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Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft
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  • Research Article
  • Published: 18 February 2016

Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft

  • Xing-Yi Ge1,
  • Ning Wang1,
  • Wei Zhang1,
  • Ben Hu1,
  • Bei Li1,
  • Yun-Zhi Zhang2,3,
  • Ji-Hua Zhou2,
  • Chu-Ming Luo1,
  • Xing-Lou Yang1,
  • Li-Jun Wu1,
  • Bo Wang1,
  • Yun Zhang4,
  • Zong-Xiao Li4 &
  • …
  • Zheng-Li Shi1 

Virologica Sinica volume 31, pages 31–40 (2016)Cite this article

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Abstract

Since the 2002–2003 severe acute respiratory syndrome (SARS) outbreak prompted a search for the natural reservoir of the SARS coronavirus, numerous alpha- and betacoronaviruses have been discovered in bats around the world. Bats are likely the natural reservoir of alpha- and betacoronaviruses, and due to the rich diversity and global distribution of bats, the number of bat coronaviruses will likely increase. We conducted a surveillance of coronaviruses in bats in an abandoned mineshaft in Mojiang County, Yunnan Province, China, from 2012–2013. Six bat species were frequently detected in the cave: Rhinolophus sinicus, Rhinolophus affinis, Hipposideros pomona, Miniopterus schreibersii, Miniopterus fuliginosus, and Miniopterus fuscus. By sequencing PCR products of the coronavirus RNA-dependent RNA polymerase gene (RdRp), we found a high frequency of infection by a diverse group of coronaviruses in different bat species in the mineshaft. Sequenced partial RdRp fragments had 80%–99% nucleic acid sequence identity with well-characterized Alphacoronavirus species, including BtCoV HKU2, BtCoV HKU8, and BtCoV1, and unassigned species BtCoV HKU7 and BtCoV HKU10. Additionally, the surveillance identified two unclassified betacoronaviruses, one new strain of SARS-like coronavirus, and one potentially new betacoronavirus species. Furthermore, coronavirus co-infection was detected in all six bat species, a phenomenon that fosters recombination and promotes the emergence of novel virus strains. Our findings highlight the importance of bats as natural reservoirs of coronaviruses and the potentially zoonotic source of viral pathogens.

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References

  • Anthony SJ, Ojeda-Flores R, Rico-Chavez O, Navarrete-Macias I, Zambrana-Torrelio CM, Rostal MK, Epstein JH, Tipps T, Liang E, Sanchez-Leon M, Sotomayor-Bonilla J, Aguirre AA, Avila-Flores R, Medellin RA, Goldstein T, Suzan G, Daszak P, Lipkin WI. 2013. Coronaviruses in bats from Mexico. J Gen Virol, 94: 1028–1038.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baker ML, Schountz T, Wang LF. 2013. Antiviral immune responses of bats: a review. Zoonoses Public Health, 60: 104–116.

    Article  CAS  PubMed  Google Scholar 

  • Bruckova M, McIntosh K, Kapikian AZ, Chanock RM. 1970. The adaptation of two human coronavirus strains (OC38 and OC43) to growth in cell monolayers. Proc Soc Exp Biol Med, 135: 431–435.

    Article  CAS  PubMed  Google Scholar 

  • Cavanagh D, Britton P. 2012. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Family Coronaviridae. In: International Committee on Taxonomy of Viruses. Andrew M.Q. King MJA, Eric B. Carstens, and Elliot J. Lefkowitz (eds). Cambridge: Academic Press Elsevier, pp. 770–792.

    Google Scholar 

  • Chu DK, Peiris JS, Chen H, Guan Y, Poon LL. 2008. Genomic characterizations of bat coronaviruses (1A, 1B and HKU8) and evidence for co-infections in Miniopterus bats. J Gen Virol, 89: 1282–1287.

    Article  CAS  PubMed  Google Scholar 

  • Chu DK, Poon LL, Chan KH, Chen H, Guan Y, Yuen KY, Peiris JS. 2006. Coronaviruses in bent-winged bats (Miniopterus spp.). J Gen Virol, 87: 2461–2466.

    Article  CAS  PubMed  Google Scholar 

  • Corman VM, Ithete NL, Richards LR, Schoeman MC, Preiser W, Drosten C, Drexler JF. 2014. Rooting the phylogenetic tree of Middle East respiratory syndrome coronavirus by characterization of a conspecific virus from an African bat. J Virol, 88: 11297–11303.

    Article  PubMed Central  PubMed  Google Scholar 

  • De Benedictis P, Marciano S, Scaravelli D, Priori P, Zecchin B, Capua I, Monne I, Cattoli G. 2013. Alpha and lineage C beta-CoV infections in Italian bats. Virus Genes, 48: 366–371.

    Article  PubMed  Google Scholar 

  • de Souza Luna LK, Heiser V, Regamey N, Panning M, Drexler JF, Mulangu S, Poon L, Baumgarte S, Haijema BJ, Kaiser L, Drosten C. 2007. Generic detection of coronaviruses and differentiation at the prototype strain level by reverse transcription-PCR and nonfluorescent low-density microarray. J Clin Microbiol, 45: 1049–1052.

    Article  PubMed Central  PubMed  Google Scholar 

  • Drexler JF, Corman VM, Wegner T, Tateno AF, Zerbinati RM, Gloza-Rausch F, Seebens A, Muller MA, Drosten C. 2011. Amplification of emerging viruses in a bat colony. Emerg Infect Dis, 17: 449–456.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Drexler JF, Gloza-Rausch F, Glende J, Corman VM, Muth D, Goettsche M, Seebens A, Niedrig M, Pfefferle S, Yordanov S, Zhelyazkov L, Hermanns U, Vallo P, Lukashev A, Muller MA, Deng H, Herrler G, Drosten C. 2010. Genomic characterization of severe acute respiratory syndrome-related coronavirus in European bats and classification of coronaviruses based on partial RNA-dependent RNA polymerase gene sequences. J Virol, 84: 11336–11349.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ge XY, Li JL, Yang XL, Chmura AA, Zhu G, Epstein JH, Mazet JK, Hu B, Zhang W, Peng C, Zhang YJ, Luo CM, Tan B, Wang N, Zhu Y, Crameri G, Zhang SY, Wang LF, Daszak P, Shi ZL. 2013. Isolation and characterization of a bat SARS-like coronavirus that uses the ACE2 receptor. Nature, 503: 535–538.

    Article  CAS  PubMed  Google Scholar 

  • Geldenhuys M, Weyer J, Nel LH, Markotter W. 2013. Coronaviruses in South african bats. Vector Borne Zoonotic Dis, 13: 516–519.

    Article  PubMed  Google Scholar 

  • Goes LG, Ruvalcaba SG, Campos AA, Queiroz LH, de Carvalho C, Jerez JA, Durigon EL, Davalos LI, Dominguez SR. 2013. Novel bat coronaviruses, Brazil and Mexico. Emerg Infect Dis, 19: 1711–1713.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gouilh MA, Puechmaille SJ, Gonzalez JP, Teeling E, Kittayapong P, Manuguerra JC. 2011. SARS-Coronavirus ancestor's foot-prints in South-East Asian bat colonies and the refuge theory. Infect Genet Evol, 11: 1690–1702.

    Article  PubMed  Google Scholar 

  • Graham RL, Donaldson EF, Baric RS. 2013. A decade after SARS: strategies for controlling emerging coronaviruses. Nat Rev Microbiol, 11: 836–848.

    Article  CAS  PubMed  Google Scholar 

  • Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser (Oxf), 41: 95–98.

    CAS  Google Scholar 

  • Huelsenbeck JP, Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17: 754–755.

    Article  CAS  PubMed  Google Scholar 

  • Irwin DM, Kocher TD, Wilson AC. 1991. Evolution of the Cytochrome-B Gene of Mammals. J Mol Evol, 32: 128–144.

    Article  CAS  PubMed  Google Scholar 

  • Kusanagi K, Kuwahara H, Katoh T, Nunoya T, Ishikawa Y, Samejima T, Tajima M. 1992. Isolation and serial propagation of porcine epidemic diarrhea virus in cell cultures and partial characterization of the isolate. J Vet Med Sci, 54: 313–318.

    Article  CAS  PubMed  Google Scholar 

  • Lai MMC, Perlman S, Anderson LJ. 2007. Coronaviridae. In: Fields Virology, Knipe DM, Howley PM (eds). Philadephia: Lippincott Williams & Wilkins, pp. 1305–1336.

    Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23: 2947–2948.

    Article  CAS  PubMed  Google Scholar 

  • Lau SK, Li KS, Tsang AK, Lam CS, Ahmed S, Chen H, Chan KH, Woo PC, Yuen KY. 2013. Genetic characterization of Betacoronavirus lineage C viruses in bats reveals marked sequence divergence in the spike protein of pipistrellus bat coronavirus HKU5 in Japanese pipistrelle: implications for the origin of the novel Middle East respiratory syndrome coronavirus. J Virol, 87: 8638–8650.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lau SK, Li KS, Tsang AK, Shek CT, Wang M, Choi GK, Guo R, Wong BH, Poon RW, Lam CS, Wang SY, Fan RY, Chan KH, Zheng BJ, Woo PC, Yuen KY. 2012. Recent transmission 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, 86: 11906–11918.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, Wong SS, Leung SY, Chan KH, Yuen KY. 2005. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A, 102: 14040–14045.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lau SKP, Woo PCY, Li KSM, Huang Y, Wang M, Lam CSF, Xu HF, Guo RT, Chan KH, Zheng BJ, Yuen KY. 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.

    Article  CAS  PubMed  Google Scholar 

  • Lelli D, Papetti A, Sabelli C, Rosti E, Moreno A, Boniotti MB. 2013. Detection of coronaviruses in bats of various species in Italy. Viruses, 5: 2679–2689.

    Article  PubMed Central  PubMed  Google Scholar 

  • Li W, Shi Z, Yu M, Ren W, Smith C, Epstein JH, Wang H, Crameri G, Hu Z, Zhang H, Zhang J, McEachern J, Field H, Daszak P, Eaton BT, Zhang S, Wang LF. 2005. Bats are natural reservoirs of SARS-like coronaviruses. Science, 310: 676–679.

    Article  CAS  PubMed  Google Scholar 

  • Luis AD, Hayman DTS, O'Shea TJ, Cryan PM, Gilbert AT, Pulliam JRC, Mills JN, Timonin ME, Willis CKR, Cunningham AA, Fooks AR, Rupprecht CE, Wood JLN, Webb CT. 2013. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proc Biol Sci, 280: 20122753.

    Article  PubMed Central  PubMed  Google Scholar 

  • Macnaughton MR, Madge MH. 1978. The genome of human coronavirus strain 229E. J Gen Virol, 39: 497–504.

    Article  CAS  PubMed  Google Scholar 

  • Martin DP, Williamson C, Posada D. 2005. RDP2: recombination detection and analysis from sequence alignments. Bioinformatics, 21: 260–262.

    Article  CAS  PubMed  Google Scholar 

  • Mayer F, von Helversen O. 2001. Cryptic diversity in European bats. Proc Biol Sci, 268: 1825–1832.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mihindukulasuriya KA, Wu G, St Leger J, Nordhausen RW, Wang D. 2008. Identification of a novel coronavirus from a beluga whale by using a panviral microarray. J Virol, 82: 5084–5088.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mizutani T. 2001. The mechanism of MHV transcription. Uirusu, 51: 225–236. (In Janpanese)

    Article  CAS  PubMed  Google Scholar 

  • Pedersen NC, Black JW, Boyle JF, Evermann JF, McKeirnan AJ, Ott RL. 1984. Pathogenic differences between various feline coronavirus isolates. Adv Exp Med Biol, 173: 365–380.

    Article  CAS  PubMed  Google Scholar 

  • Peiris JS, Lai ST, Poon LL, Guan Y, Yam LY, Lim W, Nicholls J, Yee WK, Yan WW, Cheung MT, Cheng VC, Chan KH, Tsang DN, Yung RW, Ng TK, Yuen KY. 2003. Coronavirus as a possible cause of severe acute respiratory syndrome. Lancet, 361: 1319–1325.

    Article  CAS  PubMed  Google Scholar 

  • Poon LL, Chu DK, Chan KH, Wong OK, Ellis TM, Leung YH, Lau SK, Woo PC, Suen KY, Yuen KY, Guan Y, Peiris JS. 2005. Identification of a novel coronavirus in bats. J Virol, 79: 2001–2009.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Quan PL, Firth C, Street C, Henriquez JA, Petrosov A, Tashmukhamedova A, Hutchison SK, Egholm M, Osinubi MO, Niezgoda M, Ogunkoya AB, Briese T, Rupprecht CE, Lipkin WI. 2010. Identification of a severe acute respiratory syndrome coronavirus-like virus in a leaf-nosed bat in Nigeria. MBio, 1. doi: 10.1128/mBio.00208-10.

    Google Scholar 

  • Shi ZL. 2013. Emerging infectious diseases associated with bat viruses. Science China-Life Sciences, 56: 678–682.

    Article  PubMed  Google Scholar 

  • Tang XC, Zhang JX, Zhang SY, Wang P, Fan XH, Li LF, Li G, Dong BQ, Liu W, Cheung CL, Xu KM, Song WJ, Vijaykrishna D, Poon LLM, Peiris JSM, Smith GJD, Chen H, Guan Y. 2006. Prevalence and genetic diversity of coronaviruses in bats from China. J Virol, 80: 7481–7490.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tong S, Conrardy C, Ruone S, Kuzmin IV, Guo X, Tao Y, Niezgoda M, Haynes L, Agwanda B, Breiman RF, Anderson LJ, Rupprecht CE. 2009. Detection of novel SARS-like and other coronaviruses in bats from Kenya. Emerg Infect Dis, 15: 482–485.

    Article  PubMed Central  PubMed  Google Scholar 

  • van Boheemen S, de Graaf M, Lauber C, Bestebroer TM, Raj VS, Zaki AM, Osterhaus AD, Haagmans BL, Gorbalenya AE, Snijder EJ, Fouchier RA. 2012. Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans. MBio, 3. doi: 10.1128/mBio.00473-12.

    Google Scholar 

  • van der Hoek L, Pyrc K, Jebbink MF, Vermeulen-Oost W, Berkhout RJ, Wolthers KC, Wertheim-van Dillen PM, Kaandorp J, Spaargaren J, Berkhout B. 2004. Identification of a new human coronavirus. Nat Med, 10: 368–373.

    Article  CAS  PubMed  Google Scholar 

  • Wacharapluesadee S, Duengkae P, Rodpan A, Kaewpom T, Maneeorn P, Kanchanasaka B, Yingsakmongkon S, Sittidetboripat N, Chareesaen C, Khlangsap N, Pidthong A, Leadprathom K, Ghai S, Epstein JH, Daszak P, Olival KJ, Blair PJ, Callahan MV, Hemachudha T. 2015. Diversity of coronavirus in bats from Eastern Thailand. Virol J, 12: 57.

    Article  PubMed Central  PubMed  Google Scholar 

  • Watanabe S, Masangkay JS, Nagata N, Morikawa S, Mizutani T, Fukushi S, Alviola P, Omatsu T, Ueda N, Iha K, Taniguchi S, Fujii H, Tsuda S, Endoh M, Kato K, Tohya Y, Kyuwa S, Yoshikawa Y, Akashi H. 2010. Bat Coronaviruses and Experimental Infection of Bats, the Philippines. Emerg Infect Dis, 16: 1217–1223.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Woo PC, Lau SK, Chu CM, Chan KH, Tsoi HW, Huang Y, Wong BH, Poon RW, Cai JJ, Luk WK, Poon LL, Wong SS, Guan Y, Peiris JS, Yuen KY. 2005. Characterization and complete genome sequence of a novel coronavirus, coronavirus HKU1, from patients with pneumonia. J Virol, 79: 884–895.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Woo PC, Lau SK, Lam CS, Lau CC, Tsang AK, Lau JH, Bai R, Teng JL, Tsang CC, Wang M, Zheng BJ, Chan KH, Yuen KY. 2012a. 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, 86: 3995–4008.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Woo PC, Lau SK, Li KS, Poon RW, Wong BH, Tsoi HW, Yip BC, Huang Y, Chan KH, Yuen KY. 2006. Molecular diversity of coronaviruses in bats. Virology, 351: 180–187.

    Article  CAS  PubMed  Google Scholar 

  • Woo PCY, Lau SKP, Huang Y, Yuen KY. 2009. Coronavirus Diversity, Phylogeny and Interspecies Jumping. Exp Biol Med (Maywood), 234: 1117–1127.

    Article  CAS  Google Scholar 

  • Woo PCY, Lau SKP, Li KSM, Tsang AKL, Yuen KY. 2012b. Genetic relatedness of the novel human group C betacoronavirus to Tylonycteris bat coronavirus HKU4 and Pipistrellus bat coronavirus HKU5. Emerg Microb Infect, 1: e35.

    Article  CAS  Google Scholar 

  • Wu ZQ, Yang L, Yang F, Ren XW, Jiang JY, Dong J, Sun LL, Zhu YF, Zhou HN, Jin Q. 2014. Novel Henipa-like Virus, Mojiang Paramyxovirus, in rats, China, 2012. Emerg Infect Dis, 20: 1064–1066.

    PubMed Central  PubMed  Google Scholar 

  • Yuan J, Hon CC, Li Y, Wang D, Xu G, Zhang H, Zhou P, Poon LL, Lam TT, Leung FC, Shi Z. 2010. Intraspecies diversity of SARS-like coronaviruses in Rhinolophus sinicus and its implications for the origin of SARS coronaviruses in humans. J Gen Virol, 91: 1058–1062.

    Article  CAS  PubMed  Google Scholar 

  • Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. 2012. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med, 367: 1814–1820.

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, 430071, China

    Xing-Yi Ge, Ning Wang, Wei Zhang, Ben Hu, Bei Li, Chu-Ming Luo, Xing-Lou Yang, Li-Jun Wu, Bo Wang & Zheng-Li Shi

  2. Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Yunnan Institute of Endemic Diseases Control and Prevention, Dali, 671000, China

    Yun-Zhi Zhang & Ji-Hua Zhou

  3. School of Public Health, Dali University, Dali, 671000, China

    Yun-Zhi Zhang

  4. Mojiang Center for Diseases Control and Prevention, Mojiang, 654800, China

    Yun Zhang & Zong-Xiao Li

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  1. Xing-Yi Ge
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  2. Ning Wang
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Correspondence to Zheng-Li Shi.

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ORCID: 0000-0001-8089-163X

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Ge, XY., Wang, N., Zhang, W. et al. Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft. Virol. Sin. 31, 31–40 (2016). https://doi.org/10.1007/s12250-016-3713-9

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  • Received: 01 January 2016

  • Accepted: 22 January 2016

  • Published: 18 February 2016

  • Issue Date: February 2016

  • DOI: https://doi.org/10.1007/s12250-016-3713-9

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Keywords

  • coronavirus
  • bat
  • coinfection
  • mineshaft
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