Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia
Identifieur interne : 001059 ( Pmc/Corpus ); précédent : 001058; suivant : 001060Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia
Auteurs : Audrey Lacroix ; Veasna Duong ; Vibol Hul ; Sorn San ; Hull Davun ; Keo Omaliss ; Sokha Chea ; Alexandre Hassanin ; Watthana Theppangna ; Soubanh Silithammavong ; Kongsy Khammavong ; Sinpakone Singhalath ; Zoe Greatorex ; Amanda E. Fine ; Tracey Goldstein ; Sarah Olson ; Damien O. Joly ; Lucy Keatts ; Philippe Dussart ; Aneta Afelt ; Roger Frutos ; Philippe BuchySource :
- Infection, Genetics and Evolution [ 1567-1348 ] ; 2016.
Abstract
South-East Asia is a hot spot for emerging zoonotic diseases, and bats have been recognized as hosts for a large number of zoonotic viruses such as Severe Acute Respiratory Syndrome (SARS), responsible for acute respiratory syndrome outbreaks. Thus, it is important to expand our knowledge of the presence of viruses in bats which could represent a risk to humans. Coronaviruses (CoVs) have been reported in bat species from Thailand, China, Indonesia, Taiwan and the Philippines. However no such work was conducted in Cambodia or Lao PDR. Between 2010 and 2013, 1965 bats were therefore sampled at interfaces with human populations in these two countries. They were tested for the presence of coronavirus by consensus reverse transcription-PCR assay. A total of 93 samples (4.7%) from 17 genera of bats tested positive. Sequence analysis revealed the presence of potentially 37 and 56 coronavirus belonging to alpha-coronavirus (αCoV) and beta-CoV (βCoV), respectively. The βCoVs group is known to include some coronaviruses highly pathogenic to human, such as SARS-CoV and MERS-CoV. All coronavirus sequences generated from frugivorous bats (family
Url:
DOI: 10.1016/j.meegid.2016.11.029
PubMed: 27932284
PubMed Central: 7106194
Links to Exploration step
PMC:7106194Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia</title><author><name sortKey="Lacroix, Audrey" sort="Lacroix, Audrey" uniqKey="Lacroix A" first="Audrey" last="Lacroix">Audrey Lacroix</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Duong, Veasna" sort="Duong, Veasna" uniqKey="Duong V" first="Veasna" last="Duong">Veasna Duong</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Hul, Vibol" sort="Hul, Vibol" uniqKey="Hul V" first="Vibol" last="Hul">Vibol Hul</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation></author><author><name sortKey="San, Sorn" sort="San, Sorn" uniqKey="San S" first="Sorn" last="San">Sorn San</name><affiliation><nlm:aff id="af0010">National Veterinary Research Institute, Ministry of Agriculture Forestry and Fisheries, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Davun, Hull" sort="Davun, Hull" uniqKey="Davun H" first="Hull" last="Davun">Hull Davun</name><affiliation><nlm:aff id="af0010">National Veterinary Research Institute, Ministry of Agriculture Forestry and Fisheries, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Omaliss, Keo" sort="Omaliss, Keo" uniqKey="Omaliss K" first="Keo" last="Omaliss">Keo Omaliss</name><affiliation><nlm:aff id="af0015">Forest Administration, Ministry of Agriculture Forestry and Fisheries, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Chea, Sokha" sort="Chea, Sokha" uniqKey="Chea S" first="Sokha" last="Chea">Sokha Chea</name><affiliation><nlm:aff id="af0020">Wildlife Conservation Society, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Hassanin, Alexandre" sort="Hassanin, Alexandre" uniqKey="Hassanin A" first="Alexandre" last="Hassanin">Alexandre Hassanin</name><affiliation><nlm:aff id="af0025">Muséum national d'Histoire naturelle, Institut de Systématique, Evolution, Biodiversité (ISYEB), UMR 7205 MNHN CNRS UPMC, France</nlm:aff></affiliation></author><author><name sortKey="Theppangna, Watthana" sort="Theppangna, Watthana" uniqKey="Theppangna W" first="Watthana" last="Theppangna">Watthana Theppangna</name><affiliation><nlm:aff id="af0030">National Animal Health Laboratory, Ministry of Agriculture Forestry and Fisheries, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Silithammavong, Soubanh" sort="Silithammavong, Soubanh" uniqKey="Silithammavong S" first="Soubanh" last="Silithammavong">Soubanh Silithammavong</name><affiliation><nlm:aff id="af0035">Wildlife Conservation Society, Lao Democratic People's Republic</nlm:aff></affiliation><affiliation><nlm:aff id="af0040">Metabiota Inc., Vientiane, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Khammavong, Kongsy" sort="Khammavong, Kongsy" uniqKey="Khammavong K" first="Kongsy" last="Khammavong">Kongsy Khammavong</name><affiliation><nlm:aff id="af0035">Wildlife Conservation Society, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Singhalath, Sinpakone" sort="Singhalath, Sinpakone" uniqKey="Singhalath S" first="Sinpakone" last="Singhalath">Sinpakone Singhalath</name><affiliation><nlm:aff id="af0035">Wildlife Conservation Society, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Greatorex, Zoe" sort="Greatorex, Zoe" uniqKey="Greatorex Z" first="Zoe" last="Greatorex">Zoe Greatorex</name><affiliation><nlm:aff id="af0035">Wildlife Conservation Society, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Fine, Amanda E" sort="Fine, Amanda E" uniqKey="Fine A" first="Amanda E." last="Fine">Amanda E. Fine</name><affiliation><nlm:aff id="af0045">Wildlife Conservation Society, Vietnam Program, Hanoi, Vietnam</nlm:aff></affiliation></author><author><name sortKey="Goldstein, Tracey" sort="Goldstein, Tracey" uniqKey="Goldstein T" first="Tracey" last="Goldstein">Tracey Goldstein</name><affiliation><nlm:aff id="af0050">One Health Institute, School of Veterinary Medicine, University of California, Davis, USA</nlm:aff></affiliation></author><author><name sortKey="Olson, Sarah" sort="Olson, Sarah" uniqKey="Olson S" first="Sarah" last="Olson">Sarah Olson</name><affiliation><nlm:aff id="af0055">Wildlife Conservation Society, Wildlife Health Program, Bronx, New York, USA</nlm:aff></affiliation></author><author><name sortKey="Joly, Damien O" sort="Joly, Damien O" uniqKey="Joly D" first="Damien O." last="Joly">Damien O. Joly</name><affiliation><nlm:aff id="af0055">Wildlife Conservation Society, Wildlife Health Program, Bronx, New York, USA</nlm:aff></affiliation><affiliation><nlm:aff id="af0060">Metabiota Inc., Nanaimo, British Columbia, Canada</nlm:aff></affiliation></author><author><name sortKey="Keatts, Lucy" sort="Keatts, Lucy" uniqKey="Keatts L" first="Lucy" last="Keatts">Lucy Keatts</name><affiliation><nlm:aff id="af0020">Wildlife Conservation Society, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Dussart, Philippe" sort="Dussart, Philippe" uniqKey="Dussart P" first="Philippe" last="Dussart">Philippe Dussart</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Afelt, Aneta" sort="Afelt, Aneta" uniqKey="Afelt A" first="Aneta" last="Afelt">Aneta Afelt</name><affiliation><nlm:aff id="af0065">Institute of Physical Geography, Faculty of Geography and Regional Studies, University of Warsaw, Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Frutos, Roger" sort="Frutos, Roger" uniqKey="Frutos R" first="Roger" last="Frutos">Roger Frutos</name><affiliation><nlm:aff id="af0070">Cirad, UMR 17, Cirad-Ird, TA-A17/G, Montpellier, France</nlm:aff></affiliation><affiliation><nlm:aff id="af0075">Université de Montpellier, IES, UMR 5214, CNRS-UM, Montpellier, France</nlm:aff></affiliation></author><author><name sortKey="Buchy, Philippe" sort="Buchy, Philippe" uniqKey="Buchy P" first="Philippe" last="Buchy">Philippe Buchy</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation><affiliation><nlm:aff id="af0080">GSK Vaccines R&D, 150 Beach road, # 22-00, 189720, Singapore</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27932284</idno><idno type="pmc">7106194</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7106194</idno><idno type="RBID">PMC:7106194</idno><idno type="doi">10.1016/j.meegid.2016.11.029</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">001059</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001059</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia</title><author><name sortKey="Lacroix, Audrey" sort="Lacroix, Audrey" uniqKey="Lacroix A" first="Audrey" last="Lacroix">Audrey Lacroix</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Duong, Veasna" sort="Duong, Veasna" uniqKey="Duong V" first="Veasna" last="Duong">Veasna Duong</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Hul, Vibol" sort="Hul, Vibol" uniqKey="Hul V" first="Vibol" last="Hul">Vibol Hul</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation></author><author><name sortKey="San, Sorn" sort="San, Sorn" uniqKey="San S" first="Sorn" last="San">Sorn San</name><affiliation><nlm:aff id="af0010">National Veterinary Research Institute, Ministry of Agriculture Forestry and Fisheries, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Davun, Hull" sort="Davun, Hull" uniqKey="Davun H" first="Hull" last="Davun">Hull Davun</name><affiliation><nlm:aff id="af0010">National Veterinary Research Institute, Ministry of Agriculture Forestry and Fisheries, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Omaliss, Keo" sort="Omaliss, Keo" uniqKey="Omaliss K" first="Keo" last="Omaliss">Keo Omaliss</name><affiliation><nlm:aff id="af0015">Forest Administration, Ministry of Agriculture Forestry and Fisheries, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Chea, Sokha" sort="Chea, Sokha" uniqKey="Chea S" first="Sokha" last="Chea">Sokha Chea</name><affiliation><nlm:aff id="af0020">Wildlife Conservation Society, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Hassanin, Alexandre" sort="Hassanin, Alexandre" uniqKey="Hassanin A" first="Alexandre" last="Hassanin">Alexandre Hassanin</name><affiliation><nlm:aff id="af0025">Muséum national d'Histoire naturelle, Institut de Systématique, Evolution, Biodiversité (ISYEB), UMR 7205 MNHN CNRS UPMC, France</nlm:aff></affiliation></author><author><name sortKey="Theppangna, Watthana" sort="Theppangna, Watthana" uniqKey="Theppangna W" first="Watthana" last="Theppangna">Watthana Theppangna</name><affiliation><nlm:aff id="af0030">National Animal Health Laboratory, Ministry of Agriculture Forestry and Fisheries, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Silithammavong, Soubanh" sort="Silithammavong, Soubanh" uniqKey="Silithammavong S" first="Soubanh" last="Silithammavong">Soubanh Silithammavong</name><affiliation><nlm:aff id="af0035">Wildlife Conservation Society, Lao Democratic People's Republic</nlm:aff></affiliation><affiliation><nlm:aff id="af0040">Metabiota Inc., Vientiane, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Khammavong, Kongsy" sort="Khammavong, Kongsy" uniqKey="Khammavong K" first="Kongsy" last="Khammavong">Kongsy Khammavong</name><affiliation><nlm:aff id="af0035">Wildlife Conservation Society, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Singhalath, Sinpakone" sort="Singhalath, Sinpakone" uniqKey="Singhalath S" first="Sinpakone" last="Singhalath">Sinpakone Singhalath</name><affiliation><nlm:aff id="af0035">Wildlife Conservation Society, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Greatorex, Zoe" sort="Greatorex, Zoe" uniqKey="Greatorex Z" first="Zoe" last="Greatorex">Zoe Greatorex</name><affiliation><nlm:aff id="af0035">Wildlife Conservation Society, Lao Democratic People's Republic</nlm:aff></affiliation></author><author><name sortKey="Fine, Amanda E" sort="Fine, Amanda E" uniqKey="Fine A" first="Amanda E." last="Fine">Amanda E. Fine</name><affiliation><nlm:aff id="af0045">Wildlife Conservation Society, Vietnam Program, Hanoi, Vietnam</nlm:aff></affiliation></author><author><name sortKey="Goldstein, Tracey" sort="Goldstein, Tracey" uniqKey="Goldstein T" first="Tracey" last="Goldstein">Tracey Goldstein</name><affiliation><nlm:aff id="af0050">One Health Institute, School of Veterinary Medicine, University of California, Davis, USA</nlm:aff></affiliation></author><author><name sortKey="Olson, Sarah" sort="Olson, Sarah" uniqKey="Olson S" first="Sarah" last="Olson">Sarah Olson</name><affiliation><nlm:aff id="af0055">Wildlife Conservation Society, Wildlife Health Program, Bronx, New York, USA</nlm:aff></affiliation></author><author><name sortKey="Joly, Damien O" sort="Joly, Damien O" uniqKey="Joly D" first="Damien O." last="Joly">Damien O. Joly</name><affiliation><nlm:aff id="af0055">Wildlife Conservation Society, Wildlife Health Program, Bronx, New York, USA</nlm:aff></affiliation><affiliation><nlm:aff id="af0060">Metabiota Inc., Nanaimo, British Columbia, Canada</nlm:aff></affiliation></author><author><name sortKey="Keatts, Lucy" sort="Keatts, Lucy" uniqKey="Keatts L" first="Lucy" last="Keatts">Lucy Keatts</name><affiliation><nlm:aff id="af0020">Wildlife Conservation Society, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Dussart, Philippe" sort="Dussart, Philippe" uniqKey="Dussart P" first="Philippe" last="Dussart">Philippe Dussart</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation></author><author><name sortKey="Afelt, Aneta" sort="Afelt, Aneta" uniqKey="Afelt A" first="Aneta" last="Afelt">Aneta Afelt</name><affiliation><nlm:aff id="af0065">Institute of Physical Geography, Faculty of Geography and Regional Studies, University of Warsaw, Warsaw, Poland</nlm:aff></affiliation></author><author><name sortKey="Frutos, Roger" sort="Frutos, Roger" uniqKey="Frutos R" first="Roger" last="Frutos">Roger Frutos</name><affiliation><nlm:aff id="af0070">Cirad, UMR 17, Cirad-Ird, TA-A17/G, Montpellier, France</nlm:aff></affiliation><affiliation><nlm:aff id="af0075">Université de Montpellier, IES, UMR 5214, CNRS-UM, Montpellier, France</nlm:aff></affiliation></author><author><name sortKey="Buchy, Philippe" sort="Buchy, Philippe" uniqKey="Buchy P" first="Philippe" last="Buchy">Philippe Buchy</name><affiliation><nlm:aff id="af0005">Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</nlm:aff></affiliation><affiliation><nlm:aff id="af0080">GSK Vaccines R&D, 150 Beach road, # 22-00, 189720, Singapore</nlm:aff></affiliation></author></analytic><series><title level="j">Infection, Genetics and Evolution</title><idno type="ISSN">1567-1348</idno><idno type="eISSN">1567-7257</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>South-East Asia is a hot spot for emerging zoonotic diseases, and bats have been recognized as hosts for a large number of zoonotic viruses such as Severe Acute Respiratory Syndrome (SARS), responsible for acute respiratory syndrome outbreaks. Thus, it is important to expand our knowledge of the presence of viruses in bats which could represent a risk to humans. Coronaviruses (CoVs) have been reported in bat species from Thailand, China, Indonesia, Taiwan and the Philippines. However no such work was conducted in Cambodia or Lao PDR. Between 2010 and 2013, 1965 bats were therefore sampled at interfaces with human populations in these two countries. They were tested for the presence of coronavirus by consensus reverse transcription-PCR assay. A total of 93 samples (4.7%) from 17 genera of bats tested positive. Sequence analysis revealed the presence of potentially 37 and 56 coronavirus belonging to alpha-coronavirus (αCoV) and beta-CoV (βCoV), respectively. The βCoVs group is known to include some coronaviruses highly pathogenic to human, such as SARS-CoV and MERS-CoV. All coronavirus sequences generated from frugivorous bats (family <italic>Pteropodidae</italic>) (<italic>n</italic> = 55) clustered with other bat βCoVs of lineage D, whereas one coronavirus from <italic>Pipistrellus coromandra</italic> fell in the lineage C of βCoVs which also includes the MERS-CoV. αCoVs were all detected in various genera of insectivorous bats and clustered with diverse bat αCoV sequences previously published. A closely related strain of PEDV, responsible for severe diarrhea in pigs (PEDV-CoV), was detected in 2 <italic>Myotis</italic> bats. We highlighted the presence and the high diversity of coronaviruses circulating in bats from Cambodia and Lao PDR. Three new bat genera and species were newly identified as host of coronaviruses, namely <italic>Macroglossus</italic> sp., <italic>Megaerops niphanae</italic> and <italic>Myotis horsfieldii</italic></p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Alsahafi, A J" uniqKey="Alsahafi A">A.J. Alsahafi</name></author><author><name sortKey="Cheng, A C" uniqKey="Cheng A">A.C. Cheng</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Amengual, B" uniqKey="Amengual B">B. Amengual</name></author><author><name sortKey="Bourhy, H" uniqKey="Bourhy H">H. Bourhy</name></author><author><name sortKey="L Pez Roig, M" uniqKey="L Pez Roig M">M. López-Roig</name></author><author><name sortKey="Serra Cobo, J" uniqKey="Serra Cobo J">J. Serra-Cobo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Amman, B R" uniqKey="Amman B">B.R. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Infect Genet Evol</journal-id><journal-id journal-id-type="iso-abbrev">Infect. Genet. Evol</journal-id><journal-title-group><journal-title>Infection, Genetics and Evolution</journal-title></journal-title-group><issn pub-type="ppub">1567-1348</issn><issn pub-type="epub">1567-7257</issn><publisher><publisher-name>Elsevier B.V.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27932284</article-id><article-id pub-id-type="pmc">7106194</article-id><article-id pub-id-type="publisher-id">S1567-1348(16)30513-5</article-id><article-id pub-id-type="doi">10.1016/j.meegid.2016.11.029</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Genetic diversity of coronaviruses in bats in Lao PDR and Cambodia</article-title></title-group><contrib-group><contrib contrib-type="author" id="au0005"><name><surname>Lacroix</surname><given-names>Audrey</given-names></name><xref rid="af0005" ref-type="aff">a</xref></contrib><contrib contrib-type="author" id="au0010"><name><surname>Duong</surname><given-names>Veasna</given-names></name><xref rid="af0005" ref-type="aff">a</xref></contrib><contrib contrib-type="author" id="au0015"><name><surname>Hul</surname><given-names>Vibol</given-names></name><xref rid="af0005" ref-type="aff">a</xref></contrib><contrib contrib-type="author" id="au0020"><name><surname>San</surname><given-names>Sorn</given-names></name><xref rid="af0010" ref-type="aff">b</xref></contrib><contrib contrib-type="author" id="au0025"><name><surname>Davun</surname><given-names>Hull</given-names></name><xref rid="af0010" ref-type="aff">b</xref></contrib><contrib contrib-type="author" id="au0030"><name><surname>Omaliss</surname><given-names>Keo</given-names></name><xref rid="af0015" ref-type="aff">c</xref></contrib><contrib contrib-type="author" id="au0035"><name><surname>Chea</surname><given-names>Sokha</given-names></name><xref rid="af0020" ref-type="aff">d</xref></contrib><contrib contrib-type="author" id="au0040"><name><surname>Hassanin</surname><given-names>Alexandre</given-names></name><xref rid="af0025" ref-type="aff">e</xref></contrib><contrib contrib-type="author" id="au0045"><name><surname>Theppangna</surname><given-names>Watthana</given-names></name><xref rid="af0030" ref-type="aff">f</xref></contrib><contrib contrib-type="author" id="au0050"><name><surname>Silithammavong</surname><given-names>Soubanh</given-names></name><xref rid="af0035" ref-type="aff">g</xref><xref rid="af0040" ref-type="aff">h</xref></contrib><contrib contrib-type="author" id="au0055"><name><surname>Khammavong</surname><given-names>Kongsy</given-names></name><xref rid="af0035" ref-type="aff">g</xref></contrib><contrib contrib-type="author" id="au0060"><name><surname>Singhalath</surname><given-names>Sinpakone</given-names></name><xref rid="af0035" ref-type="aff">g</xref></contrib><contrib contrib-type="author" id="au0065"><name><surname>Greatorex</surname><given-names>Zoe</given-names></name><xref rid="af0035" ref-type="aff">g</xref></contrib><contrib contrib-type="author" id="au0070"><name><surname>Fine</surname><given-names>Amanda E.</given-names></name><xref rid="af0045" ref-type="aff">i</xref></contrib><contrib contrib-type="author" id="au0075"><name><surname>Goldstein</surname><given-names>Tracey</given-names></name><xref rid="af0050" ref-type="aff">j</xref></contrib><contrib contrib-type="author" id="au0080"><name><surname>Olson</surname><given-names>Sarah</given-names></name><xref rid="af0055" ref-type="aff">k</xref></contrib><contrib contrib-type="author" id="au0085"><name><surname>Joly</surname><given-names>Damien O.</given-names></name><xref rid="af0055" ref-type="aff">k</xref><xref rid="af0060" ref-type="aff">l</xref></contrib><contrib contrib-type="author" id="au0090"><name><surname>Keatts</surname><given-names>Lucy</given-names></name><xref rid="af0020" ref-type="aff">d</xref></contrib><contrib contrib-type="author" id="au0095"><name><surname>Dussart</surname><given-names>Philippe</given-names></name><xref rid="af0005" ref-type="aff">a</xref></contrib><contrib contrib-type="author" id="au0100"><name><surname>Afelt</surname><given-names>Aneta</given-names></name><xref rid="af0065" ref-type="aff">m</xref></contrib><contrib contrib-type="author" id="au0105"><name><surname>Frutos</surname><given-names>Roger</given-names></name><email>roger.frutos@ies.univ-montp2.fr</email><xref rid="af0070" ref-type="aff">n</xref><xref rid="af0075" ref-type="aff">o</xref><xref rid="cr0005" ref-type="corresp">⁎</xref></contrib><contrib contrib-type="author" id="au0110"><name><surname>Buchy</surname><given-names>Philippe</given-names></name><email>buchyphilippe@hotmail.com</email><xref rid="af0005" ref-type="aff">a</xref><xref rid="af0080" ref-type="aff">p</xref><xref rid="cr0010" ref-type="corresp">⁎⁎</xref></contrib></contrib-group><aff id="af0005"><label>a</label>Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia</aff><aff id="af0010"><label>b</label>National Veterinary Research Institute, Ministry of Agriculture Forestry and Fisheries, Cambodia</aff><aff id="af0015"><label>c</label>Forest Administration, Ministry of Agriculture Forestry and Fisheries, Cambodia</aff><aff id="af0020"><label>d</label>Wildlife Conservation Society, Cambodia</aff><aff id="af0025"><label>e</label>Muséum national d'Histoire naturelle, Institut de Systématique, Evolution, Biodiversité (ISYEB), UMR 7205 MNHN CNRS UPMC, France</aff><aff id="af0030"><label>f</label>National Animal Health Laboratory, Ministry of Agriculture Forestry and Fisheries, Lao Democratic People's Republic</aff><aff id="af0035"><label>g</label>Wildlife Conservation Society, Lao Democratic People's Republic</aff><aff id="af0040"><label>h</label>Metabiota Inc., Vientiane, Lao Democratic People's Republic</aff><aff id="af0045"><label>i</label>Wildlife Conservation Society, Vietnam Program, Hanoi, Vietnam</aff><aff id="af0050"><label>j</label>One Health Institute, School of Veterinary Medicine, University of California, Davis, USA</aff><aff id="af0055"><label>k</label>Wildlife Conservation Society, Wildlife Health Program, Bronx, New York, USA</aff><aff id="af0060"><label>l</label>Metabiota Inc., Nanaimo, British Columbia, Canada</aff><aff id="af0065"><label>m</label>Institute of Physical Geography, Faculty of Geography and Regional Studies, University of Warsaw, Warsaw, Poland</aff><aff id="af0070"><label>n</label>Cirad, UMR 17, Cirad-Ird, TA-A17/G, Montpellier, France</aff><aff id="af0075"><label>o</label>Université de Montpellier, IES, UMR 5214, CNRS-UM, Montpellier, France</aff><aff id="af0080"><label>p</label>GSK Vaccines R&D, 150 Beach road, # 22-00, 189720, Singapore</aff><author-notes><corresp id="cr0005"><label>⁎</label>Correspondence to: R. Frutos, Cirad, UMR 17, Cirad-Ird, TA-A17/G, Montpellier, France. <email>roger.frutos@ies.univ-montp2.fr</email></corresp><corresp id="cr0010"><label>⁎⁎</label>Correspondence to: P. Buchy, Institut Pasteur du Cambodge, Virology Unit, Phnom Penh, Cambodia. <email>buchyphilippe@hotmail.com</email></corresp></author-notes><pub-date pub-type="pmc-release"><day>6</day><month>12</month><year>2016</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>3</month><year>2017</year></pub-date><pub-date pub-type="epub"><day>6</day><month>12</month><year>2016</year></pub-date><volume>48</volume><fpage>10</fpage><lpage>18</lpage><history><date date-type="received"><day>1</day><month>8</month><year>2016</year></date><date date-type="rev-recd"><day>26</day><month>11</month><year>2016</year></date><date date-type="accepted"><day>26</day><month>11</month><year>2016</year></date></history><permissions><copyright-statement>© 2016 Elsevier B.V. All rights reserved.</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Elsevier B.V.</copyright-holder><license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p></license></permissions><abstract id="ab0005"><p>South-East Asia is a hot spot for emerging zoonotic diseases, and bats have been recognized as hosts for a large number of zoonotic viruses such as Severe Acute Respiratory Syndrome (SARS), responsible for acute respiratory syndrome outbreaks. Thus, it is important to expand our knowledge of the presence of viruses in bats which could represent a risk to humans. Coronaviruses (CoVs) have been reported in bat species from Thailand, China, Indonesia, Taiwan and the Philippines. However no such work was conducted in Cambodia or Lao PDR. Between 2010 and 2013, 1965 bats were therefore sampled at interfaces with human populations in these two countries. They were tested for the presence of coronavirus by consensus reverse transcription-PCR assay. A total of 93 samples (4.7%) from 17 genera of bats tested positive. Sequence analysis revealed the presence of potentially 37 and 56 coronavirus belonging to alpha-coronavirus (αCoV) and beta-CoV (βCoV), respectively. The βCoVs group is known to include some coronaviruses highly pathogenic to human, such as SARS-CoV and MERS-CoV. All coronavirus sequences generated from frugivorous bats (family <italic>Pteropodidae</italic>) (<italic>n</italic> = 55) clustered with other bat βCoVs of lineage D, whereas one coronavirus from <italic>Pipistrellus coromandra</italic> fell in the lineage C of βCoVs which also includes the MERS-CoV. αCoVs were all detected in various genera of insectivorous bats and clustered with diverse bat αCoV sequences previously published. A closely related strain of PEDV, responsible for severe diarrhea in pigs (PEDV-CoV), was detected in 2 <italic>Myotis</italic> bats. We highlighted the presence and the high diversity of coronaviruses circulating in bats from Cambodia and Lao PDR. Three new bat genera and species were newly identified as host of coronaviruses, namely <italic>Macroglossus</italic> sp., <italic>Megaerops niphanae</italic> and <italic>Myotis horsfieldii</italic></p></abstract><abstract abstract-type="graphical" id="ab0010"><title>Graphical abstract</title><p><fig id="f0015" position="anchor"><alt-text id="al0025">Image 1</alt-text><graphic xlink:href="fx1_lrg"></graphic></fig></p></abstract><abstract abstract-type="author-highlights" id="ab0015"><title>Highlights</title><p><list list-type="simple" id="l0005"><list-item id="li0005"><label>•</label><p id="p0005">Coronaviruses detected in bats from Lao PDR and Cambodia.</p></list-item><list-item id="li0010"><label>•</label><p id="p0010">High diversity of αCoVs and βCoVs circulating in bats in Cambodia and Lao PDR.</p></list-item><list-item id="li0015"><label>•</label><p id="p0015">One strain of βCoV, a new member of the MERS-CoV sister-clade, detected from <italic>Pipistrellus coromandra</italic>.</p></list-item><list-item id="li0020"><label>•</label><p id="p0020">A αCoV strain genetically related to PEDV-CoV, detected from <italic>Myotis horsfieldii</italic>.</p></list-item><list-item id="li0025"><label>•</label><p id="p0025">CoVs detected for the first time in <italic>Megaerops niphanae</italic>, <italic>Myotis horsfieldii</italic> and <italic>Macroglossus</italic> sp.</p></list-item></list></p></abstract><kwd-group id="ks0005"><title>Keywords</title><kwd>Coronaviruses</kwd><kwd>Bats</kwd><kwd>Genetic diversity</kwd><kwd>Cambodia</kwd><kwd>Lao PDR</kwd></kwd-group></article-meta></front><body><sec id="s0005"><label>1</label><title>Introduction</title><p id="p0030">Coronaviruses (CoVs) are enveloped, single stranded positive-sense RNA viruses displaying a large genome of 26 kb to 32 kb (<xref rid="bb0230" ref-type="bibr">Masters, 2006</xref>). They are classified within 4 groups based on genotype and serological characteristics: <italic>Alphacoronaviruses</italic> (αCoVs), <italic>Betacoronaviruses</italic> (βCoVs), <italic>Gammacoronaviruses</italic>, and the recently created group of the <italic>Deltacoronaviruses</italic> (<xref rid="bb0410" ref-type="bibr">Woo et al., 2009</xref>, <xref rid="bb0415" ref-type="bibr">Woo et al., 2012</xref>). Their host range is very wide and includes both mammalian and avian species. Coronaviruses can cause acute and chronic respiratory, enteric, neurological and hepatic diseases in their hosts (<xref rid="bb0395" ref-type="bibr">Weiss and Navas-Martin, 2005</xref>). Coronaviruses of animal origin were responsible for the Severe Acute Respiratory Syndrome (SARS) outbreak in 2003–2004, which was associated with deaths in Hong Kong, China, South East Asia and North America (<xref rid="bb0070" ref-type="bibr">Centers for Disease Control and Prevention (CDC), 2003</xref>; <xref rid="bb0280" ref-type="bibr">Peiris et al., 2003</xref>) and the current epidemics of MERS in the Arabian Peninsula (<xref rid="bb0005" ref-type="bibr">Alsahafi and Cheng, 2016</xref>) and Korea (<xref rid="bb0080" ref-type="bibr">Choi, 2015</xref>).</p><p id="p0035">Bats have been identified as natural reservoirs for several zoonotic viruses, such as henipaviruses (<xref rid="bb0440" ref-type="bibr">Young et al., 1996</xref>, <xref rid="bb0095" ref-type="bibr">Chua et al., 2000</xref>, <xref rid="bb0145" ref-type="bibr">Halpin et al., 2000</xref>) lyssaviruses variants (<xref rid="bb0035" ref-type="bibr">Banyard et al., 2014</xref>) and Ebola virus (<xref rid="bb0215" ref-type="bibr">Leroy et al., 2005</xref>, <xref rid="bb0210" ref-type="bibr">Leroy et al., 2009</xref>). Bats have been identified as the natural host of the SARS-CoV, (<xref rid="bb0380" ref-type="bibr">Wang et al., 2006</xref>), and recently, the NeoCoV from the clade the Middle Eastern Respiratory Syndrome (MERS-CoV) was detected in a sub-Saharan bat (<italic>Neoromicia capensis</italic>) besides its camel host (<xref rid="bb0100" ref-type="bibr">Corman et al., 2014</xref>). A growing number of coronaviruses have been detected in bats since the SARS-CoV outbreak (<xref rid="bb0085" ref-type="bibr">Chu et al., 2006</xref>, <xref rid="bb0090" ref-type="bibr">Chu et al., 2008</xref>, <xref rid="bb0190" ref-type="bibr">Lau et al., 2007</xref>, <xref rid="bb0195" ref-type="bibr">Lau et al., 2010</xref>, <xref rid="bb0200" ref-type="bibr">Lau et al., 2012</xref>, <xref rid="bb0390" ref-type="bibr">Watanabe et al., 2010</xref>, <xref rid="bb0135" ref-type="bibr">Gouilh et al., 2011</xref>, <xref rid="bb0355" ref-type="bibr">Tsuda et al., 2012</xref>, <xref rid="bb0370" ref-type="bibr">Wacharapluesadee et al., 2013</xref>, <xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>, <xref rid="bb0020" ref-type="bibr">Anindita et al., 2015</xref>, <xref rid="bb0430" ref-type="bibr">Xu et al., 2016</xref>, <xref rid="bb0075" ref-type="bibr">Chen et al., 2016</xref>, <xref rid="bb0175" ref-type="bibr">Kim et al., 2016</xref>) including a high diversity of coronaviruses, recently detected in five Thai provinces neighboring Cambodia (<xref rid="bb0370" ref-type="bibr">Wacharapluesadee et al., 2013</xref>, <xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>).</p><p id="p0040">The order Chiroptera represents approximately 20% of all living mammal species (<xref rid="bb0345" ref-type="bibr">Teeling et al., 2005</xref>). Over 25% of the worlds bat diversity is found in South-East Asia, established in many natural, urban and suburban environments (<xref rid="bb0185" ref-type="bibr">Kingston, 2013</xref>). Seventy species of bats have been described so far in Cambodia whereas ninety species are known in Lao PDR, including <italic>Yangochiroptera</italic> and <italic>Yinpterochiroptera</italic> (<xref rid="bb0235" ref-type="bibr">Matveev, 2005</xref>, <xref rid="bb0305" ref-type="bibr">Sarak et al., 2013</xref>). Apart from Singapore, bats are hunted for food or preparation of traditional medicines and are found in food markets throughout South-East Asia, despite bats are protected by the law in these countries (<xref rid="bb0205" ref-type="bibr">Lee et al., 2014</xref>, <xref rid="bb0255" ref-type="bibr">Mildenstein et al., 2016</xref>). Bat farms, where artificial roosts are erected to facilitate bat guano harvest to serve as agricultural fertilizer, are becoming common in South-East Asia, including in Cambodia (<xref rid="bb0350" ref-type="bibr">Thi et al., 2014</xref>) In Thailand, coronaviruses belonging to the lineages B and C of betacoronaviruses were detected in bat guano (<xref rid="bb0135" ref-type="bibr">Gouilh et al., 2011</xref>, <xref rid="bb0370" ref-type="bibr">Wacharapluesadee et al., 2013</xref>). Moreover, several studies evidenced the presence of coronavirus belonging to the betacoronavirus group in close areas (<xref rid="bb4000" ref-type="bibr">He et al., 2014</xref>, <xref rid="bb0020" ref-type="bibr">Anindita et al., 2015</xref>, <xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>)</p><p id="p0045">Due to evolving land-use such as deforestation, infrastructure development, urban development, and agricultural expansion, bat populations are settling in areas closer to human dwellings (<xref rid="bb0165" ref-type="bibr">Jung and Threlfall, 2016</xref>), increasing the likelihood of contact between bats and humans. Socio-economic-driven changes of the environment are also impacting the bats and thus may affect virus biodiversity (<xref rid="bb0225" ref-type="bibr">Looi and Chua, 2007</xref>, <xref rid="bb0360" ref-type="bibr">Turmelle and Olival, 2009</xref>, <xref rid="bb0055" ref-type="bibr">Brierley et al., 2016</xref>). These factors may also contribute to an increased occurrence of contacts between bats and humans, which in turn, may increase the potential transmission of zoonotic pathogens, including a coronaviruses. Despite the prolificacy of such interfaces in the region, so far no study has been conducted on bat coronaviruses in Cambodia and Lao PDR. To our knowledge, this is the first study to investigate the presence and the diversity of coronaviruses in bats in Cambodia and Lao PDR.</p></sec><sec id="s0010"><label>2</label><title>Materials and methods</title><sec id="s0015"><label>2.1</label><title>Ethics</title><p id="p0050">The study was approved by the National Veterinary Research Institute and Forest Administration department of the Ministry of Agriculture Forestry and Fisheries in Cambodia, as well as by the National Animal Health Laboratory of the Ministry of Agriculture Forestry and Fisheries, in Lao PDR, and under the Institutional Animal Care and Use Committee at the University of California, Davis (protocol number: 16048). Since Cambodia and Lao PDR have no ethic committee overseeing animal experimentation, animals were treated in compliance with the guidelines of the American Society of Mammalogists and within the framework of the European Union legislation guidelines (Directive 86/609/EEC).</p></sec><sec id="s0020"><label>2.2</label><title>Collection of bat samples</title><p id="p0055">Bat samples from various species were collected from different locations in Lao PDR and Cambodia, over a 3-year period (from November 2010 to December 2013). Bat species were identified to genus or species by trained biologists and veterinarians. The sampling was performed in two phases: Phase 1 was carried out in 2010 by the Institut Pasteur in Cambodia (IPC) and the <italic>Muséum national d'Histoire naturelle</italic> (MNHN; Paris, France) in cooperation with Cambodian government partners. Bats were captured and humanely euthanized in full compliance with local ethical and legal guidelines. The capture sites were located in Ratanakiri, Stung Treng and Preah Vihear provinces in Cambodia. They were chosen because of their easier accessibility to the collection team. Rectal swabs were stored in viral transport medium solution (VTM; containing tryptose phosphate Broth 2.95%, 145 mM of NaCl, 5% gelatin, 54 mM Amphotericin B, 106 U of penicillin-streptomycine per liter, 80 mg of gentamycine per liter [Sigma-Aldrich, Irvine, UK]). Tissue specimens (<italic>i.e.</italic> lung, liver, spleen, kidney, heart) were placed in separate cryotubes. All specimens were immediately transferred into liquid nitrogen containers before being transported to the Institut Pasteur laboratory where they were stored at − 80 °C prior to testing. The second sampling phase was performed by the Wildlife Conservation Society (WCS) from 2011 to 2013. During this phase 2, no animals were killed and samples were collected at four key interfaces for increased contact (and potential disease transmission) between bats and humans: fresh-food markets; freshly hunted in rural communities for subsistence or sale; wild meat restaurants; and bat guano farms. In Lao PDR the majority of samples were obtained from freshly dead bats found in food markets, with a small number collected from bats captured by subsistence hunters; in Cambodia the majority of samples were collected at wild meat restaurants where bats were butchered, prepared and served, with additional samples obtained from freshly trapped bats (live and dead) held by hunters and middle-men in rural communities, and at a bat guano farm. In this study, sterile swabs were used to collect freshly voided fecal samples from tarpaulins placed under the guano farm roosts. Rectal and oral swabs and tissue samples were also collected from individual animals that had died of natural causes and were found fresh beneath bat guano farm roosts. Oral and rectal swabs were collected opportunistically from fresh dead and live bats at the market, hunting and restaurant locations. Swab and tissue samples were placed in separate cryovials in VTM and immediately stored on liquid nitrogen in dewars for transport to the laboratory where they were stored in − 80 °C freezers until testing.</p></sec><sec id="s0025"><label>2.3</label><title>RNA extraction and nested-RT-PCR</title><p id="p0060">Viral RNA was extracted using the QIAamp Viral RNA Mini Kit (Qiagen, Hilden, Germany) according to the supplier's instructions. Reverse transcription (RT) was performed using SuperScript III (Invitrogen, San Diego, CA). The PCR mixture (final volume: 25 μl) contained 2 μl of cDNA, PCR buffer (50 mM Tris-HCl (pH 9.0); 50 mM NaCl; 5 mM MgCl2), 200 μM (each) deoxynucleoside triphosphates (dNTPs), 20 pmol of each primer targeting the RdRp gene (adapted from <xref rid="bb0390" ref-type="bibr">Watanabe et al., 2010</xref>) (<xref rid="t0005" ref-type="table">Table 1</xref>), and 1 U of HOT FIREPol® DNA Polymerase (Solis BioDyne, Tartu, Estonia). The PCR mixture was incubated at 95 °C for 12 min, followed by 35 cycles at 95 °C for 30 s, 50 °C for 30 s, and 72 °C for 1 min, and by a final extension at 72 °C for 5 min. A nested PCR amplification using forward primer CoV-Fwd2 and the same reverse primer, was performed on 1 μl of the primary PCR products, using the same amplification conditions. The amplification of sequences specific to CoVs was attested by the visualization of a 440 bp and a 434 bp fragment after the first and second PCR round, respectively. To limit the risk of contamination, RNA extraction, reverse transcription-PCR (RT-PCR), nested-PCR and gel electrophoresis were carried out in separate rooms. In addition, negative controls (water) were included in each run of the nested-RT-PCR assay and results were validated only if these controls tested negative while the positive controls (plasmids prepared by cloning the gene of interest) had to test positive. Amplification of longer fragments of the RdRp gene (<italic>i.e.</italic> 1370 bp) was performed on cDNA of 38 positive samples, by a nested RT-PCR using gene-specific primers designed by multiple alignments of known CoV sequences from the same clusters. Amplified product were sequenced in both directions by direct Sanger sequencing in commercial facilities (Macrogen, Inc., Seoul, Korea). Sequence data were deposited in GenBank and accession numbers ranging from KX284902 to KX520662 and KY010629 to KY010666 are provided in <xref rid="ec0015" ref-type="supplementary-material">Supplementary Table 1</xref>. Since many coronaviruses from different bat genera were detected, and for the sake of clarity, a short name of the strain, the sample code, and the host classification were abbreviated to be used in the sequence nomenclature (<xref rid="ec0020" ref-type="supplementary-material">Supplementary Table 2</xref>). For example, the sequence “Bat coronavirus 512/2005/PREDICT-KHP13-PTR1-0109”, corresponding to the Bat coronavirus 512/2005 strain (BatCoV-512), detected in the sample KHP13-PTR1-0109 (P109), from a <italic>Scotophilus kuhlii</italic> (Sku) was abbreviated as: BatCoV-512_P109_Sku. The abbreviations used to code the bat classification, are listed in the <xref rid="ec0020" ref-type="supplementary-material">Supplementary Table 2</xref>.<table-wrap position="float" id="t0005"><label>Table 1</label><caption><p>Primers used for the detection of CoVs.</p></caption><alt-text id="al0015">Table 1</alt-text><table frame="hsides" rules="groups"><thead><tr><th>Gene</th><th>Round</th><th>Primer name</th><th>Sequence 5′-3′</th></tr></thead><tbody><tr><td>RdRp</td><td>1st</td><td>CoV-Fwd1</td><td>GGTTGGGAYTAYCCHAARTGTGA</td></tr><tr><td>RdRp</td><td>1st and 2nd</td><td>CoV-Rvs2</td><td>CCATCATCASWYRAATCATCATA</td></tr><tr><td>RdRp</td><td>2nd</td><td>CoV-Fwd2</td><td>GAYTAYCCHAARTGTGAYAGAGC</td></tr></tbody></table></table-wrap></p></sec><sec id="s0030"><label>2.4</label><title>Sequence analysis</title><p id="p0070">Sequences were assembled and analyzed using CLC Genomics Workbench version 3.6.1 and BioEdit, version 7.0.9.1. Sequences were aligned with a representative set of CoV sequences retrieved from GenBank using Seaview, version 4.5.4 (<xref rid="bb0140" ref-type="bibr">Gouy et al., 2010</xref>). Phylogenetic trees based on RNA sequences were constructed using the Maximum Likelihood method with the GTR + G + I model and bootstrap values (BP) were calculated after 1000 replicates. The best evolutionary model was determined using MEGA version 6.06. Trees displaying protein sequences were constructed using the neighbor joining method and bootstrap values were calculated after 1000 replicates. Phylogenetic and molecular evolutionary analyses were conducted using Seaview version 4.5.4.</p></sec><sec id="s0035"><label>2.5</label><title>Geographic data</title><p id="p0075">Land cover data was obtained from GlobeLand30 service operated by the <xref rid="bb3000" ref-type="bibr">National Geomatics Center of China (NGCC, 2014)</xref>. Initial data was produced in 2010 with an update in 2014. Images used for GlobeLand30 (GLC30) classification were multispectral images with a 30-meter resolution. Six classes of land cover were considered: cropland, forest, grassland, wetland, water bodies and human settlement area. Land cover structure for each sampling location of sampling is described in <xref rid="ec0025" ref-type="supplementary-material">Supplementary Table 3</xref>. Data mapping was conducted with Quantum GIS, version 2.8.2.</p></sec></sec><sec id="s0040"><label>3</label><title>Results</title><sec id="s0045"><label>3.1</label><title>Sampling location, land cover use and hosts</title><p id="p0085">A total of 1965 bats were sampled in 44 locations from nine provinces in Cambodia and eight provinces in Lao PDR (<xref rid="ec0005" ref-type="supplementary-material">Supplementary Fig. 1</xref>). The characteristics of the environments around sampling site are described in <xref rid="ec0025" ref-type="supplementary-material">Supplementary Table 3</xref>. Bats originating from 5 districts (<italic>i.e.</italic> Kasi and Vang Vieng districts in Lao PDR and Choam Khsant, Kean Svay, and Moung Russei districts in Cambodia) represented 60% of all the bats collected. Sampled bats were wild, live captured during phase 1 (<italic>n</italic> = 322), where as in phase 2 (<italic>n</italic> = 1643) they were: hunted by villagers for local consumption (<italic>n</italic> = 455); for sale in markets (<italic>n</italic> = 791); being butchered and prepared for sale at wild meat restaurants (<italic>n</italic> = 392) or on a bat guano farm (<italic>n</italic> = 5) (<xref rid="ec0025" ref-type="supplementary-material">Supplementary Table 3</xref>). Apart from bats trapped during phase 1 or animals sampled on the guano farm (site reference C6) during phase 2, the exact location where the animals were captured remained imprecise. However, the chiroptera were always captured by hunters in areas close to the location where the animals were sampled, <italic>i.e.</italic> mostly in areas at the border of deep forests, in mixed agricultural zones with sparse forests, in suburban zones close to sparse forest, in naturals protected forest areas, in places close to water surfaces or in limestone karst areas with mountain forests (<xref rid="ec0005" ref-type="supplementary-material">Supplementary Fig. 1</xref>, <xref rid="ec0025" ref-type="supplementary-material">Supplementary Table 3</xref>). Landscape analysis around each sampling location led to a typology comprising four main groups of land cover composition (<xref rid="ec0025" ref-type="supplementary-material">Supplementary Table 3</xref>, <xref rid="ec0005" ref-type="supplementary-material">Supplementary Fig. 1</xref>): 1) Deep forest area, well isolated from human settlements (sites: C3, C25, C29, C30, C32, C33, C34, C41, C42 and C43), 2) Isolated pockets of croplands surrounded by forest, very often forest is under fragmentation (sites: C2, C12, C16, C18, C19, C21, C22, C23, C24, C26, C27, C28, C30, C35, C36, C37, C38, C40 and C44), 3) Forest edge, mixed agricultural zones with sparse forests (sites: C5, C7, C13 and C14) and 4) typically agricultural zones, villages and suburban zones, often close to highly fragmented forests (sites: C1, C4, C6, C8, C9, C10, C11 and C20). For sites C1, C4, C6, C8 and C9 a key parameters was the presence of wetlands in the immediate vicinity.</p></sec><sec id="s0050"><label>3.2</label><title>Detection of coronaviruses</title><p id="p0095">Coronavirus RNA was detected in 93 bats (4.7%) out of 1965 animals tested. Coronavirus RNA was detected in 21 of the 44 sites with detection rates varying depending upon sites (<xref rid="t0010" ref-type="table">Table 2</xref>). However, it is not possible to run an in depth statistical analysis owing to the fact that sampling was not developed for that purpose and data are therefore biased. Detailed data are presented in <xref rid="ec0025" ref-type="supplementary-material">Supplementary Table 3</xref>. Nevertheless, in highly transformed areas (mostly croplands and urbanized areas), bat biodiversity was lower while the detection rate of coronavirus was higher (<xref rid="t0010" ref-type="table">Table 2</xref>, <xref rid="ec0025" ref-type="supplementary-material">Supplementary Table 3</xref>). The phylogenetic analysis based on 320-bp nucleotides of the 93 sample sequences and 34 reference sequences from GenBank indicated that 37 sequences belonged to the αCoV genus while the 56 others fell into the βCoV genus (<xref rid="f0005" ref-type="fig">Fig. 1</xref>). Out of the 56 bat-βCoVs, 55 belonged to the lineage D. The remaining strain detected (PREDICT-CoV-34_GT1-3_Pisp) belonged to the lineage C which comprises MERS-CoV and MERS-CoV-related viruses. The 55 lineage D bat-βCoVs clustered into four subclusters (D1, D2, D3 and D4) out of the five subclusters identified in this group D (<xref rid="f0005" ref-type="fig">Fig. 1</xref>). The subcluster D1 (BP = 100) comprised 7 different βCoVs, 2 sequences detected in pteropodid bats from Lao PDR and 5 from Cambodia. The subcluster D2 (BP = 80), contained 17 βCoVs detected from the Cambodian provinces of Preah Vihear, Stung Treng and Battambang. The subcluster D3 (BP = 45) contained 24 bat-βCoVs, which were mostly obtained from animals in Lao PDR (<italic>n</italic> = 22) while only 2 were detected in bats from Cambodia. The subcluster D4 comprised the remaining bat-βCoVs (BP = 78), detected in bats from Lao PDR only. Bat-αCoVs were unevenly distributed within three subclusters (<xref rid="f0005" ref-type="fig">Fig. 1</xref>). The αCoV subcluster 1 included 32 sequences from Cambodian bats. The αCoV subcluster 2 included two αCoVs from Cambodia, while the αCoV subcluster 4 cluster contained one sequence from Cambodia and two from Lao PDR. The same phylogenetic clustering was seen with analyses using the amino-acid sequences. A similar topology was obtained when analyzing the protein sequence (<xref rid="f0020" ref-type="graphic">Supplementary Fig. 2</xref>). The phylogenetic analysis based on 38 longer sequences of 1370 bp (<xref rid="f0010" ref-type="fig">Fig. 2</xref>) and the corresponding 454 amino acid sequence (<xref rid="f0025" ref-type="graphic">Supplementary Fig. 3</xref>) confirmed the tree topology described on shorter sequences in <xref rid="f0005" ref-type="fig">Fig. 1</xref> and <xref rid="f0020" ref-type="graphic">Supplementary Fig. 2</xref>, respectively. Coronavirus RNA was detected in bats belonged to 10 distinct genera. The proportion of CoVs-positive bats significantly varied depending upon the bat genus (Pearson's Chi<sup>2</sup>, <italic>p</italic> < 0.0001). The highest detection rates were found for the long-tongue fruit bats (<italic>Macroglossus</italic> sp.: 20%), the nectar cave bat (<italic>Eonycteris spelaea</italic>: 11.2%) and the lesser Asian bat (<italic>Scotophilus</italic> sp.: 9.3%). The 37 αCoV-positive bats belonged to five genera of the <italic>Yangochiroptera</italic> suborder, <italic>i.e. Rhinolophus</italic> (<italic>n</italic> = 1), <italic>Myotis</italic> (<italic>n</italic> = 2), <italic>Scotophilus</italic> (<italic>n</italic> = 31), <italic>Pipistrellus</italic> (<italic>n</italic> = 1) and <italic>Hipposideros</italic> (<italic>n</italic> = 2). A total of 56 animal tested positive for a βCoV, out of which 55 belonged to five genera of <italic>Yinpterochiroptera</italic> suborder, family <italic>Pteropodidae</italic>: <italic>i.e. Rousettus</italic> (<italic>n</italic> = 25), <italic>Cynopterus</italic> (<italic>n</italic> = 15), <italic>Eonycteris</italic> (<italic>n</italic> = 10), <italic>Macroglossus</italic> (<italic>n</italic> = 4), <italic>Megaerops</italic> (<italic>n</italic> = 1) whereas the bat infected by the PREDICT-CoV-34 strain was a <italic>Yangochiroptera</italic> of the genus <italic>Pipistrellus</italic> (<xref rid="f0010" ref-type="fig">Fig. 2</xref>). All αCoV RNA were detected in insectivorous bats while most of the βCoV RNA were detected in fruit bats.<table-wrap position="float" id="t0010"><label>Table 2</label><caption><p>Detection rates of coronavirus RNA in bats and geographical origin of the positive animals.</p></caption><alt-text id="al0020">Table 2</alt-text><table frame="hsides" rules="groups"><thead><tr><th rowspan="2">Bat</th><th rowspan="4">Total no. of samples (percentage (%) of positive)</th><th colspan="3">Origin of positive samples<xref rid="tf0005" ref-type="table-fn">a</xref><break></break>No. of samples (no. of positive)<hr></hr></th><th rowspan="4">Cambodia<break></break>No. of samples (no. of positive)</th><th rowspan="4">Site</th><th rowspan="4">Lao PDR<break></break>No. of samples (no. of positive)</th><th rowspan="4">Site</th></tr><tr><th rowspan="3">H</th><th rowspan="3">W</th><th rowspan="3">G</th></tr><tr><th>F/family</th></tr><tr><th>Genus or species</th></tr></thead><tbody><tr><td><bold><italic>Emballonuridae</italic></bold></td><td><bold>148 (0)</bold></td><td></td><td></td><td></td><td><bold>148 (0)</bold></td><td></td><td><bold>0 (0)</bold></td><td></td></tr><tr><td><italic>Taphozous</italic> sp.</td><td>148 (0)</td><td>118 (0)</td><td>30 (0)-</td><td>–</td><td>148 (0)</td><td>C9, C1, C32, C33</td><td>0 (0)</td><td></td></tr><tr><td><bold><italic>Hipposideridae</italic></bold></td><td><bold>62 (3.2)</bold></td><td></td><td></td><td></td><td><bold>4 (0)</bold></td><td></td><td><bold>58 (2)</bold></td><td></td></tr><tr><td><italic>Aselliscus</italic> sp.</td><td>7 (0)</td><td>7 (0)</td><td>–</td><td>–</td><td>0 (0)</td><td></td><td>7 (0)</td><td>C25</td></tr><tr><td><italic>Hipposideros</italic> sp.</td><td>55 (3.6)</td><td>51 (2)</td><td>4 (0)</td><td>–</td><td>4 (0)</td><td>C31, C33</td><td>51 (2)</td><td>C19, <bold>C14(+)</bold>, C21, C23, C24</td></tr><tr><td><bold><italic>Megadermatidae</italic></bold></td><td><bold>21 (0)</bold></td><td></td><td></td><td></td><td><bold>21 (0)</bold></td><td></td><td><bold>0 (0)</bold></td><td></td></tr><tr><td><italic>Megaderma</italic> sp.</td><td>21 (0)</td><td>–</td><td>21 (0)</td><td>–</td><td>21 (0)</td><td>C32, C33, C41</td><td>0 (0)</td><td></td></tr><tr><td><bold><italic>Pteropodidae</italic></bold></td><td><bold>1124 (4.9)</bold></td><td></td><td></td><td></td><td><bold>416 (25)</bold></td><td></td><td><bold>708 (30)</bold></td><td></td></tr><tr><td><italic>Cynopterus</italic> sp.</td><td>341 (4.4)</td><td>183 (8)</td><td>158 (7)</td><td>–</td><td>318 (15)</td><td><bold>C5(+),</bold> C7, <bold>C10(+)</bold>, <bold>C12(+),</bold> C11, C29, C30, <bold>C32(+)</bold>, C34, C35, C36, <bold>C37(+)</bold>, <bold>C38(+), C39(+)</bold>, C40, C41, C42, C44</td><td>23 (0)</td><td>C21, C23, C24, C26, C27, C28</td></tr><tr><td><italic>Eonycteris spelaea</italic></td><td>89 (11.2)</td><td>61 (6)</td><td>28 (4)</td><td>–</td><td>28 (4)</td><td><bold>C37(+), C38(+), C39(+),</bold> C40</td><td>61 (6)</td><td>16, <bold>C21(+), C23(+), C24(+)</bold></td></tr><tr><td><italic>Macroglossus</italic> sp.</td><td>28 (14.3)</td><td>28 (4)</td><td>–</td><td>–</td><td>21 (4)</td><td>C7<bold>, C10(+)</bold></td><td>7 (0)</td><td>C21, C24</td></tr><tr><td><italic>Megaerops niphanae</italic></td><td>130 (0.8)</td><td>122 (1)</td><td>8 (0)</td><td>–</td><td>16 (1)</td><td>C5, C7, C29, C30, C34, C39</td><td>114 (0)</td><td>C13, C14, C15, C16, C20 C21 C23, C24, C26, C27</td></tr><tr><td><italic>Megaerops</italic> sp.</td><td>12 (0)</td><td>–</td><td>12 (0)</td><td>–</td><td>12 (0)</td><td>C36, C37</td><td>0 (0)</td><td></td></tr><tr><td><italic>Pteropus</italic> sp.</td><td>10 (0)</td><td>10 (0)</td><td>–</td><td>–</td><td>10 (0)</td><td>C11</td><td>0 (0)</td><td></td></tr><tr><td><italic>Rousettus</italic> sp.</td><td>514 (4.9)</td><td>506 (24)</td><td>8 (1)</td><td>–</td><td>11(1)</td><td>C10, C11, <bold>C33(+)</bold>, C34, C37</td><td>503 (24)</td><td>C14, <bold>C15(+)</bold>, <bold>C16(+),</bold> C17, C20, <bold>C21(+),</bold> C22, <bold>C23(+)</bold>, <bold>24(+)</bold></td></tr><tr><td><bold><italic>Rhinolophidae</italic></bold></td><td><bold>154 (0.7)</bold></td><td></td><td></td><td></td><td><bold>52 (1)</bold></td><td></td><td><bold>102 (0)</bold></td><td></td></tr><tr><td><italic>Rhinolophus</italic> sp.</td><td>154(0.7)</td><td>102 (0)</td><td>52 (1)</td><td>–</td><td>52 (1)</td><td>C31, <bold>C33(+)</bold>, C37, C41, C42, C43</td><td>102 (0)</td><td>C14, C21, C23, C25</td></tr><tr><td><bold><italic>Vespertilionidae</italic></bold></td><td><bold>456 (7.7)</bold></td><td></td><td></td><td></td><td><bold>418 (35)</bold></td><td></td><td><bold>38 (0)</bold></td><td></td></tr><tr><td><italic>Harpiocephalus</italic> sp.</td><td>1 (0)</td><td>1 (0)</td><td>–</td><td>–</td><td>0 (0)</td><td></td><td>1 (0)</td><td>C20</td></tr><tr><td><italic>Ia io</italic></td><td>32 (0)</td><td>32 (0)</td><td>–</td><td>–</td><td>0 (0)</td><td></td><td>32 (0)</td><td>C18</td></tr><tr><td><italic>Myotis horsfieldii</italic></td><td>50 (4)</td><td>50 (2)</td><td>–</td><td>–</td><td>50 (2)</td><td><bold>C4</bold>(+)</td><td>0 (0)</td><td></td></tr><tr><td><italic>Myotis ricketti</italic></td><td>5 (0)</td><td>5 (0)</td><td>–</td><td>–</td><td>0 (0)</td><td></td><td>5 (0)</td><td>C20</td></tr><tr><td><italic>Pipistrellus coromandra</italic></td><td>29 (6.9)</td><td>29 (2)</td><td>–</td><td>–</td><td>29 (2)</td><td><bold>C2(+), C3(+)</bold></td><td>0 (0)</td><td></td></tr><tr><td><italic>Scotophilus</italic> sp.</td><td>338 (9.3)</td><td>333 (30)</td><td>–</td><td>5(1)</td><td>338 (31)</td><td><bold>C1(+), C6(+),</bold> C8, <bold>C9(+)</bold></td><td>0 (0)</td><td></td></tr><tr><td><italic>Tylonycteris</italic> sp.</td><td>1 (0)</td><td>–</td><td>1 (0)</td><td>–</td><td>1 (0)</td><td>C35</td><td>0 (0)</td><td></td></tr><tr><td>Total</td><td>1965 (4.7)</td><td>1638 (79)</td><td>322 (13)</td><td>5(1)</td><td>1059 (61)</td><td></td><td>906 (32)</td><td></td></tr></tbody></table><table-wrap-foot><fn id="sp0045"><p>Bat families are shown in bold.</p></fn><fn id="sp0050"><p>Sites where bats tested positive for coronavirus are in bold and marked with (+).</p></fn></table-wrap-foot><table-wrap-foot><fn id="tf0005"><label>a</label><p id="np0005">H: hunted bats, sold in markets of restaurants; W: wild bats, caught in their natural environment; G: bats collected in bat guano farms.</p></fn></table-wrap-foot></table-wrap><fig id="f0005"><label>Fig. 1</label><caption><p>Phylogenetic analysis of coronavirus sequences based on a 320 nucleotides fragment on the RdRp gene.</p><p>The tree was constructed using a Maximum Likelihood method with the GTR + G + I model. Bootstrap values (BP) were calculated after 1000 replicates. Tree is rooted to an avian coronavirus (FJ376622). The sequences detected in this study are shown with a bullet. Accession numbers related to the sequences are presented in <xref rid="ec0015" ref-type="supplementary-material">Supplementary Table 1</xref>.</p><p>The tree was constructed using a Maximum Likelihood method with the GTR + G + I model. Bootstrap values (BP) were calculated after 1000 replicates. Tree is rooted to an avian coronavirus (FJ376622). The sequences detected in this study are shown with a bullet. Accession numbers related to the sequences are presented in Supplementary Table 1.</p></caption><alt-text id="al0005">Fig. 1</alt-text><graphic xlink:href="gr1_lrg"></graphic></fig><fig id="f0010"><label>Fig. 2</label><caption><p>Sequence analysis of 1370 nucleic acid fragments of the RdRp gene of coronavirus sequences.</p><p>The tree was constructed using a Maximum Likelihood method with the GTR + G + I model. Boostrap values (BP) were calculated after 1000 replicates. Tree is rooted to an avian coronavirus (FJ376622). The sequences detected in this study are shown with a bullet. Accession numbers related to the sequences are presented in <xref rid="ec0015" ref-type="supplementary-material">Supplementary Table 1</xref>.</p><p>The tree was constructed using a Maximum Likelihood method with the GTR + G + I model. Boostrap values (BP) were calculated after 1000 replicates. Tree is rooted to an avian coronavirus (FJ376622). The sequences detected in this study are shown with a bullet. Accession numbers related to the sequences are presented in Supplementary Table 1.</p></caption><alt-text id="al0010">Fig. 2</alt-text><graphic xlink:href="gr2_lrg"></graphic></fig></p></sec><sec id="s0055"><label>3.3</label><title>Phylogenetic clustering of CoVs according to host and location</title><p id="p0105">1965 bats were from 17 different genera and 5 families. Eighty percent of the samples belonged to two bat families only, <italic>Vespertilionidae</italic> (<italic>n</italic> = 456) and <italic>Pteropodidae</italic> (<italic>n</italic> = 1124). In Lao PDR, 95.7% of the samples belonged to the <italic>Yinpterochiroptera</italic> suborder, including families <italic>Pteropodidae</italic> (78.1%), <italic>Hipposideridae</italic> (6.3%), and <italic>Rhinolophidae</italic> (11.3%) while only 4.3% were <italic>Yangochiroptera</italic> suborder from the family <italic>Vespertilionidae</italic>. In Cambodia, 35% of the bats collected belonged to suborder <italic>Yinpterochiroptera</italic>, and suborder <italic>Yangochiroptera</italic> accounted for the remainder of the collected samples (75%), including families <italic>Emballuronidae</italic> and <italic>Vespertilionidae</italic>. Only sequences from fruit bats from Cambodia and Lao PDR from the genera <italic>Rousettus</italic>, <italic>Eonycteris</italic>, <italic>Macroglossus</italic>, <italic>Cynopterus</italic> and <italic>Megaerops</italic> were found in the lineage D of βCoVs. Subcluster D1 contained two sequences from <italic>Macroglossus</italic> sp. from Cambodia (PREDICT-CoV-22 strains) and five virus sequences from <italic>Eonycteris spelaea</italic> from Lao PDR and Cambodia (PREDICT-CoV-22, R91, R77, R74, R58). Seventeen sequences were found in <italic>Cynopterus</italic> (PREDICT-CoV-24 strains, R96, R75, R72, R65, R59, R71), <italic>Rousettus</italic> sp. and <italic>Megaerops niphanae</italic> (PREDICT-CoV-24) collected in Preah Vihear and Battambang in 2010 and 2013, respectively. They fell into subcluster βCoV-D2 and displayed 98% to 100% of amino acid similarity with CoV sequences previously detected in <italic>Cynopterus sphinx</italic> and <italic>Hipposideros lekaguli</italic> in South East Thailand and China, respectively (<xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>, <xref rid="bb0430" ref-type="bibr">Xu et al., 2016</xref>). Similarly, the βCoV-D3 subcluster comprised 24 sequences found in <italic>Rousettus</italic>, <italic>Eonycteris</italic> and <italic>Macroglossus</italic> and CoVs previously identified in pteropodids from Hong Kong, Kenya, Thailand and Indonesia (genera <italic>Rousettus</italic> and <italic>Dobsonia</italic>) (<xref rid="bb0195" ref-type="bibr">Lau et al., 2010</xref>, <xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>, <xref rid="bb0020" ref-type="bibr">Anindita et al., 2015</xref>). They displayed 96.9% to 100% of amino acid identity. Seven sequences detected in <italic>Rousettus</italic> bats from Lao PDR and displaying 100% of amino acid identity, formed their own branch in subcluster D4. Additionally, the PREDICT-CoV-34 strain, detected in <italic>Pipistrellus coromandra</italic> fell into lineage C of βCoV (BP = 100) which contained sequence from MERS-CoV as well as sequences detected in <italic>Pipistrellus</italic> from Hong Kong, <italic>Neoromicia</italic> from South Africa and <italic>Myotis</italic> from China (<xref rid="bb0025" ref-type="bibr">Annan et al., 2013</xref>, <xref rid="bb0400" ref-type="bibr">Woo et al., 2006</xref>, <xref rid="bb0105" ref-type="bibr">Corman et al., 2015</xref>, <xref rid="bb0100" ref-type="bibr">Corman et al., 2014</xref>, <xref rid="bb0430" ref-type="bibr">Xu et al., 2016</xref>). The PREDICT-CoV-34 strain showed the highest similarity to the bat coronavirus isolate JPDB144 recently described in <italic>Myotis daubentonii</italic> in China (89.5% nucleic acid identity and 95% amino acid identity) (<xref rid="bb0430" ref-type="bibr">Xu et al., 2016</xref>). Sequences from the subcluster 1 displayed similar traits and were only detected in Cambodian <italic>Scotophilus</italic> (<italic>n</italic> = 31), with the exception of one sequence detected in Cambodian <italic>Pipistrellus</italic> (BatCoV512_SL2-9_Pisp). The αCoV subcluster 4 contained sequences related to the strain HKU10, detected in various bat genera in Thailand and Hong Kong (<xref rid="bb0135" ref-type="bibr">Gouilh et al., 2011</xref>, <xref rid="bb0200" ref-type="bibr">Lau et al., 2012</xref>, <xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>). In this subcluster, two sequences found in <italic>Hipposideros larvatus</italic> (PREDICT-CoV-53 strains) from Lao PDR formed their own branch (subcluster αCoV_4c), supported by a bootstrap of 100. They were related to the αCoV BatCoV Ratcha-67 (96.9% amino acid identity) previously detected in the same bat genus in Thailand (<xref rid="bb0135" ref-type="bibr">Gouilh et al., 2011</xref>). Additionally, the sequence BatCoV-25 PA201 detected in <italic>Rhinolophus shameli</italic>, showed the highest similarity with a sequence detected in the same host species in Thailand (BatCoV B554) (<xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>). Interestingly, two αCoV sequences detected from <italic>Myotis horsfieldii</italic> in Cambodia, PEDV_Kch1-04 and PEDV_Kch1-13, fell with the CoV responsible for porcine epidemic diarrhea episodes in pigs (PEDV), in the αCoV subcluster 2. They displayed 93.4% to 97.2% nucleotide identity and 96.13% to 100% amino acid identity with the porcine CoV strain PEDV. All sequences of viruses identified in <italic>Scotophilus</italic> fell in the subcluster 1 of αCoVs, those from <italic>Hipposideros</italic> belonged to the subcluster αCoV_4c, the sequences found in <italic>Myotis</italic> were all from the subcluster 2 of αCoV and the sequences of the viruses identified in <italic>Rousettus</italic> were all grouped in the lineage βCoV_D. In <italic>Pipistrellus</italic> bats from Mondulkiri province caught in 2013, the viruses detected belonged to both the αCoV and the βCoV groups.</p></sec></sec><sec id="s0060"><label>4</label><title>Discussion</title><p id="p0110">In this study, we report for the first time, the detection and description of coronaviruses in chiroptera from Cambodia and Lao PDR. This report is of importance for public health as these countries host a high biodiversity of bats and the interface at which humans and chiroptera are in close proximity. Bats are used for food and reared as a source of guano. Searching for bat-borne viruses known to be potentially pathogenic for humans such as coronaviruses is therefore of high importance. A significant diversity of CoVs was found in pteropodids both in Cambodia and Lao PDR. Overall, CoV detection rates (6.5% in Lao PDR and 4.85% in Cambodia) were in the same range as those found in Thailand (7%) (<xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>), but lower than those reported in Hong Kong (12%) or Philippines (29.6%) (<xref rid="bb0355" ref-type="bibr">Tsuda et al., 2012</xref>, <xref rid="bb0400" ref-type="bibr">Woo et al., 2006</xref>). Interestingly, for the first time, coronaviruses were detected in <italic>Megaerops niphanae</italic> and <italic>Myotis horsfieldii</italic>.</p><p id="p0115">In this study, αCoVs were mostly associated with <italic>Yangochiroptera</italic> bats whereas and βCoVs were found in <italic>Yinpterochiroptera</italic> bats, with the exception of three viruses, <italic>i.e.</italic>, 2 CoVs from the subcluster 4 of found in hipposiderids, and one βCoV from lineage C, detected in <italic>Pipistrellus</italic>. In Lao PDR, βCoVs from lineage D were all associated with pteropodids whereas αCoVs were detected from hipposiderids. In Cambodia, an association between host and virus clade was observed between bats from the genus <italic>Myotis</italic> and the αCoVs genetically related to PEDV strains. These results are in line with conclusions of previous studies: all CoVs detected in bats belonging to the <italic>Myotis</italic> genus were always αCoVs (<xref rid="bb0340" ref-type="bibr">Tang et al., 2006</xref>, <xref rid="bb0400" ref-type="bibr">Woo et al., 2006</xref>, <xref rid="bb0110" ref-type="bibr">Dominguez et al., 2007</xref>, <xref rid="bb0130" ref-type="bibr">Gloza-Rausch et al., 2008</xref>, <xref rid="bb0275" ref-type="bibr">Osborne et al., 2011</xref>, <xref rid="bb0030" ref-type="bibr">August et al., 2012</xref>, <xref rid="bb0170" ref-type="bibr">Kemenesi et al., 2014</xref>, <xref rid="bb0120" ref-type="bibr">Fischer et al., 2016</xref>). βCoVs from lineage D have frequently been found in frugivorous bat species from Madagascar, Kenya, Thailand, and Hong Kong (<xref rid="bb0405" ref-type="bibr">Woo et al., 2007</xref>, <xref rid="bb0020" ref-type="bibr">Anindita et al., 2015</xref>, <xref rid="bb0290" ref-type="bibr">Razanajatovo et al., 2015</xref>, <xref rid="bb0375" ref-type="bibr">Wacharapluesadee et al., 2015</xref>, <xref rid="bb0430" ref-type="bibr">Xu et al., 2016</xref>). A similar trend was observed in this study, as βCoVs from the lineage D were only affiliated with frugivorous bats.</p><p id="p0120">Although only part of the samples could yield a longer sequence, phylogeny based on these sequences was similar to that based on short sequences. This suggests that the phylogeny based on short sequences is reliable. Unfortunately sequencing of coronavirus can be challenging, due in part, to limited nucleic acid in field samples, as well as the high genetic diversity of the viruses (<xref rid="bb0115" ref-type="bibr">Drexler et al., 2010</xref>, <xref rid="bb0180" ref-type="bibr">King et al., 2012</xref>). Although some findings in this study suggest the possibility of host specificity, in particular for the genera <italic>Hipposideros</italic> and <italic>Myotis</italic> (associated to αCoVs from the subclusters 4c and 2 respectively), we also report shared hosts from different families for both αCoV and βCoV. For example, <italic>Pipistrellus</italic> bats from the same location were found to harbor αCoV from the subcluster 1 and lineage C βCoVs sequences. Coronaviruses from the latter lineage, which also includes the highly pathogenic MERS-CoV (<xref rid="bb0300" ref-type="bibr">Reusken et al., 2016</xref>), have been detected in humans, camels, insectivorous bats (<italic>Vespertilionidae</italic>) and frugivorous bats (<italic>Phyllostomidae</italic>) (<xref rid="bb0295" ref-type="bibr">Reusken et al., 2010</xref>, <xref rid="bb0025" ref-type="bibr">Annan et al., 2013</xref>, <xref rid="bb0370" ref-type="bibr">Wacharapluesadee et al., 2013</xref>, <xref rid="bb0100" ref-type="bibr">Corman et al., 2014</xref>, <xref rid="bb0385" ref-type="bibr">Wang et al., 2014</xref>, <xref rid="bb0260" ref-type="bibr">Munster et al., 2016</xref>). There have also been found differences in the percentage of seropositive between <italic>Rhinolophus ferrumequinum</italic> and <italic>Myotis myotis</italic> in studies of lyssavirus of European bat colonies (<xref rid="bb0310" ref-type="bibr">Serra-Cobo et al., 2013</xref>).</p><p id="p0125"><italic>Pipistrellus coromandra</italic> is a synanthropic bat and the presence of CoVs in the same clade with pathogenic viruses raises the question of the potential risk for human health resulting from deforestation and urbanization that creates habitats for these bats. <italic>Pipistrellus</italic> bats, like <italic>Myotis</italic>, comprise species with differing habitats. However, in this work, <italic>Pipistrellus coromandra</italic> was found in deforested and agricultural regions, confirming thus its synanthropic behavior in the study area considered. Further risk-assessment studies should focus on the correlation between landscape change, land use and deforestation that may affect the distribution of human-dwelling bats and therefore the coronaviruses they harbor. This risk in Cambodia might be worsened by the fact that <italic>Pipistrellus</italic> bats are hunted for food. Another related risk might be the development of guano farms, also associated with agriculture (<xref rid="bb0335" ref-type="bibr">Stibig et al., 2007</xref>, <xref rid="bb0060" ref-type="bibr">Broadhead and Izquierdo, 2010</xref>). Bats reared for guano in Thailand have shown to harbor lineage C βCoV (<xref rid="bb0370" ref-type="bibr">Wacharapluesadee et al., 2013</xref>). This activity is also developing in Cambodia (<xref rid="bb0350" ref-type="bibr">Thi et al., 2014</xref>) and the perception of risk from workers is weak. Furthermore, hunters and restaurant workers at sampling sites described being bitten by bats and were exposed to urine and feces (and in some cases blood). Bats on Cambodian guano farms are wild and free-ranging, with farmers constructing artificial roosts adjacent to their homes in order to attract bats. Farmers, who wear no protective equipment or clothing, collect guano voided onto tarpaulins or nets laid beneath the roosts and are regularly urinated and defecated upon and sometimes bitten. The risk of contamination by direct contact through urine and feces, or aerosols must therefore be considered.</p><p id="p0130">The hypothesis of a potential case of horizontal transmission between livestock and bats can be raised with the PEDV-like viruses, detected in <italic>Myotis horsfieldii</italic>. Another αCoV closely related to PEDV-CoV was recently detected in Brazil in Mexican free-tailed bats (<italic>Tadarida brasiliensis</italic>) (<xref rid="bb0325" ref-type="bibr">Simas et al., 2015</xref>). Not only is this first report of the presence of this coronavirus in <italic>Myotis horsfieldii</italic>, but the strain detected seems genetically closely related to PEDV strains that infect swine and cattle (<xref rid="bb0330" ref-type="bibr">Song and Park, 2012</xref>). <italic>Myotis</italic> bats also belong to the <italic>Vespertilionidae</italic> family and dwell in dark places including houses, farms and barns. Investigating the presence of pig farms in areas where coronavirus are detected, and the circulation of <italic>Myotis</italic> bats in the surroundings, would provide data to explore potential relations between bats and livestock. The hypothesis of a possible origin of PEDV from bats as well as a potential cross-species transmission has been raised by previous studies (<xref rid="bb0160" ref-type="bibr">Huang et al., 2013</xref>, <xref rid="bb0340" ref-type="bibr">Tang et al., 2006</xref>) and would benefit from further investigation. To date, only a limited number of studies have investigated the capacity of bat coronaviruses to be infectious to other mammals, including humans. This is notably due to a lack of data on the spike protein of these bat viruses. Indeed, the spike protein is the primary determinant for the cell tropism and pathogenesis (<xref rid="bb0045" ref-type="bibr">Belouzard et al., 2012</xref>).</p><p id="p0135">Our study had some limitations related to sampling procedure that may have affected results. Many of the samples (<italic>n</italic> = 1838) were collected from dead bats intended for human consumption. If rectal swab is the sample which represents the highest probability for detecting coronaviruses in bats (<xref rid="bb0390" ref-type="bibr">Watanabe et al., 2010</xref>), it is possible that virus survival in dead animals might be affected. The health status of the animals sampled in our study was unknown but previous studies suggest that bats might not develop disease during coronavirus infections. RNA viruses seem to have little pathogenic effect on bat's life cycle (<xref rid="bb0220" ref-type="bibr">Li et al., 2005</xref>) which may explain that bats are excellent reservoirs for zoonotic viruses including CoVs (<xref rid="bb0270" ref-type="bibr">Omatsu et al., 2007</xref>, <xref rid="bb0065" ref-type="bibr">Brook and Dobson, 2015</xref>, <xref rid="bb0150" ref-type="bibr">Han et al., 2015</xref>). Seasonality has been shown for some zoonotic virus infection rates in Chiroptera. Reproduction periods, female status and resource availabilities have been proven to affect the prevalence in bats infected by other RNA viruses (<xref rid="bb0250" ref-type="bibr">Middleton et al., 2007</xref>, <xref rid="bb0285" ref-type="bibr">Plowright et al., 2008</xref>, <xref rid="bb0365" ref-type="bibr">Wacharapluesadee et al., 2010</xref>, <xref rid="bb0125" ref-type="bibr">George et al., 2011</xref>, <xref rid="bb0015" ref-type="bibr">Amman et al., 2012</xref>, <xref rid="bb0155" ref-type="bibr">Hayman, 2015</xref>, <xref rid="bb0010" ref-type="bibr">Amengual et al., 2007</xref>). Greater shedding over such periods increase the probability of transmission of viruses to humans and the risk of emerging zoonoses (<xref rid="bb0310" ref-type="bibr">Serra-Cobo et al., 2013</xref>). Seasonality was not explored in our study due to the heterogeneity of the sampling session over time, but it would be interesting to include these parameters in further investigations. Another limitation in this work is the lack of molecular identification of bats. The collection of bat samples for barcoding or Cyt identification was not part of the field procedure and thus no bat sample has been collected during the field work. The identification was therefore limited to the genus.</p><p id="p0140">Almost all the bats which tested positive for coronaviruses were meant to be consumed by local human populations. The examples of Ebola or SARS-CoV outbreaks already suggested that wildlife hunting and consumption provided opportunities for human contamination (<xref rid="bb0050" ref-type="bibr">Bengis et al., 2004</xref>, <xref rid="bb0425" ref-type="bibr">Xu et al., 2004</xref>, <xref rid="bb0210" ref-type="bibr">Leroy et al., 2009</xref>). In Cambodia and Lao PDR, bat consumption is widespread (<xref rid="bb0245" ref-type="bibr">Mickleburgh et al., 2009</xref>, <xref rid="bb0205" ref-type="bibr">Lee et al., 2014</xref>, <xref rid="bb0255" ref-type="bibr">Mildenstein et al., 2016</xref>). These practices may increase the risk of human exposure to viruses through hosts that may be reservoirs for pathogens. Practices such as hunting, selling or cooking bats might represent efficient interfaces for virus transfer from bats to humans, and therefore need to be further investigated. It demonstrates the importance to develop guidance for rural communities exposed to bats, on how to deal with them and the potential virus threat.</p><p id="p0145">The diversity of bat coronaviruses found circulating in Cambodia and Lao PDR suggests a correlation may exist between coronaviruses and host diversity which is at least for part the consequence of anthropogenic natural environment change, mostly deforestation. The natural landscapes surrounding the collection points correlated with the known biology and ecology of the bats sampled (<xref rid="ec0025" ref-type="supplementary-material">Supplementary Table 3</xref>). Pteropodids and vespertilionids, known to roost in caves (<italic>Eonycteris</italic> or <italic>Rousettus</italic>, and <italic>Ia</italic> respectively), were collected close to karst areas in Lao PDR. In Cambodia, the <italic>Yinpterochiroptera</italic> bats belonged to 5 genera of pteropodids known to mostly live in trees (<italic>Cynopterus</italic>, <italic>Macroglossus</italic>, <italic>Megaerops</italic>, <italic>Pteropus</italic>, <italic>Rousettus</italic>). Forest coverage throughout Continental Southeast Asia has drastically evolved between 1990 and 2015 (<xref rid="ec0010" ref-type="supplementary-material">Supplementary Fig. 4</xref>). Cambodia is the country where forest loss has been the most intensive with 20% of the forest surface lost since 1990, while about 50% of the remaining surface is fragmented and 70% of the forest is in a “perforation” state, associated with agricultural development (<xref rid="bb0420" ref-type="bibr">WWF, 2013</xref>; World Bank, 2016). In Lao PDR, the forest coverage looksstable (73% in 1990, 81% in 2015), but the structure of the forest has changed. A typical feature is the fragmentation of the natural forest and its replacement by cultivated areas. However, compared to other countries in the region, the forest coverage remains the highest in Lao PDR and shows signs of resilience. This is mostly due to the geology of the country which is mainly karstic and thus less useful for agriculture. For both countries the demographic growth remains a key point for natural environment evolution, forest loss and dynamic of urban and suburban expansion. This environmental change is affecting the biodiversity of bats and therefore that of their coronaviruses. Continued deforestation, agricultural expansion and suburban growth might facilitate encounters between humans and coronaviruses from human-dwelling bats that could potentially become harmful for humans, specific attention and studies should therefore be devoted to this aspect.</p><p id="p0155">The following are the supplementary data related to this article.<supplementary-material content-type="local-data" id="ec0005"><caption><title>Supplementary Fig. 1</title><p>Geographic distribution of samples in Lao PDR and Cambodia. Sampling sites are shown by triangles and labeled from C1 to C44 (<xref rid="ec0020" ref-type="supplementary-material">Supplementary Table 2</xref>). The 21 sites where bats tested positive for coronaviruses are shown with a red triangle.</p></caption><media xlink:href="mmc1.pptx"><alt-text>Supplementary Fig. 1</alt-text></media></supplementary-material><fig id="f0020"><label>Supplementary Fig. 2</label><caption><p>Distribution of coronavirus sequences based on a 115 amino acid fragment encoded by the RdRp gene.</p><p>The tree was constructed by neighbor joining and bootstrap values were determined by 1000 replicates. The tree is rooted to an avian coronavirus (FJ376622). The sequences detected in this study are shown with a bullet. Accession numbers related to the sequences are presented in <xref rid="ec0015" ref-type="supplementary-material">Supplementary Table 1</xref>.</p></caption><alt-text id="al0035">Supplementary Fig. 2</alt-text><graphic xlink:href="gr3_lrg"></graphic></fig><fig id="f0025"><label>Supplementary Fig. 3</label><caption><p>Distribution of coronavirus sequences based on a 115 amino acid fragment encoded by the RdRp gene.</p><p>The tree was constructed by neighbor joining and bootstrap values were determined by 1000 replicates. The tree is rooted to an avian coronavirus (FJ376622). Bootstrap values (BP) were calculated after 1000 replicates. The sequences detected in this study are shown with a bullet. Accession numbers related to the sequences are presented in <xref rid="ec0015" ref-type="supplementary-material">Supplementary Table 1</xref>.</p></caption><alt-text id="al0040">Supplementary Fig. 3</alt-text><graphic xlink:href="gr4_lrg"></graphic></fig><supplementary-material content-type="local-data" id="ec0010"><caption><title>Supplementary Fig. 4</title><p>Forest cover change in South East Asia from 1990 to 2015. a. Map of forest cover change. b. Dynamic of forest cover change.</p></caption><media xlink:href="mmc2.pptx"><alt-text>Supplementary Fig. 4</alt-text></media></supplementary-material><supplementary-material content-type="local-data" id="ec0015"><caption><title>Supplementary Table 1</title><p>Accession numbers of sequences deposited in Genbank, and corresponding named used for sequence analysis.</p></caption><media xlink:href="mmc3.docx"><alt-text>Supplementary Table 1</alt-text></media></supplementary-material><supplementary-material content-type="local-data" id="ec0020"><caption><title>Supplementary Table 2</title><p>Mammals and provinces abbreviations used for coding coronavirus samples.</p></caption><media xlink:href="mmc4.docx"><alt-text>Supplementary Table 2</alt-text></media></supplementary-material><supplementary-material content-type="local-data" id="ec0025"><caption><title>Supplementary Table 3</title><p>Origin of the samples collected and description of the environment around the sampling sites.</p></caption><media xlink:href="mmc5.docx"><alt-text>Supplementary Table 3</alt-text></media></supplementary-material></p></sec><sec id="s0065"><title>Conflict of interest</title><p id="p0165">Philippe Buchy is currently an employee of GSK vaccines.</p></sec></body><back><ref-list id="bi0005"><title>References</title><ref id="bb0005"><element-citation publication-type="journal" id="rf0005"><person-group person-group-type="author"><name><surname>Alsahafi</surname><given-names>A.J.</given-names></name><name><surname>Cheng</surname><given-names>A.C.</given-names></name></person-group><article-title>The epidemiology of Middle East respiratory syndrome coronavirus in the Kingdom of Saudi Arabia, 2012–2015</article-title><source>Int. 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Dis.</source><volume>2</volume><year>1996</year><fpage>239</fpage><lpage>240</lpage><pub-id pub-id-type="pmid">8903239</pub-id></element-citation></ref></ref-list><ack id="ac0005"><title>Acknowledgements</title><p>This study was made possible by the generous support of the American people through the <funding-source id="gts0005">United States Agency for International Development</funding-source> (USAID) Emerging Pandemic Threats PREDICT project (cooperative agreement number GHN-A-OO-09-00010-00). We thank the governments of Cambodia and Laos for permission to conduct this study. We are grateful to the WCS teams and all students who helped collecting field samples. We also extend our gratitude to Dara Kong and Serey Roth Long for technical support in laboratory diagnostic. Authors are also grateful to Neil Furey, from the Center for Biodiversity Conservation of the Royal University of Phnom Penh, for his help and advice on species identification. We also thank Sarah Olson for her help with proof reading this document.</p></ack></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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