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<title xml:lang="en">Surveillance of Bat Coronaviruses in Kenya Identifies Relatives of Human Coronaviruses NL63 and 229E and Their Recombination History</title>
<author>
<name sortKey="Tao, Ying" sort="Tao, Ying" uniqKey="Tao Y" first="Ying" last="Tao">Ying Tao</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Shi, Mang" sort="Shi, Mang" uniqKey="Shi M" first="Mang" last="Shi">Mang Shi</name>
<affiliation>
<nlm:aff id="aff2">Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Chommanard, Christina" sort="Chommanard, Christina" uniqKey="Chommanard C" first="Christina" last="Chommanard">Christina Chommanard</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Queen, Krista" sort="Queen, Krista" uniqKey="Queen K" first="Krista" last="Queen">Krista Queen</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Zhang, Jing" sort="Zhang, Jing" uniqKey="Zhang J" first="Jing" last="Zhang">Jing Zhang</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Markotter, Wanda" sort="Markotter, Wanda" uniqKey="Markotter W" first="Wanda" last="Markotter">Wanda Markotter</name>
<affiliation>
<nlm:aff id="aff3">Centre for Viral Zoonoses, Department of Medical Virology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kuzmin, Ivan V" sort="Kuzmin, Ivan V" uniqKey="Kuzmin I" first="Ivan V." last="Kuzmin">Ivan V. Kuzmin</name>
<affiliation>
<nlm:aff id="aff4">Division of High Consequence Pathogens and Pathology, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Holmes, Edward C" sort="Holmes, Edward C" uniqKey="Holmes E" first="Edward C." last="Holmes">Edward C. Holmes</name>
<affiliation>
<nlm:aff id="aff2">Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Tong, Suxiang" sort="Tong, Suxiang" uniqKey="Tong S" first="Suxiang" last="Tong">Suxiang Tong</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
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<idno type="RBID">PMC:5309958</idno>
<idno type="doi">10.1128/JVI.01953-16</idno>
<date when="2017">2017</date>
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<title xml:lang="en" level="a" type="main">Surveillance of Bat Coronaviruses in Kenya Identifies Relatives of Human Coronaviruses NL63 and 229E and Their Recombination History</title>
<author>
<name sortKey="Tao, Ying" sort="Tao, Ying" uniqKey="Tao Y" first="Ying" last="Tao">Ying Tao</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Shi, Mang" sort="Shi, Mang" uniqKey="Shi M" first="Mang" last="Shi">Mang Shi</name>
<affiliation>
<nlm:aff id="aff2">Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Chommanard, Christina" sort="Chommanard, Christina" uniqKey="Chommanard C" first="Christina" last="Chommanard">Christina Chommanard</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Queen, Krista" sort="Queen, Krista" uniqKey="Queen K" first="Krista" last="Queen">Krista Queen</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Zhang, Jing" sort="Zhang, Jing" uniqKey="Zhang J" first="Jing" last="Zhang">Jing Zhang</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Markotter, Wanda" sort="Markotter, Wanda" uniqKey="Markotter W" first="Wanda" last="Markotter">Wanda Markotter</name>
<affiliation>
<nlm:aff id="aff3">Centre for Viral Zoonoses, Department of Medical Virology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Kuzmin, Ivan V" sort="Kuzmin, Ivan V" uniqKey="Kuzmin I" first="Ivan V." last="Kuzmin">Ivan V. Kuzmin</name>
<affiliation>
<nlm:aff id="aff4">Division of High Consequence Pathogens and Pathology, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Holmes, Edward C" sort="Holmes, Edward C" uniqKey="Holmes E" first="Edward C." last="Holmes">Edward C. Holmes</name>
<affiliation>
<nlm:aff id="aff2">Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia</nlm:aff>
</affiliation>
</author>
<author>
<name sortKey="Tong, Suxiang" sort="Tong, Suxiang" uniqKey="Tong S" first="Suxiang" last="Tong">Suxiang Tong</name>
<affiliation>
<nlm:aff id="aff1">Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</nlm:aff>
</affiliation>
</author>
</analytic>
<series>
<title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
<idno type="eISSN">1098-5514</idno>
<imprint>
<date when="2017">2017</date>
</imprint>
</series>
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<div type="abstract" xml:lang="en">
<title>ABSTRACT</title>
<p>Bats harbor a large diversity of coronaviruses (CoVs), several of which are related to zoonotic pathogens that cause severe disease in humans. Our screening of bat samples collected in Kenya from 2007 to 2010 not only detected RNA from several novel CoVs but, more significantly, identified sequences that were closely related to human CoVs NL63 and 229E, suggesting that these two human viruses originate from bats. We also demonstrated that human CoV NL63 is a recombinant between NL63-like viruses circulating in
<named-content content-type="genus-species">Triaenops</named-content>
bats and 229E-like viruses circulating in
<named-content content-type="genus-species">Hipposideros</named-content>
bats, with the breakpoint located near 5′ and 3′ ends of the spike (S) protein gene. In addition, two further interspecies recombination events involving the S gene were identified, suggesting that this region may represent a recombination “hot spot” in CoV genomes. Finally, using a combination of phylogenetic and distance-based approaches, we showed that the genetic diversity of bat CoVs is primarily structured by host species and subsequently by geographic distances.</p>
<p>
<bold>IMPORTANCE</bold>
Understanding the driving forces of cross-species virus transmission is central to understanding the nature of disease emergence. Previous studies have demonstrated that bats are the ultimate reservoir hosts for a number of coronaviruses (CoVs), including ancestors of severe acute respiratory syndrome coronavirus (SARS-CoV), Middle East respiratory syndrome coronavirus (MERS-CoV), and human CoV 229E (HCoV-229E). However, the evolutionary pathways of bat CoVs remain elusive. We provide evidence for natural recombination between distantly related African bat coronaviruses associated with
<named-content content-type="genus-species">Triaenops afer</named-content>
and
<named-content content-type="genus-species">Hipposideros</named-content>
sp. bats that resulted in a NL63-like virus, an ancestor of the human pathogen HCoV-NL63. These results suggest that interspecies recombination may play an important role in CoV evolution and the emergence of novel CoVs with zoonotic potential.</p>
</div>
</front>
</TEI>
<pmc article-type="research-article">
<pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">J Virol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Virol</journal-id>
<journal-id journal-id-type="hwp">jvi</journal-id>
<journal-id journal-id-type="pmc">jvi</journal-id>
<journal-id journal-id-type="publisher-id">JVI</journal-id>
<journal-title-group>
<journal-title>Journal of Virology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-538X</issn>
<issn pub-type="epub">1098-5514</issn>
<publisher>
<publisher-name>American Society for Microbiology</publisher-name>
<publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">28077633</article-id>
<article-id pub-id-type="pmc">5309958</article-id>
<article-id pub-id-type="publisher-id">01953-16</article-id>
<article-id pub-id-type="doi">10.1128/JVI.01953-16</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Genetic Diversity and Evolution</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Surveillance of Bat Coronaviruses in Kenya Identifies Relatives of Human Coronaviruses NL63 and 229E and Their Recombination History</article-title>
<alt-title alt-title-type="running-head">Bat Origin of Human Coronaviruses</alt-title>
<alt-title alt-title-type="short-authors">Tao et al.</alt-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Tao</surname>
<given-names>Ying</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Shi</surname>
<given-names>Mang</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Chommanard</surname>
<given-names>Christina</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Queen</surname>
<given-names>Krista</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Zhang</surname>
<given-names>Jing</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Markotter</surname>
<given-names>Wanda</given-names>
</name>
<xref ref-type="aff" rid="aff3">
<sup>c</sup>
</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Kuzmin</surname>
<given-names>Ivan V.</given-names>
</name>
<xref ref-type="aff" rid="aff4">
<sup>d</sup>
</xref>
<xref ref-type="author-notes" rid="fn1">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Holmes</surname>
<given-names>Edward C.</given-names>
</name>
<xref ref-type="aff" rid="aff2">
<sup>b</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes">
<name>
<surname>Tong</surname>
<given-names>Suxiang</given-names>
</name>
<xref ref-type="aff" rid="aff1">
<sup>a</sup>
</xref>
</contrib>
<aff id="aff1">
<label>a</label>
Division of Viral Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</aff>
<aff id="aff2">
<label>b</label>
Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, The University of Sydney, Sydney, Australia</aff>
<aff id="aff3">
<label>c</label>
Centre for Viral Zoonoses, Department of Medical Virology, Faculty of Health Sciences, University of Pretoria, Pretoria, South Africa</aff>
<aff id="aff4">
<label>d</label>
Division of High Consequence Pathogens and Pathology, Centers for Disease Control and Prevention, Atlanta, Georgia, USA</aff>
</contrib-group>
<contrib-group>
<contrib contrib-type="editor">
<name>
<surname>Perlman</surname>
<given-names>Stanley</given-names>
</name>
<role>Editor</role>
<aff>University of Iowa</aff>
</contrib>
</contrib-group>
<author-notes>
<corresp id="cor1">Address correspondence to Suxiang Tong,
<email>sot1@cdc.gov</email>
.</corresp>
<fn id="fn1" fn-type="present-address">
<label>*</label>
<p>Present address: Ivan V. Kuzmin, Department of Pathology, University of Texas Medical Branch, Galveston, Texas, USA.</p>
</fn>
<fn fn-type="equal">
<p>Y.T. and M.S. contributed equally to this article.</p>
</fn>
<fn fn-type="other">
<p>
<bold>Citation</bold>
Tao Y, Shi M, Chommanard C, Queen K, Zhang J, Markotter W, Kuzmin IV, Holmes EC, Tong S. 2017. Surveillance of bat coronaviruses in Kenya identifies relatives of human coronaviruses NL63 and 229E and their recombination history. J Virol 91:e01953-16.
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/JVI.01953-16">https://doi.org/10.1128/JVI.01953-16</ext-link>
.</p>
</fn>
</author-notes>
<pub-date pub-type="epreprint">
<day>11</day>
<month>1</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="epub">
<day>14</day>
<month>2</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<day>1</day>
<month>3</month>
<year>2017</year>
</pub-date>
<volume>91</volume>
<issue>5</issue>
<elocation-id>e01953-16</elocation-id>
<history>
<date date-type="received">
<day>29</day>
<month>9</month>
<year>2016</year>
</date>
<date date-type="accepted">
<day>4</day>
<month>12</month>
<year>2016</year>
</date>
</history>
<permissions>
<copyright-statement>Copyright © 2017 American Society for Microbiology.</copyright-statement>
<copyright-year>2017</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
<license license-type="asm" xlink:href="https://doi.org/10.1128/ASMCopyrightv1">
<license-p>
<ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/ASMCopyrightv1">All Rights Reserved</ext-link>
.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:href="zjv005172365001.pdf"></self-uri>
<abstract>
<title>ABSTRACT</title>
<p>Bats harbor a large diversity of coronaviruses (CoVs), several of which are related to zoonotic pathogens that cause severe disease in humans. Our screening of bat samples collected in Kenya from 2007 to 2010 not only detected RNA from several novel CoVs but, more significantly, identified sequences that were closely related to human CoVs NL63 and 229E, suggesting that these two human viruses originate from bats. We also demonstrated that human CoV NL63 is a recombinant between NL63-like viruses circulating in
<named-content content-type="genus-species">Triaenops</named-content>
bats and 229E-like viruses circulating in
<named-content content-type="genus-species">Hipposideros</named-content>
bats, with the breakpoint located near 5′ and 3′ ends of the spike (S) protein gene. In addition, two further interspecies recombination events involving the S gene were identified, suggesting that this region may represent a recombination “hot spot” in CoV genomes. Finally, using a combination of phylogenetic and distance-based approaches, we showed that the genetic diversity of bat CoVs is primarily structured by host species and subsequently by geographic distances.</p>
<p>
<bold>IMPORTANCE</bold>
Understanding the driving forces of cross-species virus transmission is central to understanding the nature of disease emergence. Previous studies have demonstrated that bats are the ultimate reservoir hosts for a number of coronaviruses (CoVs), including ancestors of severe acute respiratory syndrome coronavirus (SARS-CoV), Middle East respiratory syndrome coronavirus (MERS-CoV), and human CoV 229E (HCoV-229E). However, the evolutionary pathways of bat CoVs remain elusive. We provide evidence for natural recombination between distantly related African bat coronaviruses associated with
<named-content content-type="genus-species">Triaenops afer</named-content>
and
<named-content content-type="genus-species">Hipposideros</named-content>
sp. bats that resulted in a NL63-like virus, an ancestor of the human pathogen HCoV-NL63. These results suggest that interspecies recombination may play an important role in CoV evolution and the emergence of novel CoVs with zoonotic potential.</p>
</abstract>
<kwd-group>
<title>KEYWORDS</title>
<kwd>Africa</kwd>
<kwd>bats</kwd>
<kwd>coronavirus</kwd>
<kwd>HCoV-229E</kwd>
<kwd>HCoV-NL63</kwd>
<kwd>recombination</kwd>
<kwd>zoonoses</kwd>
</kwd-group>
<funding-group>
<award-group id="award1">
<funding-source id="gs1">HHS | Centers for Disease Control and Prevention (CDC)
<named-content content-type="funder-id">https://doi.org/10.13039/100000030</named-content>
</funding-source>
<award-id rid="gs1">Global Disease Detection program TSC funds</award-id>
<principal-award-recipient>Suxiang Tong</principal-award-recipient>
</award-group>
<award-group id="award2">
<funding-source id="gs2">Department of Health | National Health and Medical Research Council (NHMRC)
<named-content content-type="funder-id">https://doi.org/10.13039/501100000925</named-content>
</funding-source>
<award-id rid="gs2">AF30</award-id>
<principal-award-recipient>Edward C. Holmes</principal-award-recipient>
</award-group>
</funding-group>
<counts>
<count count="1" count-type="supplementary-material"></count>
<fig-count count="8"></fig-count>
<table-count count="4"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="52"></ref-count>
<page-count count="16"></page-count>
<word-count count="8329"></word-count>
</counts>
<custom-meta-group>
<custom-meta>
<meta-name>cover-date</meta-name>
<meta-value>March 2017</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
</record>

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