Evidence for an Ancestral Association of Human Coronavirus 229E with Bats
Identifieur interne : 000209 ( Pmc/Curation ); précédent : 000208; suivant : 000210Evidence for an Ancestral Association of Human Coronavirus 229E with Bats
Auteurs : Victor Max Corman [Allemagne] ; Heather J. Baldwin [Allemagne, Australie] ; Adriana Fumie Tateno [Allemagne, Brésil] ; Rodrigo Melim Zerbinati [Allemagne, Brésil] ; Augustina Annan [Ghana] ; Michael Owusu [Ghana] ; Evans Ewald Nkrumah [Ghana] ; Gael Darren Maganga [Gabon] ; Samuel Oppong [Ghana] ; Yaw Adu-Sarkodie [Ghana] ; Peter Vallo [Allemagne, République tchèque] ; Luiz Vicente Ribeiro Ferreira Da Silva Filho [Brésil] ; Eric M. Leroy [Gabon, France] ; Volker Thiel [Suisse] ; Lia Van Der Hoek [Pays-Bas] ; Leo L. M. Poon [République populaire de Chine] ; Marco Tschapka [Allemagne, Panama] ; Christian Drosten [Allemagne] ; Jan Felix Drexler [Allemagne]Source :
- Journal of Virology [ 0022-538X ] ; 2015.
Abstract
We previously showed that close relatives of human coronavirus 229E (HCoV-229E) exist in African bats. The small sample and limited genomic characterizations have prevented further analyses so far. Here, we tested 2,087 fecal specimens from 11 bat species sampled in Ghana for HCoV-229E-related viruses by reverse transcription-PCR (RT-PCR). Only hipposiderid bats tested positive. To compare the genetic diversity of bat viruses and HCoV-229E, we tested historical isolates and diagnostic specimens sampled globally over 10 years. Bat viruses were 5- and 6-fold more diversified than HCoV-229E in the
Url:
DOI: 10.1128/JVI.01755-15
PubMed: 26378164
PubMed Central: 4645311
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<author><name sortKey="Annan, Augustina" sort="Annan, Augustina" uniqKey="Annan A" first="Augustina" last="Annan">Augustina Annan</name>
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<author><name sortKey="Adu Sarkodie, Yaw" sort="Adu Sarkodie, Yaw" uniqKey="Adu Sarkodie Y" first="Yaw" last="Adu-Sarkodie">Yaw Adu-Sarkodie</name>
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<author><name sortKey="Leroy, Eric M" sort="Leroy, Eric M" uniqKey="Leroy E" first="Eric M." last="Leroy">Eric M. Leroy</name>
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<author><name sortKey="Thiel, Volker" sort="Thiel, Volker" uniqKey="Thiel V" first="Volker" last="Thiel">Volker Thiel</name>
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<author><name sortKey="Tschapka, Marco" sort="Tschapka, Marco" uniqKey="Tschapka M" first="Marco" last="Tschapka">Marco Tschapka</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Evidence for an Ancestral Association of Human Coronavirus 229E with Bats</title>
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<author><name sortKey="Baldwin, Heather J" sort="Baldwin, Heather J" uniqKey="Baldwin H" first="Heather J." last="Baldwin">Heather J. Baldwin</name>
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<affiliation wicri:level="1"><nlm:aff id="aff4">Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia</nlm:aff>
<country xml:lang="fr">Australie</country>
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<author><name sortKey="Tateno, Adriana Fumie" sort="Tateno, Adriana Fumie" uniqKey="Tateno A" first="Adriana Fumie" last="Tateno">Adriana Fumie Tateno</name>
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<author><name sortKey="Zerbinati, Rodrigo Melim" sort="Zerbinati, Rodrigo Melim" uniqKey="Zerbinati R" first="Rodrigo Melim" last="Zerbinati">Rodrigo Melim Zerbinati</name>
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<author><name sortKey="Annan, Augustina" sort="Annan, Augustina" uniqKey="Annan A" first="Augustina" last="Annan">Augustina Annan</name>
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<author><name sortKey="Owusu, Michael" sort="Owusu, Michael" uniqKey="Owusu M" first="Michael" last="Owusu">Michael Owusu</name>
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<author><name sortKey="Nkrumah, Evans Ewald" sort="Nkrumah, Evans Ewald" uniqKey="Nkrumah E" first="Evans Ewald" last="Nkrumah">Evans Ewald Nkrumah</name>
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<author><name sortKey="Maganga, Gael Darren" sort="Maganga, Gael Darren" uniqKey="Maganga G" first="Gael Darren" last="Maganga">Gael Darren Maganga</name>
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<author><name sortKey="Oppong, Samuel" sort="Oppong, Samuel" uniqKey="Oppong S" first="Samuel" last="Oppong">Samuel Oppong</name>
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<wicri:regionArea>Kwame Nkrumah University of Science and Technology, Kumasi</wicri:regionArea>
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<author><name sortKey="Adu Sarkodie, Yaw" sort="Adu Sarkodie, Yaw" uniqKey="Adu Sarkodie Y" first="Yaw" last="Adu-Sarkodie">Yaw Adu-Sarkodie</name>
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<author><name sortKey="Vallo, Peter" sort="Vallo, Peter" uniqKey="Vallo P" first="Peter" last="Vallo">Peter Vallo</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff9">Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic</nlm:aff>
<country xml:lang="fr">République tchèque</country>
<wicri:regionArea>Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno</wicri:regionArea>
</affiliation>
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<author><name sortKey="Da Silva Filho, Luiz Vicente Ribeiro Ferreira" sort="Da Silva Filho, Luiz Vicente Ribeiro Ferreira" uniqKey="Da Silva Filho L" first="Luiz Vicente Ribeiro Ferreira" last="Da Silva Filho">Luiz Vicente Ribeiro Ferreira Da Silva Filho</name>
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<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Laboratório de Virologia, Instituto de Medicina Tropical de São Paulo, Universidade de São Paulo, São Paulo</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff10">Instituto da Criança, Hospital das Clínicas da FMUSP, São Paulo, Brazil</nlm:aff>
<country xml:lang="fr">Brésil</country>
<wicri:regionArea>Instituto da Criança, Hospital das Clínicas da FMUSP, São Paulo</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Leroy, Eric M" sort="Leroy, Eric M" uniqKey="Leroy E" first="Eric M." last="Leroy">Eric M. Leroy</name>
<affiliation wicri:level="1"><nlm:aff id="aff7">Centre International de Recherches Médicales de Franceville, Franceville, Gabon</nlm:aff>
<country xml:lang="fr">Gabon</country>
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<country xml:lang="fr">France</country>
<wicri:regionArea>Institut de Recherche pour le Développement, UMR 224 (MIVEGEC), IRD/CNRS/UM1, Montpellier</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Thiel, Volker" sort="Thiel, Volker" uniqKey="Thiel V" first="Volker" last="Thiel">Volker Thiel</name>
<affiliation wicri:level="1"><nlm:aff id="aff12">Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty Bern, University of Bern, Bern, Switzerland</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty Bern, University of Bern, Bern</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff13">Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern, Switzerland</nlm:aff>
<country xml:lang="fr">Suisse</country>
<wicri:regionArea>Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Van Der Hoek, Lia" sort="Van Der Hoek, Lia" uniqKey="Van Der Hoek L" first="Lia" last="Van Der Hoek">Lia Van Der Hoek</name>
<affiliation wicri:level="1"><nlm:aff id="aff14">Department of Medical Microbiology, Academic Medical Center of the University of Amsterdam, Amsterdam, The Netherlands</nlm:aff>
<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Department of Medical Microbiology, Academic Medical Center of the University of Amsterdam, Amsterdam</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Poon, Leo L M" sort="Poon, Leo L M" uniqKey="Poon L" first="Leo L. M." last="Poon">Leo L. M. Poon</name>
<affiliation wicri:level="1"><nlm:aff id="aff15">School of Public Health, The University of Hong Kong, Hong Kong, Special Administrative Region, People's Republic of China</nlm:aff>
<country xml:lang="fr">République populaire de Chine</country>
<wicri:regionArea>School of Public Health, The University of Hong Kong, Hong Kong, Special Administrative Region</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Tschapka, Marco" sort="Tschapka, Marco" uniqKey="Tschapka M" first="Marco" last="Tschapka">Marco Tschapka</name>
<affiliation wicri:level="1"><nlm:aff id="aff3">Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff16">Smithsonian Tropical Research Institute, Balboa, Panama</nlm:aff>
<country xml:lang="fr">Panama</country>
<wicri:regionArea>Smithsonian Tropical Research Institute, Balboa</wicri:regionArea>
</affiliation>
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<author><name sortKey="Drosten, Christian" sort="Drosten, Christian" uniqKey="Drosten C" first="Christian" last="Drosten">Christian Drosten</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Institute of Virology, University of Bonn Medical Centre, Bonn, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute of Virology, University of Bonn Medical Centre, Bonn</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2">German Centre for Infection Research, (DZIF), Partner Site Bonn-Cologne, Bonn, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>German Centre for Infection Research, (DZIF), Partner Site Bonn-Cologne, Bonn</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Drexler, Jan Felix" sort="Drexler, Jan Felix" uniqKey="Drexler J" first="Jan Felix" last="Drexler">Jan Felix Drexler</name>
<affiliation wicri:level="1"><nlm:aff id="aff1">Institute of Virology, University of Bonn Medical Centre, Bonn, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Institute of Virology, University of Bonn Medical Centre, Bonn</wicri:regionArea>
</affiliation>
<affiliation wicri:level="1"><nlm:aff id="aff2">German Centre for Infection Research, (DZIF), Partner Site Bonn-Cologne, Bonn, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>German Centre for Infection Research, (DZIF), Partner Site Bonn-Cologne, Bonn</wicri:regionArea>
</affiliation>
</author>
</analytic>
<series><title level="j">Journal of Virology</title>
<idno type="ISSN">0022-538X</idno>
<idno type="eISSN">1098-5514</idno>
<imprint><date when="2015">2015</date>
</imprint>
</series>
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<front><div type="abstract" xml:lang="en"><title>ABSTRACT</title>
<p>We previously showed that close relatives of human coronavirus 229E (HCoV-229E) exist in African bats. The small sample and limited genomic characterizations have prevented further analyses so far. Here, we tested 2,087 fecal specimens from 11 bat species sampled in Ghana for HCoV-229E-related viruses by reverse transcription-PCR (RT-PCR). Only hipposiderid bats tested positive. To compare the genetic diversity of bat viruses and HCoV-229E, we tested historical isolates and diagnostic specimens sampled globally over 10 years. Bat viruses were 5- and 6-fold more diversified than HCoV-229E in the <italic>RNA-dependent RNA polymerase</italic>
(<italic>RdRp</italic>
) and <italic>spike</italic>
genes. In phylogenetic analyses, HCoV-229E strains were monophyletic and not intermixed with animal viruses. Bat viruses formed three large clades in close and more distant sister relationships. A recently described 229E-related alpaca virus occupied an intermediate phylogenetic position between bat and human viruses. According to taxonomic criteria, human, alpaca, and bat viruses form a single CoV species showing evidence for multiple recombination events. HCoV-229E and the alpaca virus showed a major deletion in the spike S1 region compared to all bat viruses. Analyses of four full genomes from 229E-related bat CoVs revealed an eighth open reading frame (ORF8) located at the genomic 3′ end. ORF8 also existed in the 229E-related alpaca virus. Reanalysis of HCoV-229E sequences showed a conserved transcription regulatory sequence preceding remnants of this ORF, suggesting its loss after acquisition of a 229E-related CoV by humans. These data suggested an evolutionary origin of 229E-related CoVs in hipposiderid bats, hypothetically with camelids as intermediate hosts preceding the establishment of HCoV-229E.</p>
<p><bold>IMPORTANCE</bold>
The ancestral origins of major human coronaviruses (HCoVs) likely involve bat hosts. Here, we provide conclusive genetic evidence for an evolutionary origin of the common cold virus HCoV-229E in hipposiderid bats by analyzing a large sample of African bats and characterizing several bat viruses on a full-genome level. Our evolutionary analyses show that animal and human viruses are genetically closely related, can exchange genetic material, and form a single viral species. We show that the putative host switches leading to the formation of HCoV-229E were accompanied by major genomic changes, including deletions in the viral spike glycoprotein gene and loss of an open reading frame. We reanalyze a previously described genetically related alpaca virus and discuss the role of camelids as potential intermediate hosts between bat and human viruses. The evolutionary history of HCoV-229E likely shares important characteristics with that of the recently emerged highly pathogenic Middle East respiratory syndrome (MERS) coronavirus.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Virol</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Virol</journal-id>
<journal-id journal-id-type="hwp">jvi</journal-id>
<journal-id journal-id-type="pmc">jvi</journal-id>
<journal-id journal-id-type="publisher-id">JVI</journal-id>
<journal-title-group><journal-title>Journal of Virology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0022-538X</issn>
<issn pub-type="epub">1098-5514</issn>
<publisher><publisher-name>American Society for Microbiology</publisher-name>
<publisher-loc>1752 N St., N.W., Washington, DC</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26378164</article-id>
<article-id pub-id-type="pmc">4645311</article-id>
<article-id pub-id-type="publisher-id">01755-15</article-id>
<article-id pub-id-type="doi">10.1128/JVI.01755-15</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Genetic Diversity and Evolution</subject>
</subj-group>
</article-categories>
<title-group><article-title>Evidence for an Ancestral Association of Human Coronavirus 229E with Bats</article-title>
<alt-title alt-title-type="running-head">HCoV-229E-Related Bat Coronaviruses</alt-title>
<alt-title alt-title-type="short-authors">Corman et al.</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Corman</surname>
<given-names>Victor Max</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"><name><surname>Baldwin</surname>
<given-names>Heather J.</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff4"><sup>d</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tateno</surname>
<given-names>Adriana Fumie</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zerbinati</surname>
<given-names>Rodrigo Melim</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Annan</surname>
<given-names>Augustina</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Owusu</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Nkrumah</surname>
<given-names>Evans Ewald</given-names>
</name>
<xref ref-type="aff" rid="aff6"><sup>f</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Maganga</surname>
<given-names>Gael Darren</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Oppong</surname>
<given-names>Samuel</given-names>
</name>
<xref ref-type="aff" rid="aff8"><sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Adu-Sarkodie</surname>
<given-names>Yaw</given-names>
</name>
<xref ref-type="aff" rid="aff8"><sup>h</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Vallo</surname>
<given-names>Peter</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff9"><sup>i</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>da Silva Filho</surname>
<given-names>Luiz Vicente Ribeiro Ferreira</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>e</sup>
</xref>
<xref ref-type="aff" rid="aff10"><sup>j</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Leroy</surname>
<given-names>Eric M.</given-names>
</name>
<xref ref-type="aff" rid="aff7"><sup>g</sup>
</xref>
<xref ref-type="aff" rid="aff11"><sup>k</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thiel</surname>
<given-names>Volker</given-names>
</name>
<xref ref-type="aff" rid="aff12"><sup>l</sup>
</xref>
<xref ref-type="aff" rid="aff13"><sup>m</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>van der Hoek</surname>
<given-names>Lia</given-names>
</name>
<xref ref-type="aff" rid="aff14"><sup>n</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Poon</surname>
<given-names>Leo L. M.</given-names>
</name>
<xref ref-type="aff" rid="aff15"><sup>o</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Tschapka</surname>
<given-names>Marco</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>c</sup>
</xref>
<xref ref-type="aff" rid="aff16"><sup>p</sup>
</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Drosten</surname>
<given-names>Christian</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" corresp="yes"><name><surname>Drexler</surname>
<given-names>Jan Felix</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>a</sup>
</xref>
<xref ref-type="aff" rid="aff2"><sup>b</sup>
</xref>
</contrib>
<aff id="aff1"><label>a</label>
Institute of Virology, University of Bonn Medical Centre, Bonn, Germany</aff>
<aff id="aff2"><label>b</label>
German Centre for Infection Research, (DZIF), Partner Site Bonn-Cologne, Bonn, Germany</aff>
<aff id="aff3"><label>c</label>
Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Ulm, Germany</aff>
<aff id="aff4"><label>d</label>
Department of Biological Sciences, Macquarie University, Sydney, New South Wales, Australia</aff>
<aff id="aff5"><label>e</label>
Laboratório de Virologia, Instituto de Medicina Tropical de São Paulo, Universidade de São Paulo, São Paulo, Brazil</aff>
<aff id="aff6"><label>f</label>
Kumasi Centre for Collaborative Research in Tropical Medicine, Kumasi, Ghana</aff>
<aff id="aff7"><label>g</label>
Centre International de Recherches Médicales de Franceville, Franceville, Gabon</aff>
<aff id="aff8"><label>h</label>
Kwame Nkrumah University of Science and Technology, Kumasi, Ghana</aff>
<aff id="aff9"><label>i</label>
Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic</aff>
<aff id="aff10"><label>j</label>
Instituto da Criança, Hospital das Clínicas da FMUSP, São Paulo, Brazil</aff>
<aff id="aff11"><label>k</label>
Institut de Recherche pour le Développement, UMR 224 (MIVEGEC), IRD/CNRS/UM1, Montpellier, France</aff>
<aff id="aff12"><label>l</label>
Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty Bern, University of Bern, Bern, Switzerland</aff>
<aff id="aff13"><label>m</label>
Federal Department of Home Affairs, Institute of Virology and Immunology, Bern and Mittelhäusern, Switzerland</aff>
<aff id="aff14"><label>n</label>
Department of Medical Microbiology, Academic Medical Center of the University of Amsterdam, Amsterdam, The Netherlands</aff>
<aff id="aff15"><label>o</label>
School of Public Health, The University of Hong Kong, Hong Kong, Special Administrative Region, People's Republic of China</aff>
<aff id="aff16"><label>p</label>
Smithsonian Tropical Research Institute, Balboa, Panama</aff>
</contrib-group>
<contrib-group><contrib contrib-type="editor"><name><surname>Schultz-Cherry</surname>
<given-names>S.</given-names>
</name>
<role>Editor</role>
</contrib>
</contrib-group>
<author-notes><corresp id="cor1">Address correspondence to Christian Drosten, <email>drosten@virology-bonn.de</email>
, or Jan Felix Drexler, <email>drexler@virology-bonn.de</email>
.</corresp>
<fn fn-type="equal"><p>V.M.C, H.J.B., and A.F.T. contributed equally to this article.</p>
</fn>
<fn fn-type="other"><p><bold>Citation</bold>
Corman VM, Baldwin HJ, Tateno AF, Zerbinati RM, Annan A, Owusu M, Nkrumah EE, Maganga GD, Oppong S, Adu-Sarkodie Y, Vallo P, da Silva Filho LVRF, Leroy EM, Thiel V, van der Hoek L, Poon LLM, Tschapka M, Drosten C, Drexler JF. 2015. Evidence for an ancestral association of human coronavirus 229E with bats. J Virol 89:11858–11870. doi:<ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.1128/JVI.01755-15">10.1128/JVI.01755-15</ext-link>
.</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>16</day>
<month>9</month>
<year>2015</year>
</pub-date>
<pub-date pub-type="collection"><day>1</day>
<month>12</month>
<year>2015</year>
</pub-date>
<volume>89</volume>
<issue>23</issue>
<fpage>11858</fpage>
<lpage>11870</lpage>
<history><date date-type="received"><day>9</day>
<month>7</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>7</day>
<month>9</month>
<year>2015</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2015, American Society for Microbiology. All Rights Reserved.</copyright-statement>
<copyright-year>2015</copyright-year>
<copyright-holder>American Society for Microbiology</copyright-holder>
</permissions>
<self-uri content-type="pdf" xlink:href="zjv02315011858.pdf"></self-uri>
<abstract><title>ABSTRACT</title>
<p>We previously showed that close relatives of human coronavirus 229E (HCoV-229E) exist in African bats. The small sample and limited genomic characterizations have prevented further analyses so far. Here, we tested 2,087 fecal specimens from 11 bat species sampled in Ghana for HCoV-229E-related viruses by reverse transcription-PCR (RT-PCR). Only hipposiderid bats tested positive. To compare the genetic diversity of bat viruses and HCoV-229E, we tested historical isolates and diagnostic specimens sampled globally over 10 years. Bat viruses were 5- and 6-fold more diversified than HCoV-229E in the <italic>RNA-dependent RNA polymerase</italic>
(<italic>RdRp</italic>
) and <italic>spike</italic>
genes. In phylogenetic analyses, HCoV-229E strains were monophyletic and not intermixed with animal viruses. Bat viruses formed three large clades in close and more distant sister relationships. A recently described 229E-related alpaca virus occupied an intermediate phylogenetic position between bat and human viruses. According to taxonomic criteria, human, alpaca, and bat viruses form a single CoV species showing evidence for multiple recombination events. HCoV-229E and the alpaca virus showed a major deletion in the spike S1 region compared to all bat viruses. Analyses of four full genomes from 229E-related bat CoVs revealed an eighth open reading frame (ORF8) located at the genomic 3′ end. ORF8 also existed in the 229E-related alpaca virus. Reanalysis of HCoV-229E sequences showed a conserved transcription regulatory sequence preceding remnants of this ORF, suggesting its loss after acquisition of a 229E-related CoV by humans. These data suggested an evolutionary origin of 229E-related CoVs in hipposiderid bats, hypothetically with camelids as intermediate hosts preceding the establishment of HCoV-229E.</p>
<p><bold>IMPORTANCE</bold>
The ancestral origins of major human coronaviruses (HCoVs) likely involve bat hosts. Here, we provide conclusive genetic evidence for an evolutionary origin of the common cold virus HCoV-229E in hipposiderid bats by analyzing a large sample of African bats and characterizing several bat viruses on a full-genome level. Our evolutionary analyses show that animal and human viruses are genetically closely related, can exchange genetic material, and form a single viral species. We show that the putative host switches leading to the formation of HCoV-229E were accompanied by major genomic changes, including deletions in the viral spike glycoprotein gene and loss of an open reading frame. We reanalyze a previously described genetically related alpaca virus and discuss the role of camelids as potential intermediate hosts between bat and human viruses. The evolutionary history of HCoV-229E likely shares important characteristics with that of the recently emerged highly pathogenic Middle East respiratory syndrome (MERS) coronavirus.</p>
</abstract>
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