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<title xml:lang="en">Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft</title>
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<name sortKey="Ge, Xing Yi" sort="Ge, Xing Yi" uniqKey="Ge X" first="Xing-Yi" last="Ge">Xing-Yi Ge</name>
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Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
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<name sortKey="Wang, Ning" sort="Wang, Ning" uniqKey="Wang N" first="Ning" last="Wang">Ning Wang</name>
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Wuhan, 430071 China</nlm:aff>
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<name sortKey="Zhang, Wei" sort="Zhang, Wei" uniqKey="Zhang W" first="Wei" last="Zhang">Wei Zhang</name>
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Wuhan, 430071 China</nlm:aff>
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<name sortKey="Li, Bei" sort="Li, Bei" uniqKey="Li B" first="Bei" last="Li">Bei Li</name>
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<name sortKey="Zhang, Yun Zhi" sort="Zhang, Yun Zhi" uniqKey="Zhang Y" first="Yun-Zhi" last="Zhang">Yun-Zhi Zhang</name>
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Dali, 671000 China</nlm:aff>
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<name sortKey="Zhou, Ji Hua" sort="Zhou, Ji Hua" uniqKey="Zhou J" first="Ji-Hua" last="Zhou">Ji-Hua Zhou</name>
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<institution>Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention,</institution>
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</institution-wrap>
Dali, 671000 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Luo, Chu Ming" sort="Luo, Chu Ming" uniqKey="Luo C" first="Chu-Ming" last="Luo">Chu-Ming Luo</name>
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<author>
<name sortKey="Yang, Xing Lou" sort="Yang, Xing Lou" uniqKey="Yang X" first="Xing-Lou" last="Yang">Xing-Lou Yang</name>
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<institution>Chinese Academy of Sciences,</institution>
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Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wu, Li Jun" sort="Wu, Li Jun" uniqKey="Wu L" first="Li-Jun" last="Wu">Li-Jun Wu</name>
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<institution>Chinese Academy of Sciences,</institution>
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Wuhan, 430071 China</nlm:aff>
</affiliation>
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<name sortKey="Wang, Bo" sort="Wang, Bo" uniqKey="Wang B" first="Bo" last="Wang">Bo Wang</name>
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<institution>Chinese Academy of Sciences,</institution>
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Wuhan, 430071 China</nlm:aff>
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<author>
<name sortKey="Zhang, Yun" sort="Zhang, Yun" uniqKey="Zhang Y" first="Yun" last="Zhang">Yun Zhang</name>
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<nlm:aff id="Aff4">Mojiang Center for Diseases Control and Prevention, Mojiang, 654800 China</nlm:aff>
</affiliation>
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<name sortKey="Li, Zong Xiao" sort="Li, Zong Xiao" uniqKey="Li Z" first="Zong-Xiao" last="Li">Zong-Xiao Li</name>
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<nlm:aff id="Aff4">Mojiang Center for Diseases Control and Prevention, Mojiang, 654800 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Shi, Zheng Li" sort="Shi, Zheng Li" uniqKey="Shi Z" first="Zheng-Li" last="Shi">Zheng-Li Shi</name>
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<nlm:aff id="Aff1">
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<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
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Wuhan, 430071 China</nlm:aff>
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<idno type="doi">10.1007/s12250-016-3713-9</idno>
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<title xml:lang="en" level="a" type="main">Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft</title>
<author>
<name sortKey="Ge, Xing Yi" sort="Ge, Xing Yi" uniqKey="Ge X" first="Xing-Yi" last="Ge">Xing-Yi Ge</name>
<affiliation>
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wang, Ning" sort="Wang, Ning" uniqKey="Wang N" first="Ning" last="Wang">Ning Wang</name>
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<nlm:aff id="Aff1">
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<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Zhang, Wei" sort="Zhang, Wei" uniqKey="Zhang W" first="Wei" last="Zhang">Wei Zhang</name>
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<nlm:aff id="Aff1">
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<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Hu, Ben" sort="Hu, Ben" uniqKey="Hu B" first="Ben" last="Hu">Ben Hu</name>
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<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Li, Bei" sort="Li, Bei" uniqKey="Li B" first="Bei" last="Li">Bei Li</name>
<affiliation>
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Zhang, Yun Zhi" sort="Zhang, Yun Zhi" uniqKey="Zhang Y" first="Yun-Zhi" last="Zhang">Yun-Zhi Zhang</name>
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<nlm:aff id="Aff2">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.464498.3</institution-id>
<institution>Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention,</institution>
<institution>Yunnan Institute of Endemic Diseases Control and Prevention,</institution>
</institution-wrap>
Dali, 671000 China</nlm:aff>
</affiliation>
<affiliation>
<nlm:aff id="Aff3">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.440682.c</institution-id>
<institution>School of Public Health,</institution>
<institution>Dali University,</institution>
</institution-wrap>
Dali, 671000 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Zhou, Ji Hua" sort="Zhou, Ji Hua" uniqKey="Zhou J" first="Ji-Hua" last="Zhou">Ji-Hua Zhou</name>
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<nlm:aff id="Aff2">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.464498.3</institution-id>
<institution>Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention,</institution>
<institution>Yunnan Institute of Endemic Diseases Control and Prevention,</institution>
</institution-wrap>
Dali, 671000 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Luo, Chu Ming" sort="Luo, Chu Ming" uniqKey="Luo C" first="Chu-Ming" last="Luo">Chu-Ming Luo</name>
<affiliation>
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Yang, Xing Lou" sort="Yang, Xing Lou" uniqKey="Yang X" first="Xing-Lou" last="Yang">Xing-Lou Yang</name>
<affiliation>
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wu, Li Jun" sort="Wu, Li Jun" uniqKey="Wu L" first="Li-Jun" last="Wu">Li-Jun Wu</name>
<affiliation>
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Wang, Bo" sort="Wang, Bo" uniqKey="Wang B" first="Bo" last="Wang">Bo Wang</name>
<affiliation>
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Zhang, Yun" sort="Zhang, Yun" uniqKey="Zhang Y" first="Yun" last="Zhang">Yun Zhang</name>
<affiliation>
<nlm:aff id="Aff4">Mojiang Center for Diseases Control and Prevention, Mojiang, 654800 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Li, Zong Xiao" sort="Li, Zong Xiao" uniqKey="Li Z" first="Zong-Xiao" last="Li">Zong-Xiao Li</name>
<affiliation>
<nlm:aff id="Aff4">Mojiang Center for Diseases Control and Prevention, Mojiang, 654800 China</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Shi, Zheng Li" sort="Shi, Zheng Li" uniqKey="Shi Z" first="Zheng-Li" last="Shi">Zheng-Li Shi</name>
<affiliation>
<nlm:aff id="Aff1">
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</nlm:aff>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Virologica Sinica</title>
<idno type="ISSN">1674-0769</idno>
<idno type="eISSN">1995-820X</idno>
<imprint>
<date when="2016">2016</date>
</imprint>
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<front>
<div type="abstract" xml:lang="en">
<p>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:
<italic>Rhinolophus sinicus</italic>
,
<italic>Rhinolophus affinis</italic>
,
<italic>Hipposideros pomona</italic>
,
<italic>Miniopterus schreibersii</italic>
,
<italic>Miniopterus fuliginosus</italic>
, and
<italic>Miniopterus fuscus</italic>
. By sequencing PCR products of the coronavirus RNA-dependent RNA polymerase gene (
<italic>RdRp</italic>
), we found a high frequency of infection by a diverse group of coronaviruses in different bat species in the mineshaft. Sequenced partial
<italic>RdRp</italic>
fragments had 80%–99% nucleic acid sequence identity with well-characterized
<italic>Alphacoronavirus</italic>
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.
<graphic position="anchor" xlink:href="12250_2016_3713_Figa_HTML" id="d29e316"></graphic>
</p>
<sec>
<title>Electronic Supplementary Material</title>
<p>Supplementary material is available for this article at 10.1007/s12250-016-3713-9 and is accessible for authorized users.</p>
</sec>
</div>
</front>
<back>
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<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Virol Sin</journal-id>
<journal-id journal-id-type="iso-abbrev">Virol Sin</journal-id>
<journal-title-group>
<journal-title>Virologica Sinica</journal-title>
</journal-title-group>
<issn pub-type="ppub">1674-0769</issn>
<issn pub-type="epub">1995-820X</issn>
<publisher>
<publisher-name>Springer Singapore</publisher-name>
<publisher-loc>Singapore</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">26920708</article-id>
<article-id pub-id-type="pmc">7090819</article-id>
<article-id pub-id-type="publisher-id">3713</article-id>
<article-id pub-id-type="doi">10.1007/s12250-016-3713-9</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Research Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Coexistence of multiple coronaviruses in several bat colonies in an abandoned mineshaft</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Ge</surname>
<given-names>Xing-Yi</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Ning</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Wei</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hu</surname>
<given-names>Ben</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Li</surname>
<given-names>Bei</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Yun-Zhi</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
<xref ref-type="aff" rid="Aff3">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhou</surname>
<given-names>Ji-Hua</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Luo</surname>
<given-names>Chu-Ming</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Yang</surname>
<given-names>Xing-Lou</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wu</surname>
<given-names>Li-Jun</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Wang</surname>
<given-names>Bo</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Yun</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Li</surname>
<given-names>Zong-Xiao</given-names>
</name>
<xref ref-type="aff" rid="Aff4">4</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Shi</surname>
<given-names>Zheng-Li</given-names>
</name>
<address>
<phone>+86-27-87197240</phone>
<email>zlshi@wh.iov.cn</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<aff id="Aff1">
<label>1</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.9227.e</institution-id>
<institution-id institution-id-type="ISNI">0000000119573309</institution-id>
<institution>Key Laboratory of Special Pathogens, Wuhan Institute of Virology,</institution>
<institution>Chinese Academy of Sciences,</institution>
</institution-wrap>
Wuhan, 430071 China</aff>
<aff id="Aff2">
<label>2</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.464498.3</institution-id>
<institution>Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention,</institution>
<institution>Yunnan Institute of Endemic Diseases Control and Prevention,</institution>
</institution-wrap>
Dali, 671000 China</aff>
<aff id="Aff3">
<label>3</label>
<institution-wrap>
<institution-id institution-id-type="GRID">grid.440682.c</institution-id>
<institution>School of Public Health,</institution>
<institution>Dali University,</institution>
</institution-wrap>
Dali, 671000 China</aff>
<aff id="Aff4">
<label>4</label>
Mojiang Center for Diseases Control and Prevention, Mojiang, 654800 China</aff>
</contrib-group>
<pub-date pub-type="epub">
<day>18</day>
<month>2</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection">
<month>2</month>
<year>2016</year>
</pub-date>
<volume>31</volume>
<issue>1</issue>
<fpage>31</fpage>
<lpage>40</lpage>
<history>
<date date-type="received">
<day>1</day>
<month>1</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>22</day>
<month>1</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>© Wuhan Institute of Virology, CAS and Springer Science+Business Media Singapore 2016</copyright-statement>
<license>
<license-p>This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.</license-p>
</license>
</permissions>
<abstract id="Abs1">
<p>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:
<italic>Rhinolophus sinicus</italic>
,
<italic>Rhinolophus affinis</italic>
,
<italic>Hipposideros pomona</italic>
,
<italic>Miniopterus schreibersii</italic>
,
<italic>Miniopterus fuliginosus</italic>
, and
<italic>Miniopterus fuscus</italic>
. By sequencing PCR products of the coronavirus RNA-dependent RNA polymerase gene (
<italic>RdRp</italic>
), we found a high frequency of infection by a diverse group of coronaviruses in different bat species in the mineshaft. Sequenced partial
<italic>RdRp</italic>
fragments had 80%–99% nucleic acid sequence identity with well-characterized
<italic>Alphacoronavirus</italic>
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.
<graphic position="anchor" xlink:href="12250_2016_3713_Figa_HTML" id="d29e316"></graphic>
</p>
<sec>
<title>Electronic Supplementary Material</title>
<p>Supplementary material is available for this article at 10.1007/s12250-016-3713-9 and is accessible for authorized users.</p>
</sec>
</abstract>
<kwd-group xml:lang="en">
<title>Keywords</title>
<kwd>coronavirus</kwd>
<kwd>bat</kwd>
<kwd>coinfection</kwd>
<kwd>mineshaft</kwd>
</kwd-group>
<custom-meta-group>
<custom-meta>
<meta-name>issue-copyright-statement</meta-name>
<meta-value>© Wuhan Institute of Virology, CAS and Springer Science+Business Media Singapore 2016</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
<body>
<sec sec-type="supplementary-material">
<title>Electronic supplementary material</title>
<sec id="Sec1">
<p>
<supplementary-material content-type="local-data" id="MOESM1">
<media xlink:href="12250_2016_3713_MOESM1_ESM.pdf">
<caption>
<p>Supplementary material, approximately 122 KB.</p>
</caption>
</media>
</supplementary-material>
</p>
</sec>
</sec>
</body>
<back>
<fn-group>
<fn>
<p>ORCID: 0000-0001-8089-163X</p>
</fn>
</fn-group>
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