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The complete genome sequence of a G3P[10] Chinese bat rotavirus suggests multiple bat rotavirus inter-host species transmission events
Infection, Genetics and Evolution 28 (2014) 1–4
Contents lists available at ScienceDirect
Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid
Correspondence The complete genome sequence of a G3P[10] Chinese bat rotavirus suggests multiple bat rotavirus inter-host species transmission events
Dear Editor, Species A rotavirus (RVA) can cause significant diarrhea in the young of various mammalian and avian species (Estes and Greenberg, 2013). RVA possesses 11 segments of double strand RNA (dsRNA) expressing six structural proteins (VP1–VP4, VP6, and VP7) and five or six non-structural proteins (NSP1–NSP5 and sometimes NSP6) (Estes and Greenberg, 2013). A uniform classification system exists for each of the 11 RVA gene segments (VP7, VP4, VP6, VP1-VP3, NSP1-NSP5) defining G-, P-, I- R-, C-, M-, A-, N-, T-, E- and H-genotypes, respectively (Matthijnssens et al., 2008). Despite this seemingly close host range restriction, RVA strains are known to frequently cross the host species barrier, resulting in the detection of RVA strains unusual to that host species (Matthijnssens et al., 2010; Mino et al., 2013; Khamrin et al., 2009). Often, but not always, such inter-host species transmissions are dead-end infections. Bats are important viral reservoirs and more than 130 viruses have been found in bats with many being highly pathogenic for humans, such as Ebola virus, Nipah virus, Hendra virus and Lyssavirus (Calisher et al., 2006; Luis et al., 2013). Esona et al. reported the first bat RVA strain RVA/Bat-wt/KEN/KE4852/2007/G25P[6] from straw-colored fruit bat (Eidolon helvum) in Africa, extending the host spectrum of RVA to bats (Esona et al., 2010). Later on, a novel bat RVA strain RVA/Bat-tc/CHN/MSLH14/2012/G3P[3] was isolated from a lesser horseshoe bat (Rhinolophus hipposideros) in Chinese Yunnan province in 2012, which was closely related genetically to Thai human and India animal RVA strains (He et al., 2013). Further study lead to the isolation of another bat RVA strain RVA/Bat-tc/CHN/MYAS33/2013/G3P[10] from a stoliczka’s trident bat (A. stoliczkanus) in Yunnan, China. The sequences of its RNA segments encoding VP7, VP4 and NSP5 were determined (GenBank accession numbers: KF649186–KF649188), and analysis based on VP7 and VP4 indicated that MYAS33 possessed the rare genotype combination G3P[10] (Xia et al., 2013). In the present study the remaining 8 segments of MYAS33 (GenBank accession numbers: KJ020887–KJ020894) were obtained. To further understand the genetic relationship of MYA S33 with RVA representatives of other hosts species, all 11 segments of MYAS33 were used for genotyping and phylogenetic analyses using previously described methods (He et al., 2013). Results showed that MYAS33 possessed the genotype constellation G3-P[10]-I8-R3-C3-M3-A9-N3-T3-E3-H6 and shared the same genotype constellation with bat RVA strain MSLH14 except for
http://dx.doi.org/10.1016/j.meegid.2014.09.005 1567-1348/Ó 2014 Published by Elsevier B.V.
VP4 (strain MYAS33 contained P[10] instead P[3]) (He et al., 2013), Phylogenetically, MYAS33 and MSLH14 are closely related to each other for the VP3, NSP1, NSP2 and NSP5 gene segments (94–97%). Despite belonging to the same genotype, gene segments VP7, VP6, VP1, VP2, NSP3 and NSP4 (84–92%), were more distantly related (Figs. 1 and 2). Interestingly strain MYAS33 had 9 out of 11 genotypes in common (except for VP4 and VP6) with the unusual equine RVA strain E3198. Furthermore, a relatively close phylogenetic relationship between MYAS33 and E3198 was found for VP7, VP1, VP2, NSP1, NSP2 and NSP5 (88–95% nt similarity), whereas the gene segments VP3, NSP3 and NSP4 of MYAS33 and E3198 were phylogenetically more distantly related to each other (87–89% nt similarity). Five gene segments (VP7, VP4, VP6, NSP4 and NSP5) of the unusual human RVA strains CMH079 have been sequenced (Khamrin et al., 2009). Strikingly their 5 respective genotypes (G3, P[10], I8, E3 and H6), were very closely related genetically to those of MYAS33 (89–98%) (Figs. 1 and 2). A similar observation was made for another unusual human RVA strain CMH222, for which only the VP7, VP4, VP6 and NSP4 gene segments had been sequenced (Khamrin et al., 2006). All 4 gene segments of CMH222 belonged to the same Asian bat-like genotype constellation (G3-P[3]-I8-E3), and also phylogenetically clustered together (77–91%). To date, two bat RVA strains had been identified from E. helvum and R. hipposideros in Kenya and China, respectively (Esona et al., 2010; He et al., 2013). In this study another bat RVA strain MYAS33 was identified from an isolate of a stoliczka’s trident bat in China, obtained in 2013. Although the sampling sites of MYAS33 and MSLH14 were 420 km apart, both strains showed a high level of genetic conservation, suggesting that their genotype constellations are typical for bat RVA strains, rather than unusual interspecies transmitted RVA strains from other host species. This further implies that the equine RVA strains E3198 and the human RVA strains CMH079 and CMH222 (possessing an Asian bat-like genotype constellation, distinct from typical human and equine RVA genotype constellations), most likely share a common ancestor with Asian bat RVAs. Of special interest are the RVA VP6 and VP4 genotypes I8 and P[10], respectively. Up to date, the I8 genotype contains only 4 RVA strains, including the two Asian bat RVAs, and the two human bat-like RVA strains CMH079 and CMH222 (Fig. 1), suggesting that this genotype could be inter-host species transmitted in Southeast Asia. Also the P[10] genotype is very rare, and in addition to MYAS33, has only been identified in a few very unusual human strains from India (Fig. 1). The identification of this genotype in bats may indicate that P[10] could be inter-host species transmitted between bats and humans. Furthermore, besides the 3 above mentioned potential examples of interspecies transmission from bats to humans and
2
Correspondence / Infection, Genetics and Evolution 28 (2014) 1–4
Fig. 1. Phylogenetic trees based on the full-length ORF nucleotide sequences of the RVA structural proteins VP7, VP4, VP6, VP1, VP2 and VP3. Filled triangle indicates strain RVA/Bat-tc/CHN/MYAS33/2013/G3P[10]; open triangles indicate bat RVA strains MSLH14 and KE4582; and filled circles indicate strains CMH079, CMH222, and E3198 which are closely related genetically to some genes of Asian bat RVA.
horses, a number of other RVA strains were found to possess multiple gene segments clustering relatively closely with bat RVA strains (MYAS33, MSLH14, KE4852) or the above mentioned potential inter-host species transmitted strains (CMH079, CMH222, E3198), such as RVA/Simian-tc/USA/RRV/1975/G3P[3],
RVA/Cow-wt/IND/RUBV3/200X/G3P[3], RVA/Rhesus-tc/USA/TUCH/ 2002/G3P[24], RVA/Human-tc/JPN/K8/1977/G1P[9], RVA/Rabbittc/CHN/N5/1992/G3P[14], RVA/Human-wt/CHN/L621/2006/G3P [9], RVA/Human-wt/AUS/RCH272/2012/G3P[14] and RVA/ Human-wt/PRY/1709SR/2009/G3P[9] among others (Figs. 1 and
Correspondence / Infection, Genetics and Evolution 28 (2014) 1–4
3
Fig. 2. Phylogenetic trees based on the full-length ORF nucleotide sequences of the RVA non-structural protein NSP1, NSP2, NSP3, NSP4 and NSP5. Filled triangle indicates strain RVA/Bat-tc/CHN/MYAS33/2013/G3P[10]; open triangles indicate bat RVA strains MSLH14 and KE4582; and filled circles indicate strains CMH079, CMH222 and E3198 which are closely related genetically to some genes of Asian bat RVA.
4
Correspondence / Infection, Genetics and Evolution 28 (2014) 1–4
2). Each of these strains, isolated from a variety of host species, is atypical for that particular host species, and may therefore be also examples of bat RVA strains transmitted among host species. However further molecular characterization of bat RVA strains from all over the world will be required to confirm or refute this hypothesis. Acknowledgements The study was supported by NSFC-Yunnan Province Joint Fund (U1036601), National ‘‘973’’ Program (Grant No. 2012CB722501) and National ‘‘863’’ Program (Grant No. 2012AA022006) to C. Tu. References Calisher, C.H., Childs, J.E., Field, H.E., Holmes, K.V., Schountz, T., 2006. Bats: important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 19, 531– 545. Esona, M.D., Mijatovic-Rustempasic, S., Conrardy, C., Tong, S., Kuzmin, I.V., Agwanda, B., Breiman, R.F., Banyai, K., Niezgoda, M., Rupprecht, C.E., Gentsch, J.R., Bowen, M.D., 2010. Reassortant group A rotavirus from straw-colored fruit bat (Eidolon helvum). Emerg. Infect. Dis. 16, 1844–1852. Estes, M.K., Greenberg, H.B., 2013. Rotaviruses. In: Knipe, D.M., Howley, P.M., Cohen, J.I., Griffin, D.E., Lamb, R.A., Martin, M.A., Racaniello, V.R., Roizman, B. (Eds.), Fields Virology. Wolters Kluwer Health/Lippincot, Williams and Wilkins, Philadelphia, pp. 1347–1401. He, B., Yang, F., Yang, W., Zhang, Y., Feng, Y., Zhou, J., Xie, J., Feng, Y., Bao, X., Guo, H., Li, Y., Xia, L., Li, N., Matthijnssens, J., Zhang, H., Tu, C., 2013. Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses. J. Virol. 87, 12357–12366. Khamrin, P., Maneekarn, N., Peerakome, S., Yagyu, F., Okitsu, S., Ushijima, H., 2006. Molecular characterization of a rare G3P[3] human rotavirus reassortant strain reveals evidence for multiple human-animal interspecies transmissions. J. Med. Virol. 78, 986–994. Khamrin, P., Maneekarn, N., Peerakome, S., Malasao, R., Thongprachum, A., Chan-it, W., Mizuguchi, M., Okitsu, S., Ushijima, H., 2009. Molecular characterization of VP4, VP6, VP7, NSP4, and NSP5/6 genes identifies an unusual G3P[10] human rotavirus strain. J. Med. Virol. 81, 176–182. Luis, A.D., Hayman, D.T., O’Shea, T.J., Cryan, P.M., Gilbert, A.T., Pulliam, J.R., Mills, J.N., Timonin, M.E., Willis, C.K., Cunningham, A.A., Fooks, A.R., Rupprecht, C.E., Wood, J.L., Webb, C.T., 2013. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc. Biol. Sci. 280, 20122753. Matthijnssens, J., Ciarlet, M., Heiman, E., Arijs, I., Delbeke, T., McDonald, S.M., Palombo, E.A., Iturriza-Gomara, M., Maes, P., Patton, J.T., Rahman, M., Van Ranst, M., 2008. Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1like and bovine rotavirus strains. J. Virol. 82, 3204–3219. Matthijnssens, J., Taraporewala, Z.F., Yang, H., Rao, S., Yuan, L., Cao, D., Haoshino, Y., Mertens, P.P.C., Carner, G.R., Mcneal, M., Sestak, K., Van Ranst, M., Patton, J.T., 2010. Simian rotaviruses possess divergent gene constellations that originated from interspecies transmission and reassortment. J. Virol. 84, 2013–2026. Mino, S., Matthijnssens, J., Badaracco, A., Garaicoechea, L., Zeller, M., Heylen, E., Van Ranst, M., Barrandeguy, M., Parreno, V., 2013. Equine G3P[3] rotavirus strain E3198 related to simian RRV and feline/canine- like rotaviruses based on complete genome analyses. Vet. Microbiol. 161, 239–246.
Xia, L., He, B., Hu, T., Zhang, W., Wang, Y., Xu, L., Li, N., Qiu, W., Yu, J., Fan, Q., Zhang, F., Tu, C., 2013. Isolation and characterization of rotavirus from bat. Chin. J. Virol. 29 (6), 632–637.
Lele Xia 1 College of Animal Science and Technology, Jilin Agricultural University, Changchun, China Institute of Military Veterinary, Academy of Military Medical Sciences, Changchun, China Quanshui Fan 1 Center for Disease Control and Prevention of Chengdu Military Region, Kunming, China Biao He 1 Lin Xu Institute of Military Veterinary, Academy of Military Medical Sciences, Changchun, China Fuqiang Zhang Tingsong Hu Yiyin Wang Center for Disease Control and Prevention of Chengdu Military Region, Kunming, China Nan Li Institute of Military Veterinary, Academy of Military Medical Sciences, Changchun, China Wei Qiu Ying Zheng Center for Disease Control and Prevention of Chengdu Military Region, Kunming, China Jelle Matthijnssens Laboratory of Clinical and Epidemiological Virology, Department of Microbiology and Immunology, Rega Institute for Medical Research, University of Leuven, Leuven, Belgium Changchun Tu College of Animal Science and Technology, Jilin Agricultural University, Changchun, China Institute of Military Veterinary, Academy of Military Medical Sciences, Changchun, China Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu Province, China Corresponding author. Address: Institute of Military Veterinary, Academy of Military Medical Sciences, 666 Liuying West Road, Jingyue Economic Development Zone, Changchun 130122, China. Tel./fax: +86 431 81032202. E-mail address: [email protected] Available online 9 September 2014
1
These authors contributed equally to this work.
Contents lists available at ScienceDirect
Infection, Genetics and Evolution journal homepage: www.elsevier.com/locate/meegid
Correspondence The complete genome sequence of a G3P[10] Chinese bat rotavirus suggests multiple bat rotavirus inter-host species transmission events
Dear Editor, Species A rotavirus (RVA) can cause significant diarrhea in the young of various mammalian and avian species (Estes and Greenberg, 2013). RVA possesses 11 segments of double strand RNA (dsRNA) expressing six structural proteins (VP1–VP4, VP6, and VP7) and five or six non-structural proteins (NSP1–NSP5 and sometimes NSP6) (Estes and Greenberg, 2013). A uniform classification system exists for each of the 11 RVA gene segments (VP7, VP4, VP6, VP1-VP3, NSP1-NSP5) defining G-, P-, I- R-, C-, M-, A-, N-, T-, E- and H-genotypes, respectively (Matthijnssens et al., 2008). Despite this seemingly close host range restriction, RVA strains are known to frequently cross the host species barrier, resulting in the detection of RVA strains unusual to that host species (Matthijnssens et al., 2010; Mino et al., 2013; Khamrin et al., 2009). Often, but not always, such inter-host species transmissions are dead-end infections. Bats are important viral reservoirs and more than 130 viruses have been found in bats with many being highly pathogenic for humans, such as Ebola virus, Nipah virus, Hendra virus and Lyssavirus (Calisher et al., 2006; Luis et al., 2013). Esona et al. reported the first bat RVA strain RVA/Bat-wt/KEN/KE4852/2007/G25P[6] from straw-colored fruit bat (Eidolon helvum) in Africa, extending the host spectrum of RVA to bats (Esona et al., 2010). Later on, a novel bat RVA strain RVA/Bat-tc/CHN/MSLH14/2012/G3P[3] was isolated from a lesser horseshoe bat (Rhinolophus hipposideros) in Chinese Yunnan province in 2012, which was closely related genetically to Thai human and India animal RVA strains (He et al., 2013). Further study lead to the isolation of another bat RVA strain RVA/Bat-tc/CHN/MYAS33/2013/G3P[10] from a stoliczka’s trident bat (A. stoliczkanus) in Yunnan, China. The sequences of its RNA segments encoding VP7, VP4 and NSP5 were determined (GenBank accession numbers: KF649186–KF649188), and analysis based on VP7 and VP4 indicated that MYAS33 possessed the rare genotype combination G3P[10] (Xia et al., 2013). In the present study the remaining 8 segments of MYAS33 (GenBank accession numbers: KJ020887–KJ020894) were obtained. To further understand the genetic relationship of MYA S33 with RVA representatives of other hosts species, all 11 segments of MYAS33 were used for genotyping and phylogenetic analyses using previously described methods (He et al., 2013). Results showed that MYAS33 possessed the genotype constellation G3-P[10]-I8-R3-C3-M3-A9-N3-T3-E3-H6 and shared the same genotype constellation with bat RVA strain MSLH14 except for
http://dx.doi.org/10.1016/j.meegid.2014.09.005 1567-1348/Ó 2014 Published by Elsevier B.V.
VP4 (strain MYAS33 contained P[10] instead P[3]) (He et al., 2013), Phylogenetically, MYAS33 and MSLH14 are closely related to each other for the VP3, NSP1, NSP2 and NSP5 gene segments (94–97%). Despite belonging to the same genotype, gene segments VP7, VP6, VP1, VP2, NSP3 and NSP4 (84–92%), were more distantly related (Figs. 1 and 2). Interestingly strain MYAS33 had 9 out of 11 genotypes in common (except for VP4 and VP6) with the unusual equine RVA strain E3198. Furthermore, a relatively close phylogenetic relationship between MYAS33 and E3198 was found for VP7, VP1, VP2, NSP1, NSP2 and NSP5 (88–95% nt similarity), whereas the gene segments VP3, NSP3 and NSP4 of MYAS33 and E3198 were phylogenetically more distantly related to each other (87–89% nt similarity). Five gene segments (VP7, VP4, VP6, NSP4 and NSP5) of the unusual human RVA strains CMH079 have been sequenced (Khamrin et al., 2009). Strikingly their 5 respective genotypes (G3, P[10], I8, E3 and H6), were very closely related genetically to those of MYAS33 (89–98%) (Figs. 1 and 2). A similar observation was made for another unusual human RVA strain CMH222, for which only the VP7, VP4, VP6 and NSP4 gene segments had been sequenced (Khamrin et al., 2006). All 4 gene segments of CMH222 belonged to the same Asian bat-like genotype constellation (G3-P[3]-I8-E3), and also phylogenetically clustered together (77–91%). To date, two bat RVA strains had been identified from E. helvum and R. hipposideros in Kenya and China, respectively (Esona et al., 2010; He et al., 2013). In this study another bat RVA strain MYAS33 was identified from an isolate of a stoliczka’s trident bat in China, obtained in 2013. Although the sampling sites of MYAS33 and MSLH14 were 420 km apart, both strains showed a high level of genetic conservation, suggesting that their genotype constellations are typical for bat RVA strains, rather than unusual interspecies transmitted RVA strains from other host species. This further implies that the equine RVA strains E3198 and the human RVA strains CMH079 and CMH222 (possessing an Asian bat-like genotype constellation, distinct from typical human and equine RVA genotype constellations), most likely share a common ancestor with Asian bat RVAs. Of special interest are the RVA VP6 and VP4 genotypes I8 and P[10], respectively. Up to date, the I8 genotype contains only 4 RVA strains, including the two Asian bat RVAs, and the two human bat-like RVA strains CMH079 and CMH222 (Fig. 1), suggesting that this genotype could be inter-host species transmitted in Southeast Asia. Also the P[10] genotype is very rare, and in addition to MYAS33, has only been identified in a few very unusual human strains from India (Fig. 1). The identification of this genotype in bats may indicate that P[10] could be inter-host species transmitted between bats and humans. Furthermore, besides the 3 above mentioned potential examples of interspecies transmission from bats to humans and
2
Correspondence / Infection, Genetics and Evolution 28 (2014) 1–4
Fig. 1. Phylogenetic trees based on the full-length ORF nucleotide sequences of the RVA structural proteins VP7, VP4, VP6, VP1, VP2 and VP3. Filled triangle indicates strain RVA/Bat-tc/CHN/MYAS33/2013/G3P[10]; open triangles indicate bat RVA strains MSLH14 and KE4582; and filled circles indicate strains CMH079, CMH222, and E3198 which are closely related genetically to some genes of Asian bat RVA.
horses, a number of other RVA strains were found to possess multiple gene segments clustering relatively closely with bat RVA strains (MYAS33, MSLH14, KE4852) or the above mentioned potential inter-host species transmitted strains (CMH079, CMH222, E3198), such as RVA/Simian-tc/USA/RRV/1975/G3P[3],
RVA/Cow-wt/IND/RUBV3/200X/G3P[3], RVA/Rhesus-tc/USA/TUCH/ 2002/G3P[24], RVA/Human-tc/JPN/K8/1977/G1P[9], RVA/Rabbittc/CHN/N5/1992/G3P[14], RVA/Human-wt/CHN/L621/2006/G3P [9], RVA/Human-wt/AUS/RCH272/2012/G3P[14] and RVA/ Human-wt/PRY/1709SR/2009/G3P[9] among others (Figs. 1 and
Correspondence / Infection, Genetics and Evolution 28 (2014) 1–4
3
Fig. 2. Phylogenetic trees based on the full-length ORF nucleotide sequences of the RVA non-structural protein NSP1, NSP2, NSP3, NSP4 and NSP5. Filled triangle indicates strain RVA/Bat-tc/CHN/MYAS33/2013/G3P[10]; open triangles indicate bat RVA strains MSLH14 and KE4582; and filled circles indicate strains CMH079, CMH222 and E3198 which are closely related genetically to some genes of Asian bat RVA.
4
Correspondence / Infection, Genetics and Evolution 28 (2014) 1–4
2). Each of these strains, isolated from a variety of host species, is atypical for that particular host species, and may therefore be also examples of bat RVA strains transmitted among host species. However further molecular characterization of bat RVA strains from all over the world will be required to confirm or refute this hypothesis. Acknowledgements The study was supported by NSFC-Yunnan Province Joint Fund (U1036601), National ‘‘973’’ Program (Grant No. 2012CB722501) and National ‘‘863’’ Program (Grant No. 2012AA022006) to C. Tu. References Calisher, C.H., Childs, J.E., Field, H.E., Holmes, K.V., Schountz, T., 2006. Bats: important reservoir hosts of emerging viruses. Clin. Microbiol. Rev. 19, 531– 545. Esona, M.D., Mijatovic-Rustempasic, S., Conrardy, C., Tong, S., Kuzmin, I.V., Agwanda, B., Breiman, R.F., Banyai, K., Niezgoda, M., Rupprecht, C.E., Gentsch, J.R., Bowen, M.D., 2010. Reassortant group A rotavirus from straw-colored fruit bat (Eidolon helvum). Emerg. Infect. Dis. 16, 1844–1852. Estes, M.K., Greenberg, H.B., 2013. Rotaviruses. In: Knipe, D.M., Howley, P.M., Cohen, J.I., Griffin, D.E., Lamb, R.A., Martin, M.A., Racaniello, V.R., Roizman, B. (Eds.), Fields Virology. Wolters Kluwer Health/Lippincot, Williams and Wilkins, Philadelphia, pp. 1347–1401. He, B., Yang, F., Yang, W., Zhang, Y., Feng, Y., Zhou, J., Xie, J., Feng, Y., Bao, X., Guo, H., Li, Y., Xia, L., Li, N., Matthijnssens, J., Zhang, H., Tu, C., 2013. Characterization of a novel G3P[3] rotavirus isolated from a lesser horseshoe bat: a distant relative of feline/canine rotaviruses. J. Virol. 87, 12357–12366. Khamrin, P., Maneekarn, N., Peerakome, S., Yagyu, F., Okitsu, S., Ushijima, H., 2006. Molecular characterization of a rare G3P[3] human rotavirus reassortant strain reveals evidence for multiple human-animal interspecies transmissions. J. Med. Virol. 78, 986–994. Khamrin, P., Maneekarn, N., Peerakome, S., Malasao, R., Thongprachum, A., Chan-it, W., Mizuguchi, M., Okitsu, S., Ushijima, H., 2009. Molecular characterization of VP4, VP6, VP7, NSP4, and NSP5/6 genes identifies an unusual G3P[10] human rotavirus strain. J. Med. Virol. 81, 176–182. Luis, A.D., Hayman, D.T., O’Shea, T.J., Cryan, P.M., Gilbert, A.T., Pulliam, J.R., Mills, J.N., Timonin, M.E., Willis, C.K., Cunningham, A.A., Fooks, A.R., Rupprecht, C.E., Wood, J.L., Webb, C.T., 2013. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc. Biol. Sci. 280, 20122753. Matthijnssens, J., Ciarlet, M., Heiman, E., Arijs, I., Delbeke, T., McDonald, S.M., Palombo, E.A., Iturriza-Gomara, M., Maes, P., Patton, J.T., Rahman, M., Van Ranst, M., 2008. Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1like and bovine rotavirus strains. J. Virol. 82, 3204–3219. Matthijnssens, J., Taraporewala, Z.F., Yang, H., Rao, S., Yuan, L., Cao, D., Haoshino, Y., Mertens, P.P.C., Carner, G.R., Mcneal, M., Sestak, K., Van Ranst, M., Patton, J.T., 2010. Simian rotaviruses possess divergent gene constellations that originated from interspecies transmission and reassortment. J. Virol. 84, 2013–2026. Mino, S., Matthijnssens, J., Badaracco, A., Garaicoechea, L., Zeller, M., Heylen, E., Van Ranst, M., Barrandeguy, M., Parreno, V., 2013. Equine G3P[3] rotavirus strain E3198 related to simian RRV and feline/canine- like rotaviruses based on complete genome analyses. Vet. Microbiol. 161, 239–246.
Xia, L., He, B., Hu, T., Zhang, W., Wang, Y., Xu, L., Li, N., Qiu, W., Yu, J., Fan, Q., Zhang, F., Tu, C., 2013. Isolation and characterization of rotavirus from bat. Chin. J. Virol. 29 (6), 632–637.
Lele Xia 1 College of Animal Science and Technology, Jilin Agricultural University, Changchun, China Institute of Military Veterinary, Academy of Military Medical Sciences, Changchun, China Quanshui Fan 1 Center for Disease Control and Prevention of Chengdu Military Region, Kunming, China Biao He 1 Lin Xu Institute of Military Veterinary, Academy of Military Medical Sciences, Changchun, China Fuqiang Zhang Tingsong Hu Yiyin Wang Center for Disease Control and Prevention of Chengdu Military Region, Kunming, China Nan Li Institute of Military Veterinary, Academy of Military Medical Sciences, Changchun, China Wei Qiu Ying Zheng Center for Disease Control and Prevention of Chengdu Military Region, Kunming, China Jelle Matthijnssens Laboratory of Clinical and Epidemiological Virology, Department of Microbiology and Immunology, Rega Institute for Medical Research, University of Leuven, Leuven, Belgium Changchun Tu College of Animal Science and Technology, Jilin Agricultural University, Changchun, China Institute of Military Veterinary, Academy of Military Medical Sciences, Changchun, China Jiangsu Co-innovation Center for Prevention and Control of Important Animal Infectious Diseases and Zoonoses, Yangzhou, Jiangsu Province, China Corresponding author. Address: Institute of Military Veterinary, Academy of Military Medical Sciences, 666 Liuying West Road, Jingyue Economic Development Zone, Changchun 130122, China. Tel./fax: +86 431 81032202. E-mail address: [email protected] Available online 9 September 2014
1
These authors contributed equally to this work.