RNA–RNA blot hybridization and gene reassortment in vitro of the Great Island serocomplex. Acta Virol 33:206–220
Brown SE, Morrison HG, Knudson DL (1989) Genetic relatedness of the Kemerovo serogroup viruses: III. RNA–RNA blot hybridization and gene reassortment in vitro of the Chenuda serocomplex. Acta Virol 33:221–234
Nunn MA, Barton TR, Wanless S, Hails RS, Harris MP, Nuttall PA (2006) Tick-borne Great Island Virus: (I) Identification of seabird host and evidence for co-feeding and viraemic transmission. Parasitology 132:233–240
Nuttall PA, Carey D, Reid HW, Harrap KA (1981) Orbiviruses and bunyaviruses from a seabird colony in Scotland. J Gen Virol 57:127–137
Gresikova M, Rajcani J (1969) Experimental pathogenicity of Tribec arbovirus of mice. Acta Virol 13:114–118
Miyamoto K, Nakao M, Fujita H, Sato F (1993) The ixodid ticks on migratory birds in Japan and the isolation of Lyme disease spirochetes from bird-feeding ticks. Jpn J Sanit Zool 44:315–315
Yamauchi K (2001) A bibliograohical survey of host-parasite relationships between birds and ticks from Japan. Bull Hoshizaki Green Found 5:271–308 (in Japanese with English abstract)
Schmidt JR, Shope RE (1971) Kemerovo virus from a migrating common redstart of Eurasia. Acta Virol 15:112
Yamashina Institute for Ornithology (2002) Atlas of Japanese Migratory Birds from 1961 to 1995. Yamashina Institute for Ornithology, Chiba
Kang JG, Kim HC, Choi CY, Nam HY, Chae HY, Chong ST, Klein TA, Ko S, Chae JS (2013) Molecular detection of Anaplasma, Bartonella, and Borrelia species in ticks collected from migratory birds from Hong-do Island, Republic of Korea. Vector Borne Zoonotic Dis 13:215–225
Palomar AM, Portillo A, Santibanez P, Mazuelas D, Arizaga J, Crespo A, Gutierrez O, Cuadrado JF, Oteo JA (2013) Crimean-Congo hemorrhagic fever virus in ticks from migratory birds, Morocco. Emerg Infect Dis 19:260–263
Acknowledgments
Collection of tick samples was supported by the Pest Control Division of Nishinomiya City Office and the Hunter Association of Nishinomiya City. This study was also supported by a grant-in-aid from the Japan Society for the Promotion of Science (JSPS) Research Fellowships for Young Scientists (12J09845) and, in part, by a grant-in-aid from the Japanese Ministry of Health, Labor and Welfare (H24-Shinko-Ippan-007), JSPS KAKENHI (21406012, 25305010 and 25893151) and the Research Program on Emerging and Re-emerging Infectious Diseases from Japan Agency for Medical Research and Development, AMED.
Author information
Authors and Affiliations
Corresponding author
Additional information
H. Ejiri and C.-K. Lim contributed equally to this work as first authors.
Electronic supplementary material
Below is the link to the electronic supplementary material.
705_2015_2588_MOESM1_ESM.ppt
Supplementary Fig. 1 Alignment of the amino acid (aa) sequences of Muko virus (MUV) open reading frame (ORF)-X, Tribeč virus (TRBV) ORF-Xa and -Xb, Kemerovo virus (KEMV) ORF-Xa and -Xb, and Great Island virus (GIV) NS4 encoded in genome segment 9. The aa sequences of the overlapping ORFs in segment 9 from these four orbiviruses were aligned using GENETYX software. The ORF-Xa and -Xb sequences of TRBV and KEMV described in a previous study [20] are indicated by solid rectangles (ORF-Xa) and shaded in gray (ORF-Xb), respectively. (PPT 388 kb)
Rights and permissions
About this article
Cite this article
Ejiri, H., Lim, CK., Isawa, H. et al. Genetic and biological characterization of Muko virus, a new distinct member of the species Great Island virus (genus Orbivirus, family Reoviridae), isolated from ixodid ticks in Japan. Arch Virol 160, 2965–2977 (2015). https://doi.org/10.1007/s00705-015-2588-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-015-2588-7