Discovery of Bat Coronaviruses through Surveillance and Probe Capture-Based Next-Generation Sequencing
Identifieur interne : 000092 ( Pmc/Checkpoint ); précédent : 000091; suivant : 000093Discovery of Bat Coronaviruses through Surveillance and Probe Capture-Based Next-Generation Sequencing
Auteurs : Bei Li [République populaire de Chine] ; Hao-Rui Si [République populaire de Chine] ; Yan Zhu [République populaire de Chine] ; Xing-Lou Yang [République populaire de Chine] ; Danielle E. Anderson [Singapour] ; Zheng-Li Shi [République populaire de Chine] ; Lin-Fa Wang [Singapour] ; Peng Zhou [République populaire de Chine]Source :
- mSphere [ 2379-5042 ] ; 2020.
Abstract
Active surveillance is both urgent and essential to predict and mitigate the emergence of bat-origin CoV in humans and livestock. However, great genetic diversity increases the chance of homologous recombination among CoVs. Performing targeted PCR, a common practice for many surveillance studies, would not reflect this diversity. NGS, on the other hand, is an expensive methodology and is prone to missing low-abundance CoV sequences. Here, we employ a capture-based NGS approach using baits targeting all CoVs. Our work demonstrates that targeted, cost-effective, large-scale, genome-level surveillance of bat CoVs is now highly feasible.
Url:
DOI: 10.1128/mSphere.00807-19
PubMed: 31996413
PubMed Central: 6992374
Affiliations:
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PMC:6992374Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Discovery of Bat Coronaviruses through Surveillance and Probe Capture-Based Next-Generation Sequencing</title><author><name sortKey="Li, Bei" sort="Li, Bei" uniqKey="Li B" first="Bei" last="Li">Bei Li</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Si, Hao Rui" sort="Si, Hao Rui" uniqKey="Si H" first="Hao-Rui" last="Si">Hao-Rui Si</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>University of Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>University of Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zhu, Yan" sort="Zhu, Yan" uniqKey="Zhu Y" first="Yan" last="Zhu">Yan Zhu</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Yang, Xing Lou" sort="Yang, Xing Lou" uniqKey="Yang X" first="Xing-Lou" last="Yang">Xing-Lou Yang</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Anderson, Danielle E" sort="Anderson, Danielle E" uniqKey="Anderson D" first="Danielle E." last="Anderson">Danielle E. Anderson</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore</addr-line></nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Shi, Zheng Li" sort="Shi, Zheng Li" uniqKey="Shi Z" first="Zheng-Li" last="Shi">Zheng-Li Shi</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, 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China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31996413</idno><idno type="pmc">6992374</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6992374</idno><idno type="RBID">PMC:6992374</idno><idno type="doi">10.1128/mSphere.00807-19</idno><date when="2020">2020</date><idno type="wicri:Area/Pmc/Corpus">001254</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001254</idno><idno type="wicri:Area/Pmc/Curation">001254</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">001254</idno><idno 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type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Si, Hao Rui" sort="Si, Hao Rui" uniqKey="Si H" first="Hao-Rui" last="Si">Hao-Rui Si</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff2"><addr-line>University of Chinese Academy of Sciences, Beijing, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>University of Chinese Academy of Sciences, Beijing</wicri:regionArea><placeName><settlement type="city">Pékin</settlement></placeName></affiliation></author><author><name sortKey="Zhu, Yan" sort="Zhu, Yan" uniqKey="Zhu Y" first="Yan" last="Zhu">Yan Zhu</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Yang, Xing Lou" sort="Yang, Xing Lou" uniqKey="Yang X" first="Xing-Lou" last="Yang">Xing-Lou Yang</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Anderson, Danielle E" sort="Anderson, Danielle E" uniqKey="Anderson D" first="Danielle E." last="Anderson">Danielle E. Anderson</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore</addr-line></nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Shi, Zheng Li" sort="Shi, Zheng Li" uniqKey="Shi Z" first="Zheng-Li" last="Shi">Zheng-Li Shi</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author><author><name sortKey="Wang, Lin Fa" sort="Wang, Lin Fa" uniqKey="Wang L" first="Lin-Fa" last="Wang">Lin-Fa Wang</name><affiliation wicri:level="1"><nlm:aff id="aff3"><addr-line>Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore</addr-line></nlm:aff><country xml:lang="fr">Singapour</country><wicri:regionArea>Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore</wicri:regionArea><wicri:noRegion>Singapore</wicri:noRegion></affiliation></author><author><name sortKey="Zhou, Peng" sort="Zhou, Peng" uniqKey="Zhou P" first="Peng" last="Zhou">Peng Zhou</name><affiliation wicri:level="3"><nlm:aff id="aff1"><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></nlm:aff><country xml:lang="fr">République populaire de Chine</country><wicri:regionArea>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan</wicri:regionArea><placeName><settlement type="city">Wuhan</settlement><region type="région">Hubei</region></placeName></affiliation></author></analytic><series><title level="j">mSphere</title><idno type="eISSN">2379-5042</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Active surveillance is both urgent and essential to predict and mitigate the emergence of bat-origin CoV in humans and livestock. However, great genetic diversity increases the chance of homologous recombination among CoVs. Performing targeted PCR, a common practice for many surveillance studies, would not reflect this diversity. NGS, on the other hand, is an expensive methodology and is prone to missing low-abundance CoV sequences. Here, we employ a capture-based NGS approach using baits targeting all CoVs. Our work demonstrates that targeted, cost-effective, large-scale, genome-level surveillance of bat CoVs is now highly feasible.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Forni, D" uniqKey="Forni D">D Forni</name></author><author><name sortKey="Cagliani, R" uniqKey="Cagliani R">R Cagliani</name></author><author><name sortKey="Clerici, M" uniqKey="Clerici M">M Clerici</name></author><author><name sortKey="Sironi, M" uniqKey="Sironi M">M Sironi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Woo, Pc" uniqKey="Woo P">PC Woo</name></author><author><name sortKey="Lau, Sk" uniqKey="Lau S">SK Lau</name></author><author><name sortKey="Huang, Y" uniqKey="Huang Y">Y Huang</name></author><author><name sortKey="Yuen, Ky" uniqKey="Yuen K">KY Yuen</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lau, Sk" uniqKey="Lau S">SK Lau</name></author><author><name sortKey="Woo, 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<front><journal-meta><journal-id journal-id-type="nlm-ta">mSphere</journal-id><journal-id journal-id-type="iso-abbrev">mSphere</journal-id><journal-id journal-id-type="hwp">msph</journal-id><journal-id journal-id-type="pmc">msph</journal-id><journal-id journal-id-type="publisher-id">mSphere</journal-id><journal-title-group><journal-title>mSphere</journal-title></journal-title-group><issn pub-type="epub">2379-5042</issn><publisher><publisher-name>American Society for Microbiology</publisher-name><publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31996413</article-id><article-id pub-id-type="pmc">6992374</article-id><article-id pub-id-type="publisher-id">mSphere00807-19</article-id><article-id pub-id-type="doi">10.1128/mSphere.00807-19</article-id><article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject></subj-group><subj-group subj-group-type="overline"><subject>Clinical Science and Epidemiology</subject></subj-group></article-categories><title-group><article-title>Discovery of Bat Coronaviruses through Surveillance and Probe Capture-Based Next-Generation Sequencing</article-title><alt-title alt-title-type="running-head">Bat Coronavirus Capture NGS</alt-title><alt-title alt-title-type="short-authors">Li et al.</alt-title></title-group><contrib-group><contrib contrib-type="author" equal-contrib="yes"><name><surname>Li</surname><given-names>Bei</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author" equal-contrib="yes"><name><surname>Si</surname><given-names>Hao-Rui</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Zhu</surname><given-names>Yan</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Yang</surname><given-names>Xing-Lou</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><name><surname>Anderson</surname><given-names>Danielle E.</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author" equal-contrib="no"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-8089-163X</contrib-id><name><surname>Shi</surname><given-names>Zheng-Li</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author" corresp="yes" equal-contrib="no"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0003-2752-0535</contrib-id><name><surname>Wang</surname><given-names>Lin-Fa</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author" corresp="yes" equal-contrib="no"><contrib-id contrib-id-type="orcid" authenticated="false">https://orcid.org/0000-0001-9863-4201</contrib-id><name><surname>Zhou</surname><given-names>Peng</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><aff id="aff1"><label>a</label><addr-line>CAS Key Laboratory of Special Pathogens, Wuhan Institute of Virology, Center for Biosafety Mega-Science, Chinese Academy of Sciences, Wuhan, China</addr-line></aff><aff id="aff2"><label>b</label><addr-line>University of Chinese Academy of Sciences, Beijing, China</addr-line></aff><aff id="aff3"><label>c</label><addr-line>Programme in Emerging Infectious Diseases, Duke-NUS Medical School, Singapore, Singapore</addr-line></aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Frieman</surname><given-names>Matthew B.</given-names></name><role>Editor</role><aff>University of Maryland, College Park</aff></contrib></contrib-group><author-notes><corresp id="cor1">Address correspondence to Lin-Fa Wang, <email>linfa.wang@duke-nus.edu.sg</email>, or Peng Zhou, <email>peng.zhou@wh.iov.cn</email>.</corresp><fn fn-type="equal"><p>Bei Li and Hao-Rui Si contributed equally. Author order was determined by the importance of their work.</p></fn><fn fn-type="other"><p><bold>Citation</bold> Li B, Si H-R, Zhu Y, Yang X-L, Anderson DE, Shi Z-L, Wang L-F, Zhou P. 2020. Discovery of bat coronaviruses through surveillance and probe capture-based next-generation sequencing. mSphere 5:e00807-19. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.1128/mSphere.00807-19">https://doi.org/10.1128/mSphere.00807-19</ext-link>.</p></fn></author-notes><pub-date pub-type="collection"><season>Jan-Feb</season><year>2020</year></pub-date><pub-date pub-type="epub"><day>29</day><month>1</month><year>2020</year></pub-date><volume>5</volume><issue>1</issue><elocation-id>e00807-19</elocation-id><history><date date-type="received"><day>6</day><month>11</month><year>2019</year></date><date date-type="accepted"><day>19</day><month>12</month><year>2019</year></date></history><permissions><copyright-statement>Copyright © 2020 Li et al.</copyright-statement><copyright-year>2020</copyright-year><copyright-holder>Li et al.</copyright-holder><license license-type="open-access" xlink:href="https://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution 4.0 International license</ext-link>.</license-p></license></permissions><self-uri content-type="pdf" xlink:href="mSphere.00807-19.pdf"></self-uri><abstract abstract-type="precis"><p>Active surveillance is both urgent and essential to predict and mitigate the emergence of bat-origin CoV in humans and livestock. However, great genetic diversity increases the chance of homologous recombination among CoVs. Performing targeted PCR, a common practice for many surveillance studies, would not reflect this diversity. NGS, on the other hand, is an expensive methodology and is prone to missing low-abundance CoV sequences. Here, we employ a capture-based NGS approach using baits targeting all CoVs. Our work demonstrates that targeted, cost-effective, large-scale, genome-level surveillance of bat CoVs is now highly feasible.</p></abstract><abstract><title>ABSTRACT</title><p>Coronaviruses (CoVs) of bat origin have caused two pandemics in this century. Severe acute respiratory syndrome (SARS)-CoV and Middle East respiratory syndrome (MERS)-CoV both originated from bats, and it is highly likely that bat coronaviruses will cause future outbreaks. Active surveillance is both urgent and essential to predict and mitigate the emergence of these viruses in humans. Next-generation sequencing (NGS) is currently the preferred methodology for virus discovery to ensure unbiased sequencing of bat CoVs, considering their high genetic diversity. However, unbiased NGS is an expensive methodology and is prone to missing low-abundance CoV sequences due to the high background level of nonviral sequences present in surveillance field samples. Here, we employ a capture-based NGS approach using baits targeting most of the CoV species. Using this technology, we effectively reduced sequencing costs by increasing the sensitivity of detection. We discovered nine full genomes of bat CoVs in this study and revealed great genetic diversity for eight of them.</p><p><bold>IMPORTANCE</bold> Active surveillance is both urgent and essential to predict and mitigate the emergence of bat-origin CoV in humans and livestock. However, great genetic diversity increases the chance of homologous recombination among CoVs. Performing targeted PCR, a common practice for many surveillance studies, would not reflect this diversity. NGS, on the other hand, is an expensive methodology and is prone to missing low-abundance CoV sequences. Here, we employ a capture-based NGS approach using baits targeting all CoVs. Our work demonstrates that targeted, cost-effective, large-scale, genome-level surveillance of bat CoVs is now highly feasible.</p></abstract><kwd-group><title>KEYWORDS</title><kwd>bat</kwd><kwd>coronavirus</kwd><kwd>genome</kwd><kwd>enrichment</kwd><kwd>next-generation sequencing</kwd></kwd-group><funding-group><award-group id="award1"><funding-source><institution-wrap><institution>Chinese Academy of Sciences (CAS)</institution><institution-id>https://doi.org/10.13039/501100002367</institution-id></institution-wrap></funding-source><award-id>XDB29010204, XDB29010101</award-id><principal-award-recipient><name><surname>Shi</surname><given-names>Zheng-Li</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Zhou</surname><given-names>Peng</given-names></name></principal-award-recipient></award-group><award-group id="award2"><funding-source><institution-wrap><institution>Ministry of Health -Singapore (MOH)</institution><institution-id>https://doi.org/10.13039/501100001350</institution-id></institution-wrap></funding-source><award-id>CDPHRG/0006/2014</award-id><principal-award-recipient><name><surname>Wang</surname><given-names>Lin-Fa</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Anderson</surname><given-names>Danielle E.</given-names></name></principal-award-recipient></award-group><award-group id="award3"><funding-source><institution-wrap><institution>MOH | National Medical Research Council (NMRC)</institution><institution-id>https://doi.org/10.13039/501100001349</institution-id></institution-wrap></funding-source><award-id>ZRRF16006</award-id><principal-award-recipient><name><surname>Wang</surname><given-names>Lin-Fa</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Anderson</surname><given-names>Danielle E.</given-names></name></principal-award-recipient></award-group><award-group id="award4"><funding-source><institution-wrap><institution>National Research Foundation Singapore (NRF)</institution><institution-id>https://doi.org/10.13039/501100001381</institution-id></institution-wrap></funding-source><award-id>NRF2016NRF-NSFC002-013, NRF2012NRF-CRP001-056</award-id><principal-award-recipient><name><surname>Wang</surname><given-names>Lin-Fa</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Anderson</surname><given-names>Danielle E.</given-names></name></principal-award-recipient></award-group><award-group id="award5"><funding-source><institution-wrap><institution>NSF | Foundation for Innovative Research Groups of the National Natural Science Foundation of China</institution><institution-id>https://doi.org/10.13039/501100012659</institution-id></institution-wrap></funding-source><award-id>81822028 81661148058</award-id><principal-award-recipient><name><surname>Zhou</surname><given-names>Peng</given-names></name></principal-award-recipient></award-group><award-group id="award6"><funding-source><institution-wrap><institution>MOST | National Science and Technology Program during the Twelfth Five-year Plan Period (National Science and Technology Program of China)</institution><institution-id>https://doi.org/10.13039/501100013385</institution-id></institution-wrap></funding-source><award-id>2018ZX10305409-004-001</award-id><principal-award-recipient><name><surname>Zhou</surname><given-names>Peng</given-names></name></principal-award-recipient></award-group><award-group id="award7"><funding-source><institution-wrap><institution>Ministry of Defence (MINDEF)</institution><institution-id>https://doi.org/10.13039/501100001463</institution-id></institution-wrap></funding-source><award-id>DIRP2015-9016102060</award-id><principal-award-recipient><name><surname>Wang</surname><given-names>Lin-Fa</given-names></name></principal-award-recipient><principal-award-recipient><name><surname>Anderson</surname><given-names>Danielle E.</given-names></name></principal-award-recipient></award-group></funding-group><counts><count count="3" count-type="supplementary-material"></count><fig-count count="3"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="25"></ref-count><page-count count="10"></page-count><word-count count="6381"></word-count></counts><custom-meta-group><custom-meta><meta-name>cover-date</meta-name><meta-value>January/February 2020</meta-value></custom-meta></custom-meta-group></article-meta></front></pmc><affiliations><list><country><li>République populaire de Chine</li><li>Singapour</li></country><region><li>Hubei</li></region><settlement><li>Pékin</li><li>Wuhan</li></settlement></list><tree><country name="République populaire de Chine"><region name="Hubei"><name sortKey="Li, Bei" sort="Li, Bei" uniqKey="Li B" first="Bei" last="Li">Bei Li</name></region><name sortKey="Shi, Zheng Li" sort="Shi, Zheng Li" uniqKey="Shi Z" first="Zheng-Li" last="Shi">Zheng-Li Shi</name><name sortKey="Si, Hao Rui" sort="Si, Hao Rui" uniqKey="Si H" first="Hao-Rui" last="Si">Hao-Rui Si</name><name sortKey="Si, Hao Rui" sort="Si, Hao Rui" uniqKey="Si H" first="Hao-Rui" last="Si">Hao-Rui Si</name><name sortKey="Yang, Xing Lou" sort="Yang, Xing Lou" uniqKey="Yang X" first="Xing-Lou" last="Yang">Xing-Lou Yang</name><name sortKey="Zhou, Peng" sort="Zhou, Peng" uniqKey="Zhou P" first="Peng" last="Zhou">Peng Zhou</name><name sortKey="Zhu, Yan" sort="Zhu, Yan" uniqKey="Zhu Y" first="Yan" last="Zhu">Yan Zhu</name></country><country name="Singapour"><noRegion><name sortKey="Anderson, Danielle E" sort="Anderson, Danielle E" uniqKey="Anderson D" first="Danielle E." last="Anderson">Danielle E. Anderson</name></noRegion><name sortKey="Wang, Lin Fa" sort="Wang, Lin Fa" uniqKey="Wang L" first="Lin-Fa" last="Wang">Lin-Fa Wang</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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