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. 2016 Apr 28;59(6):604–614. doi: 10.1007/s11427-016-5039-0

Genetic diversity of coronaviruses in Miniopterus fuliginosus bats

Jiang Du 1, Li Yang 1, Xianwen Ren 1, Junpeng Zhang 4, Jie Dong 1, Lilian Sun 1, Yafang Zhu 1, Fan Yang 1, Shuyi Zhang 3, Zhiqiang Wu 1,✉, Qi Jin 1,2,✉
PMCID: PMC7089092  PMID: 27125516

Abstract

Coronaviruses, such as severe acute respiratory syndrome coronavirus and Middle East respiratory syndrome coronavirus, pose significant public health threats. Bats have been suggested to act as natural reservoirs for both these viruses, and periodic monitoring of coronaviruses in bats may thus provide important clues about emergent infectious viruses. The Eastern bent-wing bat Miniopterus fuliginosus is distributed extensively throughout China. We therefore analyzed the genetic diversity of coronaviruses in samples of M. fuliginosus collected from nine Chinese provinces during 2011–2013. The only coronavirus genus found was Alphacoronavirus. We established six complete and five partial genomic sequences of alphacoronaviruses, which revealed that they could be divided into two distinct lineages, with close relationships to coronaviruses in Miniopterus magnater and Miniopterus pusillus. Recombination was confirmed by detecting putative breakpoints of Lineage 1 coronaviruses in M. fuliginosus and M. pusillus (Wu et al., 2015), which supported the results of topological and phylogenetic analyses. The established alphacoronavirus genome sequences showed high similarity to other alphacoronaviruses found in other Miniopterus species, suggesting that their transmission in different Miniopterus species may provide opportunities for recombination with different alphacoronaviruses. The genetic information for these novel alphacoronaviruses will improve our understanding of the evolution and genetic diversity of coronaviruses, with potentially important implications for the transmission of human diseases.

Keywords: coronavirus, Miniopterus fuliginosus, bat, co-infection, recombination

Footnotes

This article is published with open access at link.springer.com

Contributor Information

Zhiqiang Wu, Email: wuzq2009@ipbcams.ac.cn.

Qi Jin, Email: zdsys@vip.sina.com.

References

  1. Apweiler R., Attwood T.K., Bairoch A., Bateman A., Birney E., Biswas M., Bucher P., Cerutti L., Corpet F., Croning M.D., Durbin R., Falquet L., Fleischmann W., Gouzy J., Hermjakob H., Hulo N., Jonassen I., Kahn D., Kanapin A., Karavidopoulou Y., Lopez R., Marx B., Mulder N.J., Oinn T.M., Pagni M., Servant F., Sigrist C.J., Zdobnov E.M. The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res. 2001;29:37–40. doi: 10.1093/nar/29.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bateman A., Birney E., Cerruti L., Durbin R., Etwiller L., Eddy S.R., Griffiths-Jones S., Howe K.L., Marshall M., Sonnhammer E.L. The Pfam protein families database. Nucleic Acids Res. 2002;30:276–280. doi: 10.1093/nar/30.1.276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bosch B.J., van der Zee R., de Haan C.A., Rottier P.J. The coronavirus spike protein is a class I virus fusion protein: structural and functional characterization of the fusion core complex. J Virol. 2003;77:8801–8811. doi: 10.1128/JVI.77.16.8801-8811.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chen L.L., Ou H.Y., Zhang R., Zhang C.T. ZCURVE_CoV: a new system to recognize protein coding genes in coronavirus genomes, and its applications in analyzing SARS-CoV genomes. Biochem Biophys Res Commun. 2003;307:382–388. doi: 10.1016/S0006-291X(03)01192-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chu D.K., Peiris J.S., Chen H., Guan Y., Poon L.L. Genomic characterizations of bat coronaviruses (1A, 1B and HKU8) and evidence for co-infections in Miniopterus bats. J Gen Virol. 2008;89:1282–1287. doi: 10.1099/vir.0.83605-0. [DOI] [PubMed] [Google Scholar]
  6. Cui J., Han N., Streicker D., Li G., Tang X., Shi Z., Hu Z., Zhao G., Fontanet A., Guan Y., Wang L., Jones G., Field H.E., Daszak P., Zhang S. Evolutionary relationships between bat coronaviruses and their hosts. Emerg Infect Dis. 2007;13:1526–1532. doi: 10.3201/eid1310.070448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. King A.M.Q., Adams M.J., Carstens E.B. Ninth Report of the International Committee on Taxonomy of Viruses, International Union of Microbiological Societies, Virology Division. London: Elsevier Academic Press; 2011. Virus Taxonomy, Classification and Nomenclature of Viruses; pp. 806–828. [Google Scholar]
  8. Dveksler G.S., Pensiero M.N., Cardellichio C.B., Williams R.K., Jiang G.S., Holmes K.V., Dieffenbach C.W. Cloning of the mouse hepatitis virus (MHV) receptor: expression in humaaan and hamster cell lines confers susceptibility to MHV. J Virol. 1991;65:6881–6891. doi: 10.1128/jvi.65.12.6881-6891.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gonzalez J.M., Gomez-Puertas P., Cavanagh D., Gorbalenya A.E., Enjuanes L. A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch Virol. 2003;148:2207–2235. doi: 10.1007/s00705-003-0162-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Graham R.L., Baric R.S. Recombination, reservoirs, and the modular spike: mechanisms of coronavirus cross-species transmission. J Virol. 2010;84:3134–3146. doi: 10.1128/JVI.01394-09. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. [DOI] [PubMed] [Google Scholar]
  12. Herrewegh A.A., Smeenk I., Horzinek M.C., Rottier P.J., de Groot R.J. Feline coronavirus type IIstrains 79-1683 and 79-1146 originate from a double recombination between feline coronavirus type I and canine coronavirus. J Virol. 1998;72:4508–4514. doi: 10.1128/jvi.72.5.4508-4514.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Holmes K.V., Enjuanes L. Virology. The SARS coronavirus: a postgenomic era. Science. 2003;300:1377–1378. doi: 10.1126/science.1086418. [DOI] [PubMed] [Google Scholar]
  14. Jonassen C.M., Kofstad T., Larsen I.L., Lovland A., Handeland K., Follestad A., Lillehaug A. Molecular identification and characterization of novel coronaviruses infecting graylag geese (Anser anser), feral pigeons (Columbia livia) and mallards (Anas platyrhynchos) J Gen Virol. 2005;86:1597–1607. doi: 10.1099/vir.0.80927-0. [DOI] [PubMed] [Google Scholar]
  15. Kosakovsky Pond S.L., Posada D., Gravenor M.B., Woelk C.H., Frost S.D. GARD: a genetic algorithm for recombination detection. Bioinformatics. 2006;22:3096–3098. doi: 10.1093/bioinformatics/btl474. [DOI] [PubMed] [Google Scholar]
  16. Lai M.M. Coronavirus: organization, replication and expression of genome. Annu Rev Microbiol. 1990;44:303–333. doi: 10.1146/annurev.mi.44.100190.001511. [DOI] [PubMed] [Google Scholar]
  17. Lai M.M., Cavanagh D. The molecular biology of coronaviruses. Adv Virus Res. 1997;48:1–100. doi: 10.1016/S0065-3527(08)60286-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lai M.M.C., Holmes K.V. Coronaviruses. In: Knipe D.M., Howley P.M., Griffin D.E., Lamb R.A., Martin M.A., Roizman B., Straus S.E., editors. Fields Virology. Philadelphia: Lippincott Williams & Wilkins; 2001. pp. 1163–1185. [Google Scholar]
  19. Lau S.K., Li K.S., Tsang A.K., Shek C.T., Wang M., Choi G.K., Guo R., Wong B.H., Poon R.W., Lam C.S., Wang S.Y., Fan R.Y., Chan K.H., Zheng B.J., Woo P.C., Yuen K.Y. Recent trans mission of a novel alphacoronavirus, bat coronavirus HKU10, from Leschenault’s rousettes to pomona leaf-nosed bats: first evidence of interspecies transmission of coronavirus between bats of different suborders. J Virol. 2012;86:11906–11918. doi: 10.1128/JVI.01305-12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lau S.K., Woo P.C., Li K.S., Huang Y., Tsoi H.W., Wong B.H., Wong S.S., Leung S.Y., Chan K.H., Yuen K.Y. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci USA. 2005;102:14040–14045. doi: 10.1073/pnas.0506735102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lau S.K., Woo P.C., Li K.S., Huang Y., Wang M., Lam C.S., Xu H., Guo R., Chan K.H., Zheng B.J., Yuen K.Y. 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. 2007;367:428–439. doi: 10.1016/j.virol.2007.06.009. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lau S.K., Woo P.C., Yip C.C., Fan R.Y., Huang Y., Wang M., Guo R., Lam C.S., Tsang A.K., Lai K.K., Chan K.H., Che X.Y., Zheng B.J., Yuen K.Y. Isolation and characterization of a novel Betacoronavirus subgroup A coronavirus, rabbit coronavirus HKU14, from domestic rabbits. J Virol. 2012;86:5481–5496. doi: 10.1128/JVI.06927-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J.H., Wang H., Crameri G., Hu Z., Zhang H., Zhang J., McEachern J., Field H., Daszak P., Eaton B.T., Zhang S., Wang L.F. Bats are natural reservoirs of SARS-like coronaviruses. Science. 2005;310:676–679. doi: 10.1126/science.1118391. [DOI] [PubMed] [Google Scholar]
  24. Liu S., Chen J., Kong X., Shao Y., Han Z., Feng L., Cai X., Gu S., Liu M. Isolation of avian infectious bronchitis coronavirus from domestic peafowl (Pavo cristatus) and teal (Anas) J Gen Virol. 2005;86:719–725. doi: 10.1099/vir.0.80546-0. [DOI] [PubMed] [Google Scholar]
  25. Makino S., Keck J.G., Stohlman S.A., Lai M.M. High-frequency RNA recombination of murine coronaviruses. J Virol. 1986;57:729–737. doi: 10.1128/jvi.57.3.729-737.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miller-Butterworth C.M., Jacobs D.S., Harley E.H. Strong population substructure is correlated with morphology and ecology in a migratory bat. Nature. 2003;424:187–191. doi: 10.1038/nature01742. [DOI] [PubMed] [Google Scholar]
  27. Rest J.S., Mindell D.P. SARS associated coronavirus has a recombinant polymerase and coronaviruses have a history of host-shifting. Infect Genet Evol. 2003;3:219–225. doi: 10.1016/j.meegid.2003.08.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shirato K., Maeda K., Tsuda S., Suzuki K., Watanabe S., Shimoda H., Ueda N., Iha K., Taniguchi S., Kyuwa S., Endoh D., Matsuyama S., Kurane I., Saijo M., Morikawa S., Yoshikawa Y., Akashi H., Mizutani T. Detection of bat coronaviruses from Miniopterus fuliginosus in Japan. Virus Genes. 2012;44:40–44. doi: 10.1007/s11262-011-0661-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Song H.D., Tu C.C., Zhang G.W., Wang S.Y., Zheng K., Lei L.C., Chen Q.X., Gao Y.W., Zhou H.Q., Xiang H., Zheng H.J., Chern S.W., Cheng F., Pan C.M., Xuan H., Chen S.J., Luo H.M., Zhou D.H., Liu Y.F., He J.F., Qin P.Z., Li L.H., Ren Y.Q., Liang W.J., Yu Y.D., Anderson L., Wang M., Xu R.H., Wu X.W., Zheng H.Y., Chen J.D., Liang G., Gao Y., Liao M., Fang L., Jiang L.Y., Li H., Chen F., Di B., He L.J., Lin J.Y., Tong S., Kong X., Du L., Hao P., Tang H., Bernini A., Yu X.J., Spiga O., Guo Z.M., Pan H.Y., He W.Z., Manuguerra J.C., Fontanet A., Danchin A., Niccolai N., Li Y.X., Wu C.I., Zhao G.P. Cross-host evolution of severe acute respiratory syndrome coronavirus in palm civet and human. Proc Natl Acad Sci USA. 2005;102:2430–2435. doi: 10.1073/pnas.0409608102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sonnhammer E.L., von Heijne G., Krogh A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol. 1998;6:175–182. [PubMed] [Google Scholar]
  31. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–2739. doi: 10.1093/molbev/msr121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tang X.C., Zhang J.X., Zhang S.Y., Wang P., Fan X.H., Li L.F., Li G., Dong B.Q., Liu W., Cheung C.L., Xu K.M., Song W.J., Vijaykrishna D., Poon L.L., Peiris J.S., Smith G.J., Chen H., Guan Y. Prevalence and genetic diversity of coronaviruses in bats from China. J Virol. 2006;80:7481–7490. doi: 10.1128/JVI.00697-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. van Boheemen S., de Graaf M., Lauber C., Bestebroer T.M., Raj V.S., Zaki A.M., Osterhaus A.D., Haagmans B.L., Gorbalenya A.E., Snijder E.J., Fouchier R.A. MBio. 2012. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Vijaykrishna D., Smith G.J., Zhang J.X., Peiris J.S., Chen H., Guan Y. Evolutionary insights into the ecology of coronaviruses. J Virol. 2007;81:4012–4020. doi: 10.1128/JVI.02605-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weiss S.R., Navas-Martin S. Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol Mol Biol Rev. 2005;69:635–664. doi: 10.1128/MMBR.69.4.635-664.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Woo P.C., Lau S.K., Lam C.S., Lai K.K., Huang Y., Lee P., Luk G.S., Dyrting K.C., Chan K.H., Yuen K.Y. Comparative analysis of complete genome sequences of three avian coronaviruses reveals a novel group 3c coronavirus. J Virol. 2009;83:908–917. doi: 10.1128/JVI.01977-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Woo P.C., Lau S.K., Lam C.S., Lau C.C., Tsang A.K., Lau J.H., Bai R., Teng J.L., Tsang C.C., Wang M., Zheng B.J., Chan K.H., Yuen K.Y. Discovery of seven novel Mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus. J Virol. 2012;86:3995–4008. doi: 10.1128/JVI.06540-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Woo P.C., Lau S.K., Li K.S., Poon R.W., Wong B.H., Tsoi H.W., Yip B.C., Huang Y., Chan K.H., Yuen K.Y. Molecular diversity of coronaviruses in bats. Virology. 2006;351:180–187. doi: 10.1016/j.virol.2006.02.041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Woo P.C., Lau S.K., Yip C.C., Huang Y., Tsoi H.W., Chan K.H., Yuen K.Y. Comparative analysis of 22 coronavirus HKU1 genomes reveals a novel genotype and evidence of natural recombination in coronavirus HKU1. J Virol. 2006;80:7136–7145. doi: 10.1128/JVI.00509-06. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Woo P.C., Lau S.K., Yuen K.Y. Infectious diseases emerging from Chinese wet-markets: zoonotic origins of severe respiratory viral infections. Curr Opin Infect Dis. 2006;19:401–407. doi: 10.1097/01.qco.0000244043.08264.fc. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Woo P.C., Lau S.K., Huang Y., Yuen K.Y. Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med. 2009;234:1117–1127. doi: 10.3181/0903-MR-94. [DOI] [PubMed] [Google Scholar]
  42. Woo P.C., Lau S.K., Yuen K.Y. Infectious diseases emerging from Chinese wet-markets: zoonotic origins of severe respiratory viral infections. Curr Opin Infect Dis. 2006;19:401–407. doi: 10.1097/01.qco.0000244043.08264.fc. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wu Z., Yang L., Ren X., He G., Zhang J., Yang J., Qian Z., Dong J., Sun L., Zhu Y., Du J., Yang F., Zhang S., Jin Q. Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases. ISME J. 2015;10:609–620. doi: 10.1038/ismej.2015.138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Zeng Q., Langereis M.A., van Vliet A.L., Huizinga E.G., de Groot R.J. Structure of coronavirus hemagglutinin-esterase offers insight into corona and influenza virus evolution. Proc Natl Acad Sci USA. 2008;105:9065–9069. doi: 10.1073/pnas.0800502105. [DOI] [PMC free article] [PubMed] [Google Scholar]

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