Polyphyletic origin of MERS coronaviruses and isolation of a novel clade A strain from dromedary camels in the United Arab Emirates
Identifieur interne : 000A40 ( Pmc/Checkpoint ); précédent : 000A39; suivant : 000A41Polyphyletic origin of MERS coronaviruses and isolation of a novel clade A strain from dromedary camels in the United Arab Emirates
Auteurs : Susanna K P. Lau [République populaire de Chine] ; Renate Wernery ; Emily Y M. Wong [République populaire de Chine] ; Sunitha Joseph ; Alan K L. Tsang [République populaire de Chine] ; Nissy Annie Georgy Patteril ; Shyna K. Elizabeth ; Kwok-Hung Chan [République populaire de Chine] ; Rubeena Muhammed ; Jöerg Kinne ; Kwok-Yung Yuen [République populaire de Chine] ; Ulrich Wernery ; Patrick C Y. Woo [République populaire de Chine]Source :
- Emerging Microbes & Infections [ 2222-1751 ] ; 2016.
Abstract
Little is known regarding the molecular epidemiology of Middle East respiratory syndrome coronavirus (MERS-CoV) circulating in dromedaries outside Saudi Arabia. To address this knowledge gap, we sequenced 10 complete genomes of MERS-CoVs isolated from 2 live and 8 dead dromedaries from different regions in the United Arab Emirates (UAE). Phylogenetic analysis revealed one novel clade A strain, the first detected in the UAE, and nine clade B strains. Strain D998/15 had a distinct phylogenetic position within clade A, being more closely related to the dromedary isolate NRCE-HKU205 from Egypt than to the human isolates EMC/2012 and Jordan-N3/2012. A comparison of predicted protein sequences also demonstrated the existence of two clade A lineages with unique amino acid substitutions, A1 (EMC/2012 and Jordan-N3/2012) and A2 (D998/15 and NRCE-HKU205), circulating in humans and camels, respectively. The nine clade B isolates belong to three distinct lineages: B1, B3 and B5. Two B3 strains, D1271/15 and D1189.1/15, showed evidence of recombination between lineages B4 and B5 in ORF1ab. Molecular clock analysis dated the time of the most recent common ancestor (tMRCA) of clade A to March 2011 and that of clade B to November 2011. Our data support a polyphyletic origin of MERS-CoV in dromedaries and the co-circulation of diverse MERS-CoVs including recombinant strains in the UAE.
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DOI: 10.1038/emi.2016.129
PubMed: 27999424
PubMed Central: 5180373
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Lau</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>State Key Laboratory of Emerging Infectious Diseases, Research Centre of Infection and Immunology, Carol Yu Centre for Infection, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wernery, Renate" sort="Wernery, Renate" uniqKey="Wernery R" first="Renate" last="Wernery">Renate Wernery</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Wong, Emily Y M" sort="Wong, Emily Y M" uniqKey="Wong E" first="Emily Y M" last="Wong">Emily Y M. 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Tsang</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Patteril, Nissy Annie Georgy" sort="Patteril, Nissy Annie Georgy" uniqKey="Patteril N" first="Nissy Annie Georgy" last="Patteril">Nissy Annie Georgy Patteril</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Elizabeth, Shyna K" sort="Elizabeth, Shyna K" uniqKey="Elizabeth S" first="Shyna K" last="Elizabeth">Shyna K. Elizabeth</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Chan, Kwok Hung" sort="Chan, Kwok Hung" uniqKey="Chan K" first="Kwok-Hung" last="Chan">Kwok-Hung Chan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Muhammed, Rubeena" sort="Muhammed, Rubeena" uniqKey="Muhammed R" first="Rubeena" last="Muhammed">Rubeena Muhammed</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Kinne, Joerg" sort="Kinne, Joerg" uniqKey="Kinne J" first="Jöerg" last="Kinne">Jöerg Kinne</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>State Key Laboratory of Emerging Infectious Diseases, Research Centre of Infection and Immunology, Carol Yu Centre for Infection, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wernery, Ulrich" sort="Wernery, Ulrich" uniqKey="Wernery U" first="Ulrich" last="Wernery">Ulrich Wernery</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Woo, Patrick C Y" sort="Woo, Patrick C Y" uniqKey="Woo P" first="Patrick C Y" last="Woo">Patrick C Y. Woo</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>State Key Laboratory of Emerging Infectious Diseases, Research Centre of Infection and Immunology, Carol Yu Centre for Infection, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">27999424</idno><idno type="pmc">5180373</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5180373</idno><idno type="RBID">PMC:5180373</idno><idno type="doi">10.1038/emi.2016.129</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000135</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000135</idno><idno type="wicri:Area/Pmc/Curation">000135</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000135</idno><idno type="wicri:Area/Pmc/Checkpoint">000A40</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000A40</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Polyphyletic origin of MERS coronaviruses and isolation of a novel clade A strain from dromedary camels in the United Arab Emirates</title><author><name sortKey="Lau, Susanna K P" sort="Lau, Susanna K P" uniqKey="Lau S" first="Susanna K P" last="Lau">Susanna K P. Lau</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>State Key Laboratory of Emerging Infectious Diseases, Research Centre of Infection and Immunology, Carol Yu Centre for Infection, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wernery, Renate" sort="Wernery, Renate" uniqKey="Wernery R" first="Renate" last="Wernery">Renate Wernery</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Wong, Emily Y M" sort="Wong, Emily Y M" uniqKey="Wong E" first="Emily Y M" last="Wong">Emily Y M. Wong</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Joseph, Sunitha" sort="Joseph, Sunitha" uniqKey="Joseph S" first="Sunitha" last="Joseph">Sunitha Joseph</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Tsang, Alan K L" sort="Tsang, Alan K L" uniqKey="Tsang A" first="Alan K L" last="Tsang">Alan K L. Tsang</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Patteril, Nissy Annie Georgy" sort="Patteril, Nissy Annie Georgy" uniqKey="Patteril N" first="Nissy Annie Georgy" last="Patteril">Nissy Annie Georgy Patteril</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Elizabeth, Shyna K" sort="Elizabeth, Shyna K" uniqKey="Elizabeth S" first="Shyna K" last="Elizabeth">Shyna K. Elizabeth</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Chan, Kwok Hung" sort="Chan, Kwok Hung" uniqKey="Chan K" first="Kwok-Hung" last="Chan">Kwok-Hung Chan</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Muhammed, Rubeena" sort="Muhammed, Rubeena" uniqKey="Muhammed R" first="Rubeena" last="Muhammed">Rubeena Muhammed</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Kinne, Joerg" sort="Kinne, Joerg" uniqKey="Kinne J" first="Jöerg" last="Kinne">Jöerg Kinne</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>State Key Laboratory of Emerging Infectious Diseases, Research Centre of Infection and Immunology, Carol Yu Centre for Infection, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wernery, Ulrich" sort="Wernery, Ulrich" uniqKey="Wernery U" first="Ulrich" last="Wernery">Ulrich Wernery</name><affiliation><nlm:aff id="aff3"><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></nlm:aff><wicri:noCountry code="nlm country">UAE</wicri:noCountry></affiliation></author><author><name sortKey="Woo, Patrick C Y" sort="Woo, Patrick C Y" uniqKey="Woo P" first="Patrick C Y" last="Woo">Patrick C Y. Woo</name><affiliation wicri:level="1"><nlm:aff id="aff1"><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff2"><institution>State Key Laboratory of Emerging Infectious Diseases, Research Centre of Infection and Immunology, Carol Yu Centre for Infection, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong</institution>, Hong Kong,<country>China</country></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Emerging Microbes & Infections</title><idno type="eISSN">2222-1751</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>Little is known regarding the molecular epidemiology of Middle East respiratory syndrome coronavirus (MERS-CoV) circulating in dromedaries outside Saudi Arabia. To address this knowledge gap, we sequenced 10 complete genomes of MERS-CoVs isolated from 2 live and 8 dead dromedaries from different regions in the United Arab Emirates (UAE). Phylogenetic analysis revealed one novel clade A strain, the first detected in the UAE, and nine clade B strains. Strain D998/15 had a distinct phylogenetic position within clade A, being more closely related to the dromedary isolate NRCE-HKU205 from Egypt than to the human isolates EMC/2012 and Jordan-N3/2012. A comparison of predicted protein sequences also demonstrated the existence of two clade A lineages with unique amino acid substitutions, A1 (EMC/2012 and Jordan-N3/2012) and A2 (D998/15 and NRCE-HKU205), circulating in humans and camels, respectively. The nine clade B isolates belong to three distinct lineages: B1, B3 and B5. Two B3 strains, D1271/15 and D1189.1/15, showed evidence of recombination between lineages B4 and B5 in ORF1ab. Molecular clock analysis dated the time of the most recent common ancestor (tMRCA) of clade A to March 2011 and that of clade B to November 2011. Our data support a polyphyletic origin of MERS-CoV in dromedaries and the co-circulation of diverse MERS-CoVs including recombinant strains in the UAE.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Emerg Microbes Infect</journal-id><journal-id journal-id-type="iso-abbrev">Emerg Microbes Infect</journal-id><journal-title-group><journal-title>Emerging Microbes & Infections</journal-title></journal-title-group><issn pub-type="epub">2222-1751</issn><publisher><publisher-name>Nature Publishing Group</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">27999424</article-id><article-id pub-id-type="pmc">5180373</article-id><article-id pub-id-type="pii">emi2016129</article-id><article-id pub-id-type="doi">10.1038/emi.2016.129</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject></subj-group></article-categories><title-group><article-title>Polyphyletic origin of MERS coronaviruses and isolation of a novel clade A strain from dromedary camels in the United Arab Emirates</article-title><alt-title alt-title-type="running">Dromedary MERS coronaviruses in the United Arab Emirates</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Lau</surname><given-names>Susanna K P</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff2">2</xref><xref ref-type="author-notes" rid="note1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wernery</surname><given-names>Renate</given-names></name><xref ref-type="aff" rid="aff3">3</xref><xref ref-type="author-notes" rid="note1"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wong</surname><given-names>Emily Y M</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Joseph</surname><given-names>Sunitha</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Tsang</surname><given-names>Alan K L</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Patteril</surname><given-names>Nissy Annie Georgy</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Elizabeth</surname><given-names>Shyna K</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Chan</surname><given-names>Kwok-Hung</given-names></name><xref ref-type="aff" rid="aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Muhammed</surname><given-names>Rubeena</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Kinne</surname><given-names>Jöerg</given-names></name><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Yuen</surname><given-names>Kwok-Yung</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Wernery</surname><given-names>Ulrich</given-names></name><xref ref-type="aff" rid="aff3">3</xref><xref ref-type="corresp" rid="caf1">*</xref></contrib><contrib contrib-type="author"><name><surname>Woo</surname><given-names>Patrick C Y</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff2">2</xref><xref ref-type="corresp" rid="caf2">*</xref></contrib><aff id="aff1"><label>1</label><institution>Department of Microbiology, The University of Hong Kong</institution>, Hong Kong,<country>China</country></aff><aff id="aff2"><label>2</label><institution>State Key Laboratory of Emerging Infectious Diseases, Research Centre of Infection and Immunology, Carol Yu Centre for Infection, Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, The University of Hong Kong</institution>, Hong Kong,<country>China</country></aff><aff id="aff3"><label>3</label><institution>Central Veterinary Research Laboratory</institution>, PO Box 597, Dubai,<country>UAE</country></aff></contrib-group><author-notes><corresp id="caf1"><label>*</label>E-mail: <email>cvrl@cvrl.ae</email></corresp><corresp id="caf2"><label>*</label>E-mail: <email>pcywoo@hku.hk</email></corresp><fn fn-type="present-address" id="note1"><label>*</label><p>These authors contributed equally to this work.</p></fn></author-notes><pub-date pub-type="ppub"><month>12</month><year>2016</year></pub-date><pub-date pub-type="epub"><day>21</day><month>12</month><year>2016</year></pub-date><pub-date pub-type="pmc-release"><day>1</day><month>12</month><year>2016</year></pub-date><volume>5</volume><issue>12</issue><fpage>e128</fpage><lpage></lpage><history><date date-type="received"><day>05</day><month>08</month><year>2016</year></date><date date-type="rev-recd"><day>23</day><month>09</month><year>2016</year></date><date date-type="accepted"><day>11</day><month>10</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016 The Author(s)</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>The Author(s)</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/4.0/"><pmc-comment>author-paid</pmc-comment>
<license-p>This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><abstract><p>Little is known regarding the molecular epidemiology of Middle East respiratory syndrome coronavirus (MERS-CoV) circulating in dromedaries outside Saudi Arabia. To address this knowledge gap, we sequenced 10 complete genomes of MERS-CoVs isolated from 2 live and 8 dead dromedaries from different regions in the United Arab Emirates (UAE). Phylogenetic analysis revealed one novel clade A strain, the first detected in the UAE, and nine clade B strains. Strain D998/15 had a distinct phylogenetic position within clade A, being more closely related to the dromedary isolate NRCE-HKU205 from Egypt than to the human isolates EMC/2012 and Jordan-N3/2012. A comparison of predicted protein sequences also demonstrated the existence of two clade A lineages with unique amino acid substitutions, A1 (EMC/2012 and Jordan-N3/2012) and A2 (D998/15 and NRCE-HKU205), circulating in humans and camels, respectively. The nine clade B isolates belong to three distinct lineages: B1, B3 and B5. Two B3 strains, D1271/15 and D1189.1/15, showed evidence of recombination between lineages B4 and B5 in ORF1ab. Molecular clock analysis dated the time of the most recent common ancestor (tMRCA) of clade A to March 2011 and that of clade B to November 2011. Our data support a polyphyletic origin of MERS-CoV in dromedaries and the co-circulation of diverse MERS-CoVs including recombinant strains in the UAE.</p></abstract><kwd-group><kwd>clade A</kwd><kwd>dromedary camels</kwd><kwd>MERS</kwd><kwd>Middle East respiratory syndrome coronavirus</kwd><kwd>novel</kwd><kwd>polyphyletic</kwd><kwd>United Arab Emirates</kwd></kwd-group></article-meta></front><floats-group><fig id="fig1"><label>Figure 1</label><caption><p>Geographical distribution of dromedaries in the United Arab Emirates infected with MERS-CoV strains that were isolated in the present study. The number of dromedaries corresponds to the number of MERS-CoV isolates from the sampling location.</p></caption><graphic xlink:href="emi2016129f1"></graphic></fig><fig id="fig2"><label>Figure 2</label><caption><p>Maximum-likelihood phylogeny based on the complete genome sequences of 182 MERS-CoV strains. A general time-reversible model of nucleotide substitution with estimated base frequencies, the proportion of invariant sites, and the gamma distribution of rates across sites were used in the maximum-likelihood analysis. Bootstrap values are shown next to the branches. The scale bar indicates the number of nucleotide substitutions per site. MERS-CoVs from dromedaries are indicated in black circles. The ten MERS-CoV strains sequenced in the present study are colored: blue, Dubai; brown, Umm Al Quwain; green, Saudi Arabia. MERS-CoVs isolated from the United Arab Emirates are indicated by gray boxes.</p></caption><graphic xlink:href="emi2016129f2"></graphic></fig><fig id="fig3"><label>Figure 3</label><caption><p>Maximum-likelihood phylogeny based on ORF1a, ORF1b and S gene sequences of 182 MERS-CoV strains. TIM1+I+G, GTR+I+G, and TK 2+I substitution models were selected for the ORF1a, ORF1b and S gene trees, respectively. Bootstrap values are shown next to the branches. The scale bar indicates the number of nucleotide substitutions per site. MERS-CoVs from dromedaries are indicated in black circles. The 10 MERS-CoV strains sequenced in the present study are colored: blue, Dubai; brown, Umm Al Quwain; green, Saudi Arabia. MERS-CoVs isolated from the United Arab Emirates are indicated by gray boxes.</p></caption><graphic xlink:href="emi2016129f3"></graphic></fig><fig id="fig4"><label>Figure 4</label><caption><p>Detection of potential recombination events by bootscan analysis and multiple alignments. Bootscanning was conducted with Simplot version 3.5.1 (F84 model; window size, 1,500 bp; step, 200 bp) on a gapless nucleotide alignment. (<bold>A</bold>) D1271/15 and D1189.1/15 were used as the query sequences and compared with the genome sequences of a lineage 4 MERS-CoV strain Hafr-Al-Batin 1 (red, KF600628), a lineage 1 MERS-CoV strain UAE/Abu Dhabi_UAE_9 (green, KP209312) and a lineage 5 MERS-CoV strain D1157/15 (blue, KX108944). (<bold>B</bold>) D2731.3/14 was used as the query sequence and compared with the genome sequences of a lineage 1 MERS-CoV strain, FRA/UAE (green, KF745068), a lineage 4 MERS-CoV strain, KFMC-4 (red, KT121575) and a lineage 5 MERS-CoV strain, England-Qatar/2012 (blue, KC667074).</p></caption><graphic xlink:href="emi2016129f4"></graphic></fig><fig id="fig5"><label>Figure 5</label><caption><p>Maximum-likelihood trees constructed using nucleotide sequences of non-recombination regions (<bold>A</bold>), and recombination regions (<bold>B</bold>) detected using RDP4. The non-recombination region is approximately positions 1 to 14957 and 28836 to 30087, and the recombination region is approximately positions 14958 to 28835, with position numbering based on the D1189.1/15 genome sequence. Lineages are indicated by colored boxes: lineage 1, green; lineage 3, red; and lineage 5, blue.</p></caption><graphic xlink:href="emi2016129f5"></graphic></fig><fig id="fig6"><label>Figure 6</label><caption><p>Estimation of time to the most recent common ancestor for MERS-CoV. The time-scaled phylogeny was summarized from all Markov chain Monte Carlo phylogenies of the concatenated coding regions (ORF1ab, S, E, M and N) of 90 phylogenetically distinct MERS-CoV genomes, which were analyzed under the relaxed-clock model with an uncorrelated lognormal distribution in BEAST version 1.8.0. The 10 MERS-CoV genomes sequenced in this study are in boldface.</p></caption><graphic xlink:href="emi2016129f6"></graphic></fig><table-wrap id="tbl1"><label>Table 1</label><caption><title>Clinical and epidemiological data of the 10 dromedaries with MERS-CoV strains isolated and sequenced in this study</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col><col align="left"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><bold>Strains</bold></th><th align="left" valign="top" charoff="50"><bold>Clade/lineage</bold></th><th align="left" valign="top" charoff="50"><bold>Sex/age</bold></th><th align="left" valign="top" charoff="50"><bold>Date of sample collection</bold></th><th align="left" valign="top" charoff="50"><bold>Clinical samples</bold></th><th align="left" valign="top" charoff="50"><bold>Live/dead dromedary (causes of death)</bold></th><th align="left" valign="top" charoff="50"><bold>Origin of dromedary</bold></th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">D1164.1/14</td><td align="center" valign="top" charoff="50">B1</td><td align="left" valign="top" charoff="50">F/5 months</td><td align="left" valign="top" charoff="50">6 Jun, 2014</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Live</td><td align="left" valign="top" charoff="50">Breeding herd returning from Saudi Arabia</td></tr><tr><td align="left" valign="top" charoff="50">D2597.2/14</td><td align="center" valign="top" charoff="50">B1</td><td align="left" valign="top" charoff="50">NA/6 months</td><td align="left" valign="top" charoff="50">13 Dec, 2014</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Live</td><td align="left" valign="top" charoff="50">Dairy farm in Dubai</td></tr><tr><td align="left" valign="top" charoff="50">D252/15</td><td align="center" valign="top" charoff="50">B1</td><td align="left" valign="top" charoff="50">F/1 month</td><td align="left" valign="top" charoff="50">30 Jan, 2015</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Dead (white muscle disease, isosporosis abdominal edema disease)</td><td align="left" valign="top" charoff="50">Dairy farm in Dubai</td></tr><tr><td align="left" valign="top" charoff="50">D374/15</td><td align="center" valign="top" charoff="50">B1</td><td align="left" valign="top" charoff="50">M/1 month</td><td align="left" valign="top" charoff="50">12 Feb, 2015</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Dead (colisepticemia)</td><td align="left" valign="top" charoff="50">Dairy farm in Dubai</td></tr><tr><td align="left" valign="top" charoff="50">D383/15</td><td align="center" valign="top" charoff="50">B1</td><td align="left" valign="top" charoff="50">F/1 month</td><td align="left" valign="top" charoff="50">14 Feb, 2015</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Dead (colisepticemia)</td><td align="left" valign="top" charoff="50">Dairy farm in Dubai</td></tr><tr><td align="left" valign="top" charoff="50">D389/15</td><td align="center" valign="top" charoff="50">B1</td><td align="left" valign="top" charoff="50">M/15 days</td><td align="left" valign="top" charoff="50">15 Feb, 2015</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Dead (septicemia)</td><td align="left" valign="top" charoff="50">Dairy farm in Dubai</td></tr><tr><td align="left" valign="top" charoff="50">D998/15</td><td align="center" valign="top" charoff="50">A2</td><td align="left" valign="top" charoff="50">F/1 month</td><td align="left" valign="top" charoff="50">23 April, 2015</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Dead (white muscle disease and clostridiosis)</td><td align="left" valign="top" charoff="50">Dairy farm in Dubai<xref ref-type="fn" rid="t1-fn2">a</xref></td></tr><tr><td align="left" valign="top" charoff="50">D1157/15</td><td align="center" valign="top" charoff="50">B5</td><td align="left" valign="top" charoff="50">F/1 month</td><td align="left" valign="top" charoff="50">12 May, 2015</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Dead (septicemia)</td><td align="left" valign="top" charoff="50">Dairy farm in Dubai</td></tr><tr><td align="left" valign="top" charoff="50">D1271/15</td><td align="center" valign="top" charoff="50">B3</td><td align="left" valign="top" charoff="50">M/3 month</td><td align="left" valign="top" charoff="50">29 May, 2015</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Dead (high fever, purulent nasal discharge, pneumonia)</td><td align="left" valign="top" charoff="50">Dairy farm in Dubai</td></tr><tr><td align="left" valign="top" charoff="50">D1189.1/15</td><td align="center" valign="top" charoff="50">B3</td><td align="left" valign="top" charoff="50">F/6-9 months</td><td align="left" valign="top" charoff="50">18 May, 2015</td><td align="left" valign="top" charoff="50">Nasal swab</td><td align="left" valign="top" charoff="50">Dead (nasal discharge)</td><td align="left" valign="top" charoff="50">Umm Al Quwain</td></tr></tbody></table><table-wrap-foot><fn id="t1-fn1"><p>Abbreviation: Not available, NA.</p></fn><fn id="t1-fn2"><label>a</label><p>A special dairy farm with camel mothers from Pakistan.</p></fn></table-wrap-foot></table-wrap><table-wrap id="tbl2"><label>Table 2</label><caption><title>Comparison of amino acid substitutions between different clades and lineages</title></caption><table frame="hsides" rules="groups" border="1"><colgroup><col align="left"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="center"></col><col align="left"></col></colgroup><thead valign="bottom"><tr><th align="left" valign="top" charoff="50"><bold>Clade/lineage</bold></th><th align="center" valign="top" charoff="50"><bold>Species</bold></th><th align="center" valign="top" charoff="50"><bold>Strain</bold></th><th colspan="2" align="center" valign="top" charoff="50"><bold>nsp2</bold><hr></hr></th><th colspan="9" align="center" valign="top" charoff="50"><bold>nsp3</bold><hr></hr></th><th align="center" valign="top" charoff="50"><bold>nsp4</bold></th><th colspan="2" align="center" valign="top" charoff="50"><bold>S1</bold><hr></hr></th><th colspan="2" align="center" valign="top" charoff="50"><bold>S2</bold><hr></hr></th></tr><tr><th align="left" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"><bold>588</bold></th><th align="center" valign="top" charoff="50"><bold>726</bold></th><th align="center" valign="top" charoff="50"><bold>1000</bold></th><th align="center" valign="top" charoff="50"><bold>1024</bold></th><th align="center" valign="top" charoff="50"><bold>1055</bold></th><th align="center" valign="top" charoff="50"><bold>1066</bold></th><th align="center" valign="top" charoff="50"><bold>1370</bold></th><th align="center" valign="top" charoff="50"><bold>1574</bold></th><th align="center" valign="top" charoff="50"><bold>1717</bold></th><th align="center" valign="top" charoff="50"><bold>2114</bold></th><th align="center" valign="top" charoff="50"><bold>2481</bold></th><th align="center" valign="top" charoff="50"><bold>2780</bold></th><th align="center" valign="top" charoff="50"><bold>26</bold></th><th align="center" valign="top" charoff="50"><bold>194</bold></th><th align="center" valign="top" charoff="50"><bold>1020</bold></th><th align="center" valign="top" charoff="50"><bold>1158</bold></th></tr><tr><th align="left" valign="top" charoff="50"> </th><th align="left" valign="top" charoff="50"> </th><th align="left" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"><bold>CD</bold></th><th align="center" valign="top" charoff="50"><bold>CD</bold></th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"> </th><th align="center" valign="top" charoff="50"><bold>NT</bold></th><th align="center" valign="top" charoff="50"><bold>NT</bold></th><th align="center" valign="top" charoff="50"><bold>HR1</bold></th><th align="left" valign="top" charoff="50"> </th></tr></thead><tbody valign="top"><tr><td align="left" valign="top" charoff="50">A/1</td><td align="left" valign="top" charoff="50">Human</td><td align="left" valign="top" charoff="50">EMC/2012</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">P</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">M</td><td align="center" valign="top" charoff="50">G</td><td align="center" valign="top" charoff="50">L</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">Y</td><td align="center" valign="top" charoff="50">Q</td><td align="center" valign="top" charoff="50">S</td></tr><tr><td align="left" valign="top" charoff="50">A/1</td><td align="left" valign="top" charoff="50">Human</td><td align="left" valign="top" charoff="50">Jordan-N3 /2012</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">P</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">M</td><td align="center" valign="top" charoff="50">G</td><td align="center" valign="top" charoff="50">L</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">Y</td><td align="center" valign="top" charoff="50">Q</td><td align="center" valign="top" charoff="50">S</td></tr><tr><td align="left" valign="top" charoff="50">A/2</td><td align="left" valign="top" charoff="50">Camel</td><td align="left" valign="top" charoff="50">D998/15</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">P</td><td align="center" valign="top" charoff="50">E</td><td align="center" valign="top" charoff="50">M</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">L</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">C</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">Y</td><td align="center" valign="top" charoff="50">Q</td><td align="center" valign="top" charoff="50">S</td></tr><tr><td align="left" valign="top" charoff="50">A/2</td><td align="left" valign="top" charoff="50">Camel</td><td align="left" valign="top" charoff="50">NRCE- HKU205</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">P</td><td align="center" valign="top" charoff="50">E</td><td align="center" valign="top" charoff="50">M</td><td align="center" valign="top" charoff="50">R</td><td align="center" valign="top" charoff="50">L</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">C</td><td align="center" valign="top" charoff="50">A</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">Y</td><td align="center" valign="top" charoff="50">Q</td><td align="center" valign="top" charoff="50">S</td></tr><tr><td align="left" valign="top" charoff="50">B/5</td><td align="left" valign="top" charoff="50">Human and Camel</td><td align="left" valign="top" charoff="50">All</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">N</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">K/E</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">H</td><td align="center" valign="top" charoff="50">H/R</td><td align="center" valign="top" charoff="50">A</td></tr><tr><td align="left" valign="top" charoff="50">B/6</td><td align="left" valign="top" charoff="50">Human and Camel</td><td align="left" valign="top" charoff="50">All</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">N</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">H</td><td align="center" valign="top" charoff="50">R</td><td align="center" valign="top" charoff="50">A</td></tr><tr><td align="left" valign="top" charoff="50">B/4</td><td align="left" valign="top" charoff="50">Human and Camel</td><td align="left" valign="top" charoff="50">All</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">N</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">K/G/E</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">H</td><td align="center" valign="top" charoff="50">R</td><td align="center" valign="top" charoff="50">A</td></tr><tr><td align="left" valign="top" charoff="50">B/3</td><td align="left" valign="top" charoff="50">Human and Camel</td><td align="left" valign="top" charoff="50">All</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">N</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">K/G</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">H</td><td align="center" valign="top" charoff="50">R</td><td align="center" valign="top" charoff="50">A</td></tr><tr><td align="left" valign="top" charoff="50">B/2</td><td align="left" valign="top" charoff="50">Human and Camel</td><td align="left" valign="top" charoff="50">All</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">N</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">H</td><td align="center" valign="top" charoff="50">R</td><td align="center" valign="top" charoff="50">A</td></tr><tr><td align="left" valign="top" charoff="50">B/1</td><td align="left" valign="top" charoff="50">Human and Camel</td><td align="left" valign="top" charoff="50">All</td><td align="center" valign="top" charoff="50">T</td><td align="center" valign="top" charoff="50">N</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">S</td><td align="center" valign="top" charoff="50">K</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">K/E</td><td align="center" valign="top" charoff="50">I</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">F</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">V</td><td align="center" valign="top" charoff="50">H</td><td align="center" valign="top" charoff="50">R</td><td align="center" valign="top" charoff="50">A</td></tr></tbody></table><table-wrap-foot><fn id="t2-fn1"><p>Abbreviations: Catalytic domain, CD; N-terminal, NT; heptad region 1, HR1.</p></fn></table-wrap-foot></table-wrap></floats-group></pmc><affiliations><list><country><li>République populaire de Chine</li></country></list><tree><noCountry><name sortKey="Elizabeth, Shyna K" sort="Elizabeth, Shyna K" uniqKey="Elizabeth S" first="Shyna K" last="Elizabeth">Shyna K. Elizabeth</name><name sortKey="Joseph, Sunitha" sort="Joseph, Sunitha" uniqKey="Joseph S" first="Sunitha" last="Joseph">Sunitha Joseph</name><name sortKey="Kinne, Joerg" sort="Kinne, Joerg" uniqKey="Kinne J" first="Jöerg" last="Kinne">Jöerg Kinne</name><name sortKey="Muhammed, Rubeena" sort="Muhammed, Rubeena" uniqKey="Muhammed R" first="Rubeena" last="Muhammed">Rubeena Muhammed</name><name sortKey="Patteril, Nissy Annie Georgy" sort="Patteril, Nissy Annie Georgy" uniqKey="Patteril N" first="Nissy Annie Georgy" last="Patteril">Nissy Annie Georgy Patteril</name><name sortKey="Wernery, Renate" sort="Wernery, Renate" uniqKey="Wernery R" first="Renate" last="Wernery">Renate Wernery</name><name sortKey="Wernery, Ulrich" sort="Wernery, Ulrich" uniqKey="Wernery U" first="Ulrich" last="Wernery">Ulrich Wernery</name></noCountry><country name="République populaire de Chine"><noRegion><name sortKey="Lau, Susanna K P" sort="Lau, Susanna K P" uniqKey="Lau S" first="Susanna K P" last="Lau">Susanna K P. Lau</name></noRegion><name sortKey="Chan, Kwok Hung" sort="Chan, Kwok Hung" uniqKey="Chan K" first="Kwok-Hung" last="Chan">Kwok-Hung Chan</name><name sortKey="Lau, Susanna K P" sort="Lau, Susanna K P" uniqKey="Lau S" first="Susanna K P" last="Lau">Susanna K P. Lau</name><name sortKey="Tsang, Alan K L" sort="Tsang, Alan K L" uniqKey="Tsang A" first="Alan K L" last="Tsang">Alan K L. Tsang</name><name sortKey="Wong, Emily Y M" sort="Wong, Emily Y M" uniqKey="Wong E" first="Emily Y M" last="Wong">Emily Y M. Wong</name><name sortKey="Woo, Patrick C Y" sort="Woo, Patrick C Y" uniqKey="Woo P" first="Patrick C Y" last="Woo">Patrick C Y. Woo</name><name sortKey="Woo, Patrick C Y" sort="Woo, Patrick C Y" uniqKey="Woo P" first="Patrick C Y" last="Woo">Patrick C Y. Woo</name><name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name><name sortKey="Yuen, Kwok Yung" sort="Yuen, Kwok Yung" uniqKey="Yuen K" first="Kwok-Yung" last="Yuen">Kwok-Yung Yuen</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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