Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS
Identifieur interne : 001689 ( Pmc/Corpus ); précédent : 001688; suivant : 001690Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS
Auteurs : Jan Felix Drexler ; Victor Max Corman ; Christian DrostenSource :
- Antiviral Research [ 0166-3542 ] ; 2013.
Abstract
The SARS epidemic drew attention to bats as major coronavirus hosts. The known coronavirus genetic diversity is much higher in bats than in any other mammalian host. Lack of bat coronavirus isolates and full genomes challenge taxonomic classification. Viruses closely related to SARS-CoV, MERS-CoV and HCoV-229E exist in bats. Mechanisms of putative host switches from bats into humans are unknown.
Url:
DOI: 10.1016/j.antiviral.2013.10.013
PubMed: 24184128
PubMed Central: 7113851
Links to Exploration step
PMC:7113851Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS</title><author><name sortKey="Drexler, Jan Felix" sort="Drexler, Jan Felix" uniqKey="Drexler J" first="Jan Felix" last="Drexler">Jan Felix Drexler</name></author><author><name sortKey="Corman, Victor Max" sort="Corman, Victor Max" uniqKey="Corman V" first="Victor Max" last="Corman">Victor Max Corman</name></author><author><name sortKey="Drosten, Christian" sort="Drosten, Christian" uniqKey="Drosten C" first="Christian" last="Drosten">Christian Drosten</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24184128</idno><idno type="pmc">7113851</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7113851</idno><idno type="RBID">PMC:7113851</idno><idno type="doi">10.1016/j.antiviral.2013.10.013</idno><date when="2013">2013</date><idno type="wicri:Area/Pmc/Corpus">001689</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001689</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS</title><author><name sortKey="Drexler, Jan Felix" sort="Drexler, Jan Felix" uniqKey="Drexler J" first="Jan Felix" last="Drexler">Jan Felix Drexler</name></author><author><name sortKey="Corman, Victor Max" sort="Corman, Victor Max" uniqKey="Corman V" first="Victor Max" last="Corman">Victor Max Corman</name></author><author><name sortKey="Drosten, Christian" sort="Drosten, Christian" uniqKey="Drosten C" first="Christian" last="Drosten">Christian Drosten</name></author></analytic><series><title level="j">Antiviral Research</title><idno type="ISSN">0166-3542</idno><idno type="eISSN">1872-9096</idno><imprint><date when="2013">2013</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Highlights</title><p><list list-type="simple" id="l0005"><list-item id="o0005"><label>•</label><p id="p0235">The SARS epidemic drew attention to bats as major coronavirus hosts.</p></list-item><list-item id="o0010"><label>•</label><p id="p0240">The known coronavirus genetic diversity is much higher in bats than in any other mammalian host.</p></list-item><list-item id="o0015"><label>•</label><p id="p0245">Lack of bat coronavirus isolates and full genomes challenge taxonomic classification.</p></list-item><list-item id="o0020"><label>•</label><p id="p0250">Viruses closely related to SARS-CoV, MERS-CoV and HCoV-229E exist in bats.</p></list-item><list-item id="o0025"><label>•</label><p id="p0255">Mechanisms of putative host switches from bats into humans are unknown.</p></list-item></list></p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Adams, M J" uniqKey="Adams M">M.J. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Antiviral Res</journal-id><journal-id journal-id-type="iso-abbrev">Antiviral Res</journal-id><journal-title-group><journal-title>Antiviral Research</journal-title></journal-title-group><issn pub-type="ppub">0166-3542</issn><issn pub-type="epub">1872-9096</issn><publisher><publisher-name>Elsevier B.V.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24184128</article-id><article-id pub-id-type="pmc">7113851</article-id><article-id pub-id-type="publisher-id">S0166-3542(13)00316-1</article-id><article-id pub-id-type="doi">10.1016/j.antiviral.2013.10.013</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Ecology, evolution and classification of bat coronaviruses in the aftermath of SARS</article-title></title-group><contrib-group><contrib contrib-type="author" id="au005"><name><surname>Drexler</surname><given-names>Jan Felix</given-names></name><email>drexler@virology-bonn.de</email><xref rid="cor1" ref-type="corresp">⁎</xref></contrib><contrib contrib-type="author" id="au010"><name><surname>Corman</surname><given-names>Victor Max</given-names></name></contrib><contrib contrib-type="author" id="au015"><name><surname>Drosten</surname><given-names>Christian</given-names></name></contrib></contrib-group><aff id="af005">Institute of Virology, University of Bonn Medical Centre, Germany</aff><author-notes><corresp id="cor1"><label>⁎</label>Corresponding author. Address: Institute of Virology, University of Bonn Medical Centre, 53127 Bonn, Germany. Tel.: +49 228 287 11697; fax: +49 228 287 19144. <email>drexler@virology-bonn.de</email></corresp></author-notes><pub-date pub-type="pmc-release"><day>31</day><month>10</month><year>2013</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>1</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>31</day><month>10</month><year>2013</year></pub-date><volume>101</volume><fpage>45</fpage><lpage>56</lpage><permissions><copyright-statement>Copyright © 2013 Elsevier B.V. All rights reserved.</copyright-statement><copyright-year>2013</copyright-year><copyright-holder>Elsevier B.V.</copyright-holder><license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p></license></permissions><abstract abstract-type="author-highlights" id="ab005"><title>Highlights</title><p><list list-type="simple" id="l0005"><list-item id="o0005"><label>•</label><p id="p0235">The SARS epidemic drew attention to bats as major coronavirus hosts.</p></list-item><list-item id="o0010"><label>•</label><p id="p0240">The known coronavirus genetic diversity is much higher in bats than in any other mammalian host.</p></list-item><list-item id="o0015"><label>•</label><p id="p0245">Lack of bat coronavirus isolates and full genomes challenge taxonomic classification.</p></list-item><list-item id="o0020"><label>•</label><p id="p0250">Viruses closely related to SARS-CoV, MERS-CoV and HCoV-229E exist in bats.</p></list-item><list-item id="o0025"><label>•</label><p id="p0255">Mechanisms of putative host switches from bats into humans are unknown.</p></list-item></list></p></abstract><abstract id="ab010"><p>In 2002/2003, a novel coronavirus (CoV) caused a pandemic, infecting more than 8000 people, of whom nearly 10% died. This virus, termed <italic>severe acute respiratory syndrome-</italic>CoV was linked to a zoonotic origin from rhinolophid bats in 2005. Since then, numerous studies have described novel bat CoVs, including close relatives of the newly emerging <italic>Middle East respiratory syndrome</italic> (MERS)-CoV. In this paper we discuss CoV genomic properties and compare different taxonomic approaches in light of the technical difficulties of obtaining full genomic sequences directly from bat specimens. We first present an overview of the available studies on bat CoVs, with details on their chiropteran hosts, then comparatively analyze the increase in bat CoV studies and novel genomic sequences obtained since the SARS pandemic. We then conduct a comprehensive phylogenetic analysis of the genera <italic>Alpha</italic>- and <italic>Betacoronavirus</italic>, to show that bats harbour more CoV diversity than other mammalian hosts and are widely represented in most, but not all parts of the tree of mammalian CoVs. We next discuss preliminary evidence for phylogenetic co-segregation of CoVs and bat hosts encompassing the <italic>Betacoronavirus</italic> clades b and d, with an emphasis on the sampling bias that exists among bat species and other mammals, then present examples of CoVs infecting different hosts on the one hand and viruses apparently confined to host genera on the other. We also demonstrate a geographic bias within available studies on bat CoVs, and identify a critical lack of information from biodiversity hotspots in Africa, Asia and Latin America. We then present evidence for a zoonotic origin of four of the six known human CoVs (HCoV), three of which likely involved bats, namely SARS-CoV, MERS-CoV and HCoV-229E; compare the available data on CoV pathogenesis in bats to that in other mammalian hosts; and discuss hypotheses on the putative insect origins of CoV ancestors. Finally, we suggest caution with conclusions on the zoonotic potential of bat viruses, based only on genomic sequence data, and emphasize the need to preserve these ecologically highly relevant animals. This paper forms part of a symposium in <italic>Antiviral Research</italic> on “from SARS to MERS: 10 years of research on highly pathogenic human coronaviruses”.</p></abstract><kwd-group id="kg005"><title>Keywords</title><kwd>Coronaviridae</kwd><kwd>Alphacoronavirus</kwd><kwd>Betacoronavirus</kwd><kwd>Bats</kwd><kwd>Zoonosis</kwd><kwd>Taxonomy</kwd></kwd-group></article-meta></front><body><sec id="s0005"><label>1</label><title>Introduction</title><p id="p0005">In 2002/2003, an outbreak of severe respiratory disease occurred, infecting 8096 people worldwide and killing 774 (9.5%) of them. A novel human coronavirus (CoV) named <italic>severe acute respiratory syndrome</italic> (SARS)-CoV was identified as the causative agent (<xref rid="b0180" ref-type="bibr">Drosten et al., 2003</xref>). This virus was much more pathogenic than previously known human coronaviruses (HCoV) mainly causing mild respiratory disease (<xref rid="b0615" ref-type="bibr">van der Hoek, 2007</xref>). The clinical aspects of the SARS epidemic and research on the SARS-CoV have been reviewed in two other articles in the present series (<xref rid="b0080" ref-type="bibr">Cheng et al., 2013</xref>, <xref rid="b0280" ref-type="bibr">Hilgenfeld and Peiris, 2013</xref>).</p><p id="p0010">Animal CoV have been known since the late 1930s, including viruses that are highly pathogenic for livestock, pet and laboratory animals, such as <italic>transmissible gastroenteritis virus of swine</italic> (TGEV), <italic>bovine CoV</italic> (BCoV), <italic>feline infectious peritonitis virus</italic> (FIPV), <italic>mouse hepatitis virus</italic> (MHV) and <italic>infectious bronchitis virus</italic> (IBV) (<xref rid="b0555" ref-type="bibr">Saif, 2004</xref>). The earliest descriptions of two HCoVs termed HCoV-229E and -OC43 were already made in the 1960s (<xref rid="b0260" ref-type="bibr">Hamre and Procknow, 1966</xref>, <xref rid="b0425" ref-type="bibr">McIntosh et al., 1967</xref>). In the SARS aftermath, two additional HCoV termed -NL63 and -HKU1 were detected (<xref rid="b0625" ref-type="bibr">van der Hoek et al., 2004</xref>, <xref rid="b0665" ref-type="bibr">Woo et al., 2005</xref>). In 2012, a highly pathogenic sixth HCoV, termed <italic>Middle East respiratory syndrome</italic> (MERS)-CoV emerged in the Arabian peninsula (<xref rid="b0120" ref-type="bibr">de Groot et al., 2013</xref>, <xref rid="b0720" ref-type="bibr">Zaki et al., 2012</xref>, <xref rid="b0280" ref-type="bibr">Hilgenfeld and Peiris, 2013</xref>).</p><p id="p0015">During the SARS epidemic, first hints pointed to a zoonotic origin of the SARS-CoV, with civets as the suspected source of human infection (<xref rid="b0250" ref-type="bibr">Guan et al., 2003</xref>, <xref rid="b0580" ref-type="bibr">Song et al., 2005</xref>, <xref rid="b0700" ref-type="bibr">Xu et al., 2004</xref>). Genetically diversified CoVs related to SARS-CoV were then found in Chinese rhinolophid bats, indicating these animals may constitute the animal reservoir of this novel HCoV (<xref rid="b0345" ref-type="bibr">Lau et al., 2005</xref>, <xref rid="b0380" ref-type="bibr">Li et al., 2005</xref>). These findings and the concomitant description of Ebola viruses in African flying foxes (<xref rid="b0365" ref-type="bibr">Leroy et al., 2005</xref>) triggered research into bats as hosts of emerging pathogens. Among the factors promoting bats as animal reservoirs for mammalian viruses are their longevity, densely packed colonies, close social interaction and their ability to fly (<xref rid="b0070" ref-type="bibr">Calisher et al., 2006</xref>, <xref rid="b0400" ref-type="bibr">Luis et al., 2013</xref>). The numerous descriptions of novel viruses in bats and other animals have drastically changed our perception of the relevance of animal reservoirs for the understanding of emerging zoonoses (<xref rid="b0175" ref-type="bibr">Drosten, 2013</xref>, <xref rid="b0315" ref-type="bibr">Karesh et al., 2012</xref>, <xref rid="b0450" ref-type="bibr">Morse et al., 2012</xref>). In analogy to SARS-CoV, the novel MERS-CoV may share a putative origin in bats (<xref rid="b0020" ref-type="bibr">Annan et al., 2013</xref>). This review focuses on bats and the CoVs they host.</p><sec id="s0010"><label>1.1</label><title>Coronavirus genomic organization</title><p id="p0020">CoVs belong to the order <italic>Nidovirales</italic>, family <italic>Coronaviridae</italic> and subfamily <italic>Coronavirinae</italic>, comprising four genera termed <italic>Alpha</italic>-, <italic>Beta</italic>-, <italic>Gamma</italic>- and <italic>Deltacoronavirus</italic> (<xref rid="b0005" ref-type="bibr">Adams and Carstens, 2012</xref>, <xref rid="b0500" ref-type="bibr">Perlman and Netland, 2009</xref>). Betacoronaviruses are further separated into clades a–d, while the separation between alphacoronavirus clades a and b has been discontinued (<xref rid="b0125" ref-type="bibr">de Groot et al., 2012</xref>).</p><p id="p0025">CoV genomes are composed of one continuous RNA strand of positive polarity, ranging between approximately 27 and 32,000 nucleotides, constituting the largest continuous RNA genomes among mammalian viruses (<xref rid="b0670" ref-type="bibr">Woo et al., 2009</xref>). Starting from the 5′-end of these genomes, approximate two-thirds encodes a large open reading frame (ORF) 1, producing up to 16 nonstructural proteins (nsp). A conserved sequence UUUAAAC, located around genome positions 12–14,000 in alpha- and betacoronaviruses, provides the characteristic ribosomal slippage leading to transcription of ORF1ab (<xref rid="b0065" ref-type="bibr">Brian and Baric, 2005</xref>, <xref rid="b0415" ref-type="bibr">Masters, 2006</xref>). The functions of individual nsp are only partially understood.</p><p id="p0030">Known ORF1ab gene products include, among others, a <italic>papain-like protease</italic> (<italic>Plpro</italic>) and <italic>main protease</italic> (<italic>Mpro</italic>), a <italic>helicase</italic>, two <italic>methyltransferases</italic>, a <italic>RNA-dependent RNA polymerase</italic> (<italic>RdRp</italic>) and several innate immunity antagonists (<xref rid="b0500" ref-type="bibr">Perlman and Netland, 2009</xref>). Downstream of the ORF1ab, all CoVs contain genes coding for the structural proteins spike, envelope, membrane and nucleocapsid and several accessory genes in variable number and genomic location (<xref rid="b0670" ref-type="bibr">Woo et al., 2009</xref>). A unique CoV feature is the discontinuous transcription of genes downstream of the ORF1ab from subgenomic mRNAs, involving interaction between characteristic transcription-regulatory sequences (TRS) found in the most 5′-genomic region (leader TRS) and upstream of individual genes (body TRS) (<xref rid="b0065" ref-type="bibr">Brian and Baric, 2005</xref>, <xref rid="b0485" ref-type="bibr">Pasternak et al., 2006</xref>, <xref rid="b0500" ref-type="bibr">Perlman and Netland, 2009</xref>, <xref rid="b0670" ref-type="bibr">Woo et al., 2009</xref>).</p></sec><sec id="s0015"><label>1.2</label><title>Bat coronavirus detection and challenges for their taxonomic classification</title><p id="p0035">Almost all CoV field studies investigating bats or other animals are based on PCR assays targeting parts of the ORF1ab, typically the <italic>RdRp</italic>. In these studies, PCR amplicon sizes range from as little as 121 to around 404 base-pairs (<xref rid="b0025" ref-type="bibr">Anthony et al., 2013a</xref>, <xref rid="b0115" ref-type="bibr">da Silva Filho et al., 2012</xref>, <xref rid="b0135" ref-type="bibr">de Souza Luna et al., 2007</xref>, <xref rid="b0445" ref-type="bibr">Moes et al., 2005</xref>, <xref rid="b0600" ref-type="bibr">Tong et al., 2009</xref>). It should be noted that these small amplicon sizes drastically hinder CoV phylogenetic reconstructions. Therefore, caution should be taken when drawing conclusions on the relationships within the subfamily <italic>Coronavirinae,</italic> based on such small sequence fragments.</p><p id="p0040">There are only few characterizations of complete CoV genomes from bat feces, as summarized in <xref rid="t0005" ref-type="table">Table 1</xref>. The lack of virus isolates obtained directly from bats challenges the complete genomic characterization of these large and highly variable RNA viruses. The information originating from the four available metagenomic studies reporting CoV sequences offers even less phylogenetic power, because the resulting genomic fragments are very variable in genomic location and length (<xref rid="b0155" ref-type="bibr">Donaldson et al., 2010</xref>, <xref rid="b0215" ref-type="bibr">Ge et al., 2012</xref>, <xref rid="b0375" ref-type="bibr">Li et al., 2010</xref>, <xref rid="b0695" ref-type="bibr">Wu et al., 2012b</xref>).<table-wrap position="float" id="t0005"><label>Table 1</label><caption><p>Studies yielding bat coronavirus sequences.</p></caption><table frame="hsides" rules="groups"><thead><tr><th>Continent</th><th>Bat family yielding CoV sequences</th><th>Country</th><th>Reference</th><th>Comments</th></tr></thead><tbody><tr><td rowspan="15">America</td><td><italic>Phyllostomidae</italic></td><td>Brazil</td><td><xref rid="b0060" ref-type="bibr">Brandao et al. (2008)</xref></td><td rowspan="15">No full genome information available</td></tr><tr><td><italic>Molossidae</italic></td><td>Brazil</td><td><xref rid="b0390" ref-type="bibr">Lima et al. (2013)</xref></td></tr><tr><td><italic>Phyllostomidae</italic>, <italic>Molossidae</italic></td><td>Brazil</td><td><xref rid="b0105" ref-type="bibr">Corman et al. (2013b)</xref></td></tr><tr><td><italic>Phyllostomidae</italic>, <italic>Molossidae</italic>, <italic>Noctilionidae</italic>, <italic>Vespertilionidae</italic></td><td>Brazil</td><td><xref rid="b0235" ref-type="bibr">Góes et al. (2013)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Canada</td><td><xref rid="b0440" ref-type="bibr">Misra et al. (2009)</xref></td></tr><tr><td><italic>Phyllostomidae</italic>, <italic>Mormoopidae</italic></td><td>Costa Rica</td><td><xref rid="b0105" ref-type="bibr">Corman et al. (2013b)</xref></td></tr><tr><td><italic>Phyllostomidae</italic>, <italic>Emballonuridae</italic>, <italic>Mormoopidae</italic>, <italic>Vespertilionidae</italic></td><td>Mexico</td><td><xref rid="b0235" ref-type="bibr">Góes et al. (2013)</xref></td></tr><tr><td><italic>Phyllostomidae</italic>, <italic>Mormoopidae</italic>, <italic>Molossidae, Vespertilionidae</italic></td><td>Mexico</td><td><xref rid="b0025" ref-type="bibr">Anthony et al. (2013a)</xref></td></tr><tr><td><italic>Phyllostomidae</italic></td><td>Panama</td><td><xref rid="b0105" ref-type="bibr">Corman et al. (2013b)</xref></td></tr><tr><td><italic>Phyllostomidae</italic></td><td>Trinidad</td><td><xref rid="b0075" ref-type="bibr">Carrington et al. (2008)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>USA</td><td><xref rid="b0150" ref-type="bibr">Dominguez et al. (2007)</xref></td></tr><tr><td><italic>Vespertilionidae</italic>, <italic>Molossidae</italic></td><td>USA</td><td><xref rid="b0375" ref-type="bibr">Li et al. (2010)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>USA</td><td><xref rid="b0155" ref-type="bibr">Donaldson et al. (2010)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>USA</td><td><xref rid="b0475" ref-type="bibr">Osborne et al. (2011)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>USA</td><td><xref rid="b0290" ref-type="bibr">Huynh et al. (2012)</xref></td></tr><tr><td rowspan="13">Europe</td><td><italic>Rhinolophidae</italic>, <italic>Vespertilionidae</italic></td><td>Bulgaria</td><td><xref rid="b0170" ref-type="bibr">Drexler et al. (2010)</xref></td><td>SARS-related CoV; Full genome</td></tr><tr><td><italic>Vespertilionidae</italic></td><td>UK</td><td><xref rid="b0035" ref-type="bibr">August et al. (2012)</xref></td><td rowspan="12">No full genome information available</td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Germany</td><td><xref rid="b0230" ref-type="bibr">Gloza-Rausch et al. (2008)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Germany</td><td><xref rid="b0170" ref-type="bibr">Drexler et al. (2010)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Germany</td><td><xref rid="b0165" ref-type="bibr">Drexler et al. (2011)</xref></td></tr><tr><td><italic>Rhinolophidae</italic></td><td>Italy</td><td><xref rid="b0045" ref-type="bibr">Balboni et al. (2011)</xref></td></tr><tr><td><italic>Rhinolophidae</italic></td><td>Italy</td><td><xref rid="b0040" ref-type="bibr">Balboni et al. (2012)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Netherlands</td><td><xref rid="b0540" ref-type="bibr">Reusken et al. (2010)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Netherlands</td><td><xref rid="b0020" ref-type="bibr">Annan et al. (2013)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Roumania</td><td><xref rid="b0020" ref-type="bibr">Annan et al. (2013)</xref></td></tr><tr><td><italic>Rhinolophidae</italic></td><td>Slovakia</td><td><xref rid="b0545" ref-type="bibr">Rihtaric et al. (2010)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Spain</td><td><xref rid="b0210" ref-type="bibr">Falcon et al. (2011)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Ukraine</td><td><xref rid="b0020" ref-type="bibr">Annan et al. (2013)</xref></td></tr><tr><td rowspan="7">Africa</td><td><italic>Hipposideridae</italic></td><td>Ghana</td><td><xref rid="b0505" ref-type="bibr">Pfefferle et al. (2009)</xref></td><td rowspan="7">No full genome information available</td></tr><tr><td><italic>Nycteridae</italic></td><td>Ghana</td><td><xref rid="b0020" ref-type="bibr">Annan et al. (2013)</xref></td></tr><tr><td><italic>Pteropodidae</italic>, <italic>Hipposideridae</italic>, <italic>Vespertilionidae</italic>, <italic>Molossidae</italic></td><td>Kenya</td><td><xref rid="b0600" ref-type="bibr">Tong et al. (2009)</xref></td></tr><tr><td><italic>Pteropodidae</italic>, <italic>Megadermatidae</italic>, <italic>Vespertilionidae</italic>, <italic>Molossidae</italic></td><td>Kenya</td><td><xref rid="b0590" ref-type="bibr">Tao et al. (2012)</xref></td></tr><tr><td><italic>Hipposideridae</italic></td><td>Nigeria</td><td><xref rid="b0515" ref-type="bibr">Quan et al. (2010)</xref></td></tr><tr><td><italic>Vespertilionidae</italic>, <italic>Molossidae</italic></td><td>South Africa</td><td><xref rid="b0220" ref-type="bibr">Geldenhuys et al. (2013)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>South Africa</td><td><xref rid="b0740" ref-type="bibr">Ithete et al. (2013)</xref></td></tr><tr><td rowspan="25">Asia</td><td><italic>Pteropodidae</italic></td><td>Bangladesh</td><td><xref rid="b0030" ref-type="bibr">Anthony et al. (2013b)</xref></td><td rowspan="14">No full genome information available</td></tr><tr><td><italic>Vespertilionidae</italic></td><td>China</td><td><xref rid="b0510" ref-type="bibr">Poon et al. (2005)</xref></td></tr><tr><td><italic>Rhinolophidae</italic>, <italic>Vespertilionidae</italic></td><td>China</td><td><xref rid="b0680" ref-type="bibr">Woo et al. (2006)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>China</td><td><xref rid="b0095" ref-type="bibr">Chu et al. (2006)</xref></td></tr><tr><td><italic>Pteropodidae</italic></td><td>China</td><td><xref rid="b0340" ref-type="bibr">Lau et al. (2010b)</xref></td></tr><tr><td><italic>Rhinolophidae</italic></td><td>China</td><td><xref rid="b0715" ref-type="bibr">Yuen et al. (2012)</xref></td></tr><tr><td><italic>Hipposideridae</italic></td><td>China</td><td><xref rid="b0215" ref-type="bibr">Ge et al. (2012)</xref></td></tr><tr><td><italic>Rhinolophidae</italic>, <italic>Vespertilionidae</italic></td><td>China</td><td><xref rid="b0695" ref-type="bibr">Wu et al. (2012b)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>Japan</td><td><xref rid="b0565" ref-type="bibr">Shirato et al. (2012)</xref></td></tr><tr><td><italic>Emballonuridae, Pteropodidae</italic>, <italic>Rhinopomatidae</italic>, <italic>Vespertilionidae</italic></td><td>Saudi Arabia</td><td><xref rid="b0430" ref-type="bibr">Memish et al. (2013)</xref></td></tr><tr><td><italic>Pteropodidae</italic>, <italic>Vespertilionidae</italic></td><td>Philippines</td><td><xref rid="b0655" ref-type="bibr">Watanabe et al. (2010)</xref></td></tr><tr><td><italic>Pteropodidae</italic>, <italic>Hipposideridae</italic></td><td>Philippines</td><td><xref rid="b0605" ref-type="bibr">Tsuda et al. (2012)</xref></td></tr><tr><td><italic>Hipposideridae</italic></td><td>Thailand</td><td><xref rid="b0240" ref-type="bibr">Gouilh et al. (2011)</xref></td></tr><tr><td><italic>Molossidae</italic></td><td>Thailand</td><td><xref rid="b0650" ref-type="bibr">Wacharapluesadee et al. (2013)</xref></td></tr><tr><td><italic>Vespertilionidae</italic></td><td>China</td><td><xref rid="b0090" ref-type="bibr">Chu et al. (2008)</xref></td><td>1A/1B, HKU8; full genome</td></tr><tr><td><italic>Pteropodidae, Hipposideridae</italic></td><td>China</td><td><xref rid="b0335" ref-type="bibr">Lau et al. (2012)</xref></td><td>HKU10; full genomes</td></tr><tr><td><italic>Rhinolophidae</italic></td><td>China</td><td><xref rid="b0350" ref-type="bibr">Lau et al. (2007)</xref></td><td>HKU2; full genome</td></tr><tr><td><italic>Pteropodidae</italic>, <italic>Rhinolophidae</italic><underline>,</underline><italic>Vespertilionidae</italic></td><td>China</td><td><xref rid="b0685" ref-type="bibr">Woo et al. (2007)</xref></td><td>HKU4, HKU5, HKU9; full genome</td></tr><tr><td><italic>Rhinolophidae</italic>, <italic>Vespertilionidae</italic></td><td>China</td><td><xref rid="b0585" ref-type="bibr">Tang et al. (2006)</xref></td><td>SARS-related CoV, 512, HKU4; full genome</td></tr><tr><td><italic>Rhinolophidae</italic></td><td>China</td><td><xref rid="b0345" ref-type="bibr">Lau et al. (2005)</xref></td><td>SARS-related CoV; full genome</td></tr><tr><td><italic>Rhinolophidae</italic></td><td>China</td><td><xref rid="b0380" ref-type="bibr">Li et al. (2005)</xref></td><td>SARS-related CoV; full genome</td></tr><tr><td><italic>Rhinolophidae</italic></td><td>China</td><td><xref rid="b0525" ref-type="bibr">Ren et al. (2006)</xref></td><td>SARS-related CoV; full genome</td></tr><tr><td><italic>Rhinolophidae</italic></td><td>China</td><td><xref rid="b0710" ref-type="bibr">Yuan et al. (2010)</xref></td><td>SARS-related CoV; full genome</td></tr><tr><td><italic>Rhinolophidae</italic></td><td>China</td><td><xref rid="b0325" ref-type="bibr">Lau et al., 2010a</xref></td><td>SARS-related CoV; full genome</td></tr><tr><td><italic>Rhinolophidae</italic>, <italic>Molossidae</italic></td><td>China</td><td><xref rid="b0705" ref-type="bibr">Yang et al. (2013)</xref></td><td>SARS-related CoV; full genomes</td></tr></tbody></table></table-wrap></p><p id="p0045">To provide order in CoV taxonomy, the current proposal of the International Committee for the Taxonomy of Viruses (ICTV) is based on pairwise amino acid distances in seven concatenated partial or complete nsp domains, encompassing about 50% of the CoV genome. In technical analogy to an approach that has been validated for the RNA virus family <italic>Picornaviridae</italic> (<xref rid="b0360" ref-type="bibr">Lauber and Gorbalenya, 2012b</xref>), amino acid identity below 90% was found to be discriminatory for the designation of novel CoV species (<xref rid="b0125" ref-type="bibr">de Groot et al., 2012</xref>). A different criterion, relying on <italic>RdRp</italic>-grouping units (RGU), also used pairwise amino acid distances, but was restricted to a translated 816 nucleotide <italic>RdRp</italic> (nsp12) fragment. This was chosen as an amenable approach to account for the partial genomic sequences generated by most PCR-based field studies. It was found that defined alphacoronavirus RGU differed by at least 4.8% and betacoronavirus RGU by at least 6.3% in this <italic>RdRp</italic> fragment. This allowed a surrogate criterion for species definition in the absence of complete genomic sequences (<xref rid="b0170" ref-type="bibr">Drexler et al., 2010</xref>, <xref rid="b0590" ref-type="bibr">Tao et al., 2012</xref>). However, the increase in partial CoV sequences has caused a loss of discriminatory power of these RGU thresholds.</p><p id="p0050">For example, the novel HCoV species MERS-CoV (<xref rid="b0120" ref-type="bibr">de Groot et al., 2013</xref>, <xref rid="b0610" ref-type="bibr">van Boheemen et al., 2012</xref>) and the genetically closely related <italic>Pipistrellus</italic> bat CoVs clearly belong to one RGU (<xref rid="b0020" ref-type="bibr">Annan et al., 2013</xref>, <xref rid="b0540" ref-type="bibr">Reusken et al., 2010</xref>). However, these novel bat viruses also differ by only 5.1% from the established CoV species HKU5, implying that they share sufficient <italic>RdRp</italic> sequence identity to be classifiable within both an RGU defined either by MERS-CoV or by HKU5. Re-analysis of all available <italic>RdRp</italic> sequence data for the present paper indicated that the 4.8% threshold previously determined for alphacoronaviruses could be maintained. In contrast, a revised lower threshold of at least 5.1% amino acid sequence distance in this <italic>RdRp</italic> fragment was necessary to accommodate all betacoronavirus species included in the current ICTV proposal (<xref rid="b0125" ref-type="bibr">de Groot et al., 2012</xref>) and the novel partial CoV sequences.</p></sec><sec id="s0020"><label>1.3</label><title>Increase in coronavirus genomic sequences</title><p id="p0055"><xref rid="f0005" ref-type="fig">Fig. 1</xref>A shows the increase in bat CoV sequence deposition into GenBank that closely followed the 2002–3 SARS pandemic. An even bigger increase of overall CoV sequence entries can be observed after 2009. This is likely due to both the advent of next-generation sequencing techniques and changed GenBank policies requiring host information from submitters. <xref rid="f0005" ref-type="fig">Fig. 1</xref>B shows that the proportion of bat CoV sequences among the 5489 overall CoV entries containing host information is small, compared to those from hosts such as ungulates, birds and carnivores. Possible explanations for this difference are likely the veterinary relevance of livestock and pet CoVs and the usage of prototype viruses as laboratory models leading to sequence entries, e.g., for BCoV, TGEV, FIPV and IBV. Still, the number of bat CoV entries (<italic>n</italic> = 390) almost equalled that of HCoVs (<italic>n</italic> = 460). However, the lack of host information for HCoVs probably introduces a bias in this comparison.<fig id="f0005"><label>Fig. 1</label><caption><p>Coronavirus data in public databases. Panels A and B. Data was based on a GenBank search using the terms “Coronaviridae” [ORGANISM] AND Host [All Fields]” in the “Nucleotide” database, on June 16th, 2013. Panel C, PubMed data was retrieved from a search using the terms “coronaviruses, coronavirus, coronaviridae, coronavirinae, bat, chiroptera, bats”, on June 16th, 2013.</p></caption><graphic xlink:href="gr1"></graphic></fig></p><p id="p0060">An analysis of published CoV research reports is shown in <xref rid="f0005" ref-type="fig">Fig. 1</xref>c. The impact of the SARS-epidemic in 2002–3 on the number of CoV publications was tremendous, leading to a near four-fold increase to around 700 published studies per year after 2002. Similarly, the identification of SARS-related CoVs in bats led to around 15 studies on bat CoVs per year after 2005. Of note, this figure also shows that scientific publications began to decrease a few years after SARS-CoV disappeared. The emergence of the MERS-CoV is likely to counteract this phenomenon in the years to come.</p></sec><sec id="s0025"><label>1.4</label><title>Coronavirus phylogeny</title><p id="p0065">The rapid increase in bat CoV studies enabled hypotheses of bats as reservoir hosts for alpha and betacoronaviruses only a few years after the SARS epidemic (<xref rid="b0630" ref-type="bibr">Vijaykrishna et al., 2007</xref>, <xref rid="b0670" ref-type="bibr">Woo et al., 2009</xref>). <xref rid="f0010" ref-type="fig">Fig. 2</xref>shows the clear separation between the mammalian genera <italic>Alpha</italic>- and <italic>Betacoronavirus</italic> and the bird-associated genera <italic>Gamma</italic>- and <italic>Deltacoronavirus</italic> (<xref rid="b0660" ref-type="bibr">Weiss and Navas-Martin, 2005</xref>, <xref rid="b0675" ref-type="bibr">Woo et al., 2012</xref>) in a Bayesian phylogeny based on an 816 <italic>RdRp</italic> sequence fragment of the complete subfamily <italic>Coronavirinae</italic>. <xref rid="f0015" ref-type="fig">Fig. 3</xref>provides details of this phylogenetic analysis for the genera <italic>Alpha</italic>- and <italic>Betacoronavirus</italic>. The large number of deep branches leading to bat viruses (shown in red) emphasizes the association of these two CoV genera with bat hosts. This is particularly true for the <italic>Alphacoronavirus</italic> clade formerly designated 1b, which includes HCoV-229E, -NL63 and the <italic>Betacoronavirus</italic> clades b–d.<fig id="f0010"><label>Fig. 2</label><caption><p>Phylogenetic relationships in the subfamily <italic>Coronavirinae</italic>. Bayesian phylogeny of an 816-nucleotide <italic>RNA-dependent RNA polymerase</italic> fragment, as described previously (<xref rid="b0170" ref-type="bibr">Drexler et al., 2010</xref>) of the subfamily <italic>Coronavirinae</italic> using MrBayes V3.1 (<xref rid="b0550" ref-type="bibr">Ronquist and Huelsenbeck, 2003</xref>) under assumption of a GTR + G + I substitution model, using 2,000,000 trees sampled every 100 steps, annotated with a burn-in of 25% using TreeAnnotator V1.7.4 and visualized using FigTree V1.4 from the BEAST package (<xref rid="b0185" ref-type="bibr">Drummond et al., 2012</xref>). Cavally virus (<xref rid="b0735" ref-type="bibr">Zirkel et al., 2011</xref>) was used as an outgroup. Values at deep nodes indicate statistical support from Bayesian posterior probabilities, scale bar genetic distance.</p></caption><graphic xlink:href="gr2"></graphic></fig><fig id="f0015"><label>Fig. 3</label><caption><p>Phylogenetic relationships between coronaviruses and bat hosts. Details of the phylogeny shown in <xref rid="f0010" ref-type="fig">Fig. 2</xref> for the genera <italic>Alpha</italic>- and <italic>Betacoronavirus</italic>. ICTV species are given to the right of clade designations and bat symbols, when applicable. Virus designations include strain names, GenBank accession numbers and host information as the first three letters of the latin genus and species names. Bat viruses are shown in red. Boxes indicate <italic>Alpha</italic>- and <italic>Betacoronavirus</italic> genera, according to the coloring in <xref rid="f0010" ref-type="fig">Fig. 2</xref>.</p></caption><graphic xlink:href="gr3"></graphic></fig></p><p id="p0070">The relevance of bat CoVs for these genera is also reflected in the current taxonomic proposal of the ICTV (<xref rid="b0125" ref-type="bibr">de Groot et al., 2012</xref>). Of the 15 recognized species in these two genera, six were only found in bats. These viruses are shown with bat pictograms in <xref rid="f0015" ref-type="fig">Fig. 3</xref> and include <italic>Miniopterus bat coronavirus 1</italic>, <italic>Miniopterus bat coronavirus HKU8</italic>, <italic>Rhinolophus bat coronavirus HKU2</italic>, <italic>Scotophilus bat coronavirus 512</italic>, <italic>Pipistrellus bat coronavirus HKU5</italic>, <italic>Rousettus bat coronavirus HKU9</italic>, and <italic>Tylonycteris bat coronavirus HKU4</italic>. Many partial bat CoV <italic>RdRp</italic> sequences were not included in <xref rid="f0015" ref-type="fig">Fig. 3</xref>, because only small sequence fragments reducing the phylogenetic resolution were available (<xref rid="b0105" ref-type="bibr">Corman et al., 2013b</xref>, <xref rid="b0170" ref-type="bibr">Drexler et al., 2010</xref>). Still, the sequences from these studies (detailed in <xref rid="t0005" ref-type="table">Table 1</xref>) do not alter the overall picture of bat CoV-associated clades within the genera <italic>Alpha</italic>- and <italic>Betacoronavirus</italic>.</p><p id="p0075">For most of these bat CoVs, lack of complete genomic sequences prevents their taxonomic designation as species. Still, many of the partial sequences included in <xref rid="f0015" ref-type="fig">Fig. 3</xref> branch deeply in the phylogenetic tree and likely represent not only new species, but even new genetic clades. This is exemplified by the unclassified African <italic>Hipposideros</italic> betacoronaviruses (<xref rid="b0505" ref-type="bibr">Pfefferle et al., 2009</xref>, <xref rid="b0515" ref-type="bibr">Quan et al., 2010</xref>, <xref rid="b0600" ref-type="bibr">Tong et al., 2009</xref>), which putatively represent a yet to be defined <italic>Betacoronavirus</italic> clade e and unclassified neotropical <italic>Carollia</italic> and <italic>Pteronotus</italic> viruses (<xref rid="b0105" ref-type="bibr">Corman et al., 2013b</xref>) putatively corresponding to additional <italic>Betacoronavirus</italic> clades.</p><p id="p0080"><xref rid="f0020" ref-type="fig">Fig. 4</xref>shows that 11 of the 18 extant bat families already contain CoV descriptions, including the two major bat lineages <italic>Yinpterochiroptera</italic> and <italic>Yangochiroptera</italic> (<xref rid="b0595" ref-type="bibr">Teeling et al., 2005</xref>). In most bat families, both alpha- and betacoronaviruses are known, and these detections have originated from both frugivorous and insectivorous bat hosts. Lack of detection in the remaining bat families is likely due to non-exhaustive sampling of the almost 1200 extant bat species (<xref rid="b0560" ref-type="bibr">Schipper et al., 2008</xref>, <xref rid="b0570" ref-type="bibr">Simmons, 2005</xref>, <xref rid="b0595" ref-type="bibr">Teeling et al., 2005</xref>). This void may be filled in future studies.<fig id="f0020"><label>Fig. 4</label><caption><p>Bat families in which coronaviruses have been detected. Phylogeny of extant bat families is shown according to (<xref rid="b0570" ref-type="bibr">Simmons, 2005</xref>). Boxes indicate descriptions of alpha- and betacoronaviruses according to the coloring in <xref rid="f0010" ref-type="fig">Fig. 2</xref>.</p></caption><graphic xlink:href="gr4"></graphic></fig></p></sec><sec id="s0030"><label>1.5</label><title>Bats as coronavirus hosts worldwide</title><p id="p0085"><xref rid="f0025" ref-type="fig">Fig. 5</xref>shows the geographic origin of all 53 studies characterizing novel bat CoVs and <xref rid="t0005" ref-type="table">Table 1</xref> provides details for these studies. The figure highlights that studies from all continents are now available, but there is a drastic lack of studies from resource-limited or politically unstable settings. Specifically, several biodiversity hotspots linked to the emergence of zoonotic viruses (<xref rid="b0305" ref-type="bibr">Jones et al., 2008</xref>) are not covered at all, including the Congo basin, large parts of South-East Asia and the Neotropical ecozone. Future sampling of bats from these and other poorly studied areas will likely complete bat species coverage and further increase the known CoV genomic diversity.<fig id="f0025"><label>Fig. 5</label><caption><p>Distribution of bat coronavirus studies. Studies reporting bat CoV sequences by country are indicated, with the number of studies given in blue circles and adjusted in size accordingly. Country codes: BRA = Brazil, CAN = Canada, CRC = Costa Rica, MEX = Mexico, PAN = Panama, TRI = Trinidad and Tobago, USA = United States of America, BGR = Bulgaria, GBR = Great Britain, GER = Germany, ITA = Italy, NED = Netherlands, ROU = Romania, SLO = Slovenia, SPA = Spain, UKR = Ukraine, GHA = Ghana, KEN = Kenia, NGR = Nigeria, RCA = South African Republic, CHN = China, JPN = Japan, PHI = Philippines, THA = Thailand. The black circles for the Central African Republic (CAF), Gabon (GAB) and Australia (AUS) indicate published sequences in GenBank, but lack of publication of the corresponding studies. Countries where CoV studies have been performed are in black, others in grey.</p></caption><graphic xlink:href="gr5"></graphic></fig></p></sec><sec id="s0035"><label>1.6</label><title>Association of coronavirus clades with mammalian hosts</title><sec id="s0040"><label>1.6.1</label><title>Promiscuous versus host-specific coronaviruses</title><p id="p0090">Only a small fraction of the currently known mammalian CoVs originates from primate, ungulate, lagomorph, carnivore and rodent hosts. As shown in <xref rid="f0015" ref-type="fig">Fig. 3</xref>, bats outnumber any other mammalian host in terms of virus diversity. Throughout the CoV phylogeny, examples can be found of both “promiscuous” and very host-restricted viruses. The paramount example of a promiscuous CoV is probably <italic>Betacoronavirus 1</italic> (the species including BCoV, HCoV-OC43 and related viruses), which has been detected in cows, horses, dogs, humans, waterbucks, deer, antelopes, camels and giraffes worldwide (<xref rid="b0010" ref-type="bibr">Alekseev et al., 2008</xref>, <xref rid="b0255" ref-type="bibr">Guy et al., 2000</xref>, <xref rid="b0270" ref-type="bibr">Hasoksuz et al., 2007</xref>, <xref rid="b0300" ref-type="bibr">Jin et al., 2007</xref>, <xref rid="b0385" ref-type="bibr">Lim et al., 2013</xref>, <xref rid="b0405" ref-type="bibr">Majhdi et al., 1997</xref>, <xref rid="b0730" ref-type="bibr">Zhang et al., 1994</xref>). Similarly, FIPV, <italic>Canine coronavirus</italic> (CCoV) and TGEV are now included in a single species termed <italic>Alphacoronavirus 1</italic>, and MHV and <italic>Rat coronavirus</italic> together are now termed <italic>Murine coronavirus</italic> (<xref rid="b0125" ref-type="bibr">de Groot et al., 2012</xref>). Another example of an apparently promiscuous CoV is the unclassified bat virus HKU10, which has been detected in the bat families <italic>Hipposideridae</italic> and <italic>Pteropodidae</italic> (<xref rid="b0335" ref-type="bibr">Lau et al., 2012</xref>).</p><p id="p0095">Most other CoVs have been confined to single host genera, exemplified by the detection of SARS-related CoVs and several alphacoronaviruses in <italic>Rhinolophus</italic>, <italic>Myotis</italic>, <italic>Miniopterus</italic>, <italic>Nyctalus</italic> and <italic>Carollia</italic> bat hosts, including detections of closely related viruses in individual bats separated by thousands of miles (<xref rid="b0105" ref-type="bibr">Corman et al., 2013b</xref>, <xref rid="b0170" ref-type="bibr">Drexler et al., 2010</xref>, <xref rid="b0585" ref-type="bibr">Tang et al., 2006</xref>). Similarly, <italic>Hipposideros</italic> betacoronaviruses from Thailand, Kenya, Nigeria and Ghana are closely related (<xref rid="b0240" ref-type="bibr">Gouilh et al., 2011</xref>, <xref rid="b0505" ref-type="bibr">Pfefferle et al., 2009</xref>, <xref rid="b0515" ref-type="bibr">Quan et al., 2010</xref>, <xref rid="b0600" ref-type="bibr">Tong et al., 2009</xref>) and the betacoronavirus HKU9 has been detected in different species of flying foxes in Africa and Asia (<xref rid="b0030" ref-type="bibr">Anthony et al., 2013b</xref>, <xref rid="b0340" ref-type="bibr">Lau et al., 2010b</xref>, <xref rid="b0590" ref-type="bibr">Tao et al., 2012</xref>, <xref rid="b0655" ref-type="bibr">Watanabe et al., 2010</xref>, <xref rid="b0685" ref-type="bibr">Woo et al., 2007</xref>). Of note, the detection of both host-specific and -nonspecific mammalian CoVs parallels what can be observed in the avian <italic>Coronavirinae</italic> genera. For example, infectious bronchitis virus (IBV, genus <italic>Gammacoronavirus</italic>) has been detected in a wide range of birds, while the recently described deltacoronaviruses appear to be more host-specific (<xref rid="b0085" ref-type="bibr">Chu et al., 2011</xref>).</p></sec><sec id="s0045"><label>1.6.2</label><title>Evidence for phylogenetic co-segregation of coronaviruses and bat hosts</title><p id="p0100">Co-segregation of CoVs and their bat hosts is most visible for HKU9, the <italic>Hipposideros</italic> betacoronaviruses and the SARS-related CoV, compared to <italic>Pteropodidae</italic>, <italic>Hipposideros</italic> and <italic>Rhinolophus</italic> hosts (<xref rid="f0015" ref-type="fig">Fig. 3</xref>, <xref rid="f0020" ref-type="fig">Fig. 4</xref>). A striking counter-example is the large number of bat alphacoronaviruses that cluster together with the prototype viruses HCoV-229E, -NL63 and PEDV (<xref rid="f0015" ref-type="fig">Fig. 3</xref>). Viruses from numerous bat hosts, together with ungulate and human viruses, are contained in this part of the <italic>Alphacoronavirus</italic> tree, and in contrast to the betacoronaviruses, the designation of clearly separated subclades is challenging. However, more work needs to be done to formally analyze the degree of phylogenetic co-segregation in the <italic>Coronavirinae</italic> subfamily.</p></sec></sec><sec id="s0050"><label>1.7</label><title>Coronavirus host switches from bats</title><sec id="s0055"><label>1.7.1</label><title>Host switches suggested by phylogenetically-related viruses in humans and bats</title><p id="p0105">The most well-studied CoV host switches have probably occurred from bats to humans. The foremost example is the paradigmatic host switch of SARS-CoV from rhinolophid bats into humans or potentially civets (<xref rid="b0045" ref-type="bibr">Balboni et al., 2011</xref>, <xref rid="b0170" ref-type="bibr">Drexler et al., 2010</xref>, <xref rid="b0325" ref-type="bibr">Lau et al., 2010a</xref>, <xref rid="b0345" ref-type="bibr">Lau et al., 2005</xref>, <xref rid="b0380" ref-type="bibr">Li et al., 2005</xref>, <xref rid="b0525" ref-type="bibr">Ren et al., 2006</xref>, <xref rid="b0545" ref-type="bibr">Rihtaric et al., 2010</xref>, <xref rid="b0705" ref-type="bibr">Yang et al., 2013</xref>). These human, civet and bat viruses are now officially summarized by the ICTV in one species, termed <italic>SARS-related coronavirus</italic> (<xref rid="b0125" ref-type="bibr">de Groot et al., 2012</xref>).</p><p id="p0110">The genomic relatedness of human and bat <italic>SARS-related coronaviruses</italic> is greatest in the ORF1ab, while a bat ancestor containing the structural proteins of human SARS-CoV has so far not been detected. Bat <italic>SARS-related coronaviruses</italic> fail to interact with the human SARS-CoV receptor molecule ACE2, possibly associated with small deletions in their receptor-binding domain (RBD), compared to human SARS-CoV (<xref rid="b0370" ref-type="bibr">Li, 2013</xref>, <xref rid="b0530" ref-type="bibr">Ren et al., 2008</xref>). In line with these differences, a bat <italic>SARS-related coronavirus</italic> synthesized by reverse genetics was only infectious in cell culture and mice when the <italic>spike</italic> gene was exchanged by the human SARS-CoV homologue (<xref rid="b0050" ref-type="bibr">Becker et al., 2008</xref>). Because the RBD of European rhinolophid bat <italic>SARS-related coronaviruses</italic> was more related to that of the human SARS-CoV than the RBD from Chinese bat viruses (<xref rid="b0170" ref-type="bibr">Drexler et al., 2010</xref>), recombination may have played a role in the emergence of the human pathogenic virus.</p><p id="p0115">However, not all rhinolophid bat species have been tested for <italic>SARS-related coronaviruses.</italic> For example, only 12 of the at least 19 rhinolophid bat species that occur in China have been tested and <italic>SARS-related coronavirus</italic> sequence information is only available from 5 of these species (<xref rid="b0345" ref-type="bibr">Lau et al., 2005</xref>, <xref rid="b0380" ref-type="bibr">Li et al., 2005</xref>, <xref rid="b0510" ref-type="bibr">Poon et al., 2005</xref>, <xref rid="b0585" ref-type="bibr">Tang et al., 2006</xref>, <xref rid="b0680" ref-type="bibr">Woo et al., 2006</xref>, <xref rid="b0685" ref-type="bibr">Woo et al., 2007</xref>, <xref rid="b0705" ref-type="bibr">Yang et al., 2013</xref>, <xref rid="b0710" ref-type="bibr">Yuan et al., 2010</xref>). Therefore, further studies of <italic>Rhinolophus</italic> species in Africa, Europe and Asia may provide more insight into the ancestral bat viruses that were the source of the emergence of human SARS-CoV.</p><p id="p0120">It should also be mentioned that the <italic>Hipposideros</italic> betacoronaviruses detected in Africa and Asia are clearly distinct from <italic>SARS-related coronaviruses</italic>. These viruses can be distinguished by both sequence distance-based taxonomic approaches described above. Additionally, the phylogenetic position and genomic properties of the unclassified <italic>Hipposideros</italic> betacoronaviruses differ from <italic>SARS-related coronaviruses</italic>. These genomic properties include chiefly their different viral 3’-genome ends and accessory ORFs downstream from the <italic>membrane</italic> gene in the <italic>Hipposideros</italic> CoVs (<xref rid="b0505" ref-type="bibr">Pfefferle et al., 2009</xref>, <xref rid="b0515" ref-type="bibr">Quan et al., 2010</xref>).</p><p id="p0125">Bat ancestors were also found for HCoV-229E in African <italic>Hipposideros</italic> bats (<xref rid="b0505" ref-type="bibr">Pfefferle et al., 2009</xref>), and a growing body of data indicates that bats worldwide harbour CoVs related to the MERS-CoV (<xref rid="b0020" ref-type="bibr">Annan et al., 2013</xref>, <xref rid="b0025" ref-type="bibr">Anthony et al., 2013a</xref>, <xref rid="b0740" ref-type="bibr">Ithete et al., 2013</xref>, <xref rid="b0540" ref-type="bibr">Reusken et al., 2010</xref>, <xref rid="b0650" ref-type="bibr">Wacharapluesadee et al., 2013</xref>, <xref rid="b0685" ref-type="bibr">Woo et al., 2007</xref>). Unfortunately, no complete genomes are available yet for the putative bat ancestors of HCoV-229E and MERS-CoV.</p><p id="p0130">Putative MERS-CoV bat ancestors have been most consistently found in the bat family <italic>Vespertilionidae</italic> and the related family <italic>Molossidae</italic>. These CoVs include European <italic>Pipistrellus</italic> bat viruses; a virus termed PML/2011 from a South-African <italic>Neoromicia</italic> bat (<xref rid="b0020" ref-type="bibr">Annan et al., 2013</xref>, <xref rid="b0740" ref-type="bibr">Ithete et al., 2013</xref>); CoVs from a Spanish <italic>Hypsugo savii</italic> and <italic>Eptesicus isabellinus</italic> (<xref rid="b0210" ref-type="bibr">Falcon et al., 2011</xref>); sequences from Thai bat guano (<xref rid="b0650" ref-type="bibr">Wacharapluesadee et al., 2013</xref>); a CoV from a Mexican <italic>Nyctinomops</italic> bat (<xref rid="b0025" ref-type="bibr">Anthony et al., 2013a</xref>); and the fully sequenced betacoronavirus clade c prototype bat CoVs HKU4 and HKU5 from China (<xref rid="b0685" ref-type="bibr">Woo et al., 2007</xref>). Clade c betacoronaviruses from Ghanaian <italic>Nycteris</italic> bats were more distantly related to the MERS-CoV (<xref rid="b0020" ref-type="bibr">Annan et al., 2013</xref>). A short 203-nt <italic>RdRp</italic> sequence fragment 100% identical to the MERS-CoV prototype strain EMC/2012 was described in a single Saudi-Arabian <italic>Taphozous perforatus</italic> bat, belonging to the family Emballonuridae (<xref rid="b0430" ref-type="bibr">Memish et al., 2013</xref>). Although the high sequence identity should have facilitated characterization of other CoV genomic regions, no further virus sequence could be obtained from this specimen.</p><p id="p0135">Detection of closely related CoVs in different bat families is rare, but may occur (<xref rid="b0335" ref-type="bibr">Lau et al., 2012</xref>, <xref rid="b0705" ref-type="bibr">Yang et al., 2013</xref>). However, even if closely related MERS-CoV bat ancestors existed in both the distantly related bat families Vespertilionidae and Emballonuridae (<xref rid="f0020" ref-type="fig">Fig. 4</xref>), the lack of further CoV sequence information and the single detection of a short genome fragment require further confirmation of this finding. Interestingly, in the same study, a 202-nt sequence from a <italic>Rhinopoma hardwickii</italic> bat was detected which was 100% identical to BCoV and other Betacoronavirus 1 reference strains (<xref rid="b0430" ref-type="bibr">Memish et al., 2013</xref>). Again, whether clade a betacoronaviruses also exist in bats requires confirmation by detection in more individual bats and more CoV sequence information.</p><p id="p0140">Regarding potential intermediate hosts of MERS-CoV, camels have been shown to have antibodies against this virus at high rates and titers (<xref rid="b0495" ref-type="bibr">Perera et al., 2013</xref>, <xref rid="b0535" ref-type="bibr">Reusken et al., 2013</xref>). Conclusions on the passage of putative bat ancestors of MERS-CoV to humans via camels will only be possible upon genomic characterization of the viruses eliciting this strong antibody response.</p><p id="p0145">Finally, no direct bat ancestor of HCoV-NL63 has ever been found, although the phylogenetic clade containing this HCoV is enclosed by bat CoVs. While the recent success in cultivating HCoV-NL63 on immortalized bat cells may hint at some link between bats and this virus (<xref rid="b0290" ref-type="bibr">Huynh et al., 2012</xref>), the bat viruses described in that and all previous studies are genetically rather distant from HCoV-NL63 (<xref rid="b0105" ref-type="bibr">Corman et al., 2013b</xref>).</p></sec><sec id="s0060"><label>1.7.2</label><title>Mechanisms of host switches</title><p id="p0150">The exact mechanisms by which CoVs adapt to new hosts are unclear. Clearly, virus entry and innate immune responses are among the paramount obstacles to be overcome during viral host switching. The high degree of conservation of the MERS-CoV receptor Dipeptidyl peptidase 4 in different hosts is thus a worrying scenario (<xref rid="b0460" ref-type="bibr">Muller et al., 2012</xref>, <xref rid="b0520" ref-type="bibr">Raj et al., 2013</xref>). Generally, it is unclear whether direct zoonotic transmission from bats to humans has occurred for any HCoV. Alternative scenarios involve intermediate hosts, such as carnivores or ungulates (<xref rid="b0020" ref-type="bibr">Annan et al., 2013</xref>, <xref rid="b0110" ref-type="bibr">Cotten et al., 2013</xref>, <xref rid="b0200" ref-type="bibr">Enserink, 2013</xref>, <xref rid="b0245" ref-type="bibr">Graham and Baric, 2010</xref>, <xref rid="b0330" ref-type="bibr">Lau et al., 2013</xref>, <xref rid="b0580" ref-type="bibr">Song et al., 2005</xref>, <xref rid="b0690" ref-type="bibr">Wu et al., 2012a</xref>).</p><p id="p0155">One way to rapidly acquire novel genes that potentially facilitate host switching is recombination between different viruses. A canonical example of recombination in CoVs is FIPV type 2. The prototype strains of this feline virus are recombinants between FIPV type 1 and CCoV in different parts of the ORF1b and <italic>Spike</italic> genes (<xref rid="b0275" ref-type="bibr">Herrewegh et al., 1998</xref>). Recombination has also been hypothesized to be involved in the emergence of the SARS-CoV (<xref rid="b0245" ref-type="bibr">Graham and Baric, 2010</xref>, <xref rid="b0285" ref-type="bibr">Hon et al., 2008</xref>, <xref rid="b0325" ref-type="bibr">Lau et al., 2010a</xref>, <xref rid="b0710" ref-type="bibr">Yuan et al., 2010</xref>) and HCoV-OC43 genotypes (<xref rid="b0320" ref-type="bibr">Lau et al., 2011</xref>). However, the observed recombination events in SARS-CoV and HCoV-OC43 are restricted to genetically closely related viruses. The exact recombination partners giving rise to SARS-CoV have never been detected.</p><p id="p0160">Another phenomenon putatively associated with CoV adaptation to distinct hosts and cells is exemplified by the variable deletions spanning over 600 nucleotides in the globular S1 domain of the <italic>Spike</italic> gene that is associated with a change from enteric (TGEV) to respiratory tract (<italic>Porcine respiratory coronavirus</italic>, PRCV) tropism. Whether the 290-nucleotide deletion downstream from the <italic>Spike</italic> gene in HCoV-OC43, in comparison to its likely ancestral virus BCoV (<xref rid="b0635" ref-type="bibr">Vijgen et al., 2006</xref>, <xref rid="b0640" ref-type="bibr">Vijgen et al., 2005</xref>), represents an adaptation to a human host remains unknown.</p></sec></sec><sec id="s0065"><label>1.8</label><title>Coronavirus pathology in bats compared to other mammalian hosts</title><p id="p0165">There is little information on the clinical consequences of CoV infections for bat hosts. In humans, HCoVs-NL63, -OC43, -HKU1 and -229E circulate constantly. SARS-CoV disappeared a few years after its epidemic transmission, while the novel MERS-CoV may only be starting to spread (<xref rid="b0200" ref-type="bibr">Enserink, 2013</xref>). All HCoV cause primarily respiratory symptoms in humans (<xref rid="b0260" ref-type="bibr">Hamre and Procknow, 1966</xref>, <xref rid="b0425" ref-type="bibr">McIntosh et al., 1967</xref>, <xref rid="b0490" ref-type="bibr">Peiris et al., 2003</xref>, <xref rid="b0615" ref-type="bibr">van der Hoek, 2007</xref>, <xref rid="b0620" ref-type="bibr">van der Hoek et al., 2006</xref>, <xref rid="b0665" ref-type="bibr">Woo et al., 2005</xref>), although the MERS-CoV has also been associated with severe renal complications (<xref rid="b0720" ref-type="bibr">Zaki et al., 2012</xref>). HCoV shedding in feces is not uncommon (<xref rid="b0395" ref-type="bibr">Liu et al., 2004</xref>), and there are sporadic reports on CoVs in humans with gastroenteritis, e.g., a case report on BCoV in a pediatric patient leading to the tentative designation <italic>Human enteric coronavirus</italic> (<xref rid="b0730" ref-type="bibr">Zhang et al., 1994</xref>). However, CoVs are apparently not generally related to gastroenteritis in humans (<xref rid="b0205" ref-type="bibr">Esper et al., 2010</xref>).</p><p id="p0170">In comparison, the clinical picture in other animals is considerably more variable, ranging from mild respiratory and gastroenteric symptoms to systemic disease with hepatitis, multi-organ failure and death (summarized in <xref rid="b0555" ref-type="bibr">Saif, 2004</xref>). The high CoV concentrations in bat feces (<xref rid="b0020" ref-type="bibr">Annan et al., 2013</xref>, <xref rid="b0165" ref-type="bibr">Drexler et al., 2011</xref>), together with the recovery of coronaviral RNA from the small and large intestine of frugivorous bats (<xref rid="b0655" ref-type="bibr">Watanabe et al., 2010</xref>) point to replication in the enteric tract. This is compatible both with the use of bat fecal material or intestinal specimens to detect bat CoVs in almost all published studies and with the high CoV RNA concentrations in the lower intestine of naturally infected hedgehogs (<xref rid="b0100" ref-type="bibr">Corman et al., 2013a</xref>). Although there are no apparent clinical signs of gastroenteritis (<xref rid="b0655" ref-type="bibr">Watanabe et al., 2010</xref>) or any other disease in bats, it should be noted that bats appear to raise antibodies against their coronaviruses at high rates (<xref rid="b0340" ref-type="bibr">Lau et al., 2010b</xref>, <xref rid="b0345" ref-type="bibr">Lau et al., 2005</xref>, <xref rid="b0455" ref-type="bibr">Muller et al., 2007</xref>, <xref rid="b0605" ref-type="bibr">Tsuda et al., 2012</xref>). Whether this correlates with the severity of infection remains unknown.</p><p id="p0175">From an ecologic point of view, CoVs seem to rely on massive amplification on a population level during bat reproductive seasonal cycles, potentially associated with fecal-oral transmission (<xref rid="b0165" ref-type="bibr">Drexler et al., 2011</xref>, <xref rid="b0230" ref-type="bibr">Gloza-Rausch et al., 2008</xref>, <xref rid="b0475" ref-type="bibr">Osborne et al., 2011</xref>). Similar phenomena have been observed for other bat-associated viruses, such as the filo-, henipa-, astro- and lyssaviruses (<xref rid="b0015" ref-type="bibr">Amman et al., 2012</xref>, <xref rid="b0165" ref-type="bibr">Drexler et al., 2011</xref>, <xref rid="b0225" ref-type="bibr">George et al., 2011</xref>, <xref rid="b0645" ref-type="bibr">Wacharapluesadee et al., 2010</xref>). Still, respiratory or vertical CoV transmission cannot be ruled out at this point, mostly due to the necessity of shielding these protected animals from human interference. Hypothetically, one could question whether insectivorous bats that rely on a functional larynx for echolocation of prey could even tolerate respiratory infection. This highly speculative scenario could point to an evolution of bat (corona-) viruses towards infection outside the respiratory tract. Alternatively, it could represent a sample bias due to the rapid death and decay of bats suffering from any respiratory disease that impairs predation, a likely scenario given the very active metabolism of bats, which for example requires insectivorous bats to consume several grams of insects per night (<xref rid="b0195" ref-type="bibr">Encarnação and Dietz, 2006</xref>).</p></sec></sec><sec id="s0070"><label>2</label><title>Discussion</title><p id="p0180">Ten years after the SARS epidemic, there is an overwhelming body of evidence highlighting the relevance of bats for the evolution of mammalian CoVs (<xref rid="b0630" ref-type="bibr">Vijaykrishna et al., 2007</xref>, <xref rid="b0670" ref-type="bibr">Woo et al., 2009</xref>). From a taxonomic perspective, there is a clear need for the establishment of reliable criteria for these viruses, such as those established for the family <italic>Picornaviridae</italic> (<xref rid="b0360" ref-type="bibr">Lauber and Gorbalenya, 2012b</xref>). The challenges observed in attempts to transfer these distance-based approaches to less well characterized virus families such as the <italic>Filoviridae</italic> (<xref rid="b0355" ref-type="bibr">Lauber and Gorbalenya, 2012a</xref>) highlight that the current set of CoV taxonomic criteria will likely have to be optimized and thoroughly validated.</p><p id="p0185">Both the existing ICTV and the RGU-based attempts use a similar methodological background and offer more reliable criteria than phylogeny alone. However, both suffer from several shortcomings. Loss of discriminatory sharpness upon the increment in known CoV genetic diversity will likely limit these approaches, although the ICTV criteria may prove more robust, due to the larger genomic fragments incorporated. From a technical point of view, it should be noted that the extension of the <italic>RdRp</italic> fragment size used for RGU definitions can be challenging when field specimens contain low RNA concentrations (<xref rid="b0105" ref-type="bibr">Corman et al., 2013b</xref>, <xref rid="b0170" ref-type="bibr">Drexler et al., 2010</xref>). A similar difficulty can be observed for the ICTV proposal, which requires the characterization of approximately 50% of a typical CoV genome. The more than 20 unclassified CoV species in the current ICTV proposal demonstrate that this task is not easily fulfilled for viruses which have not been grown in culture (<xref rid="b0125" ref-type="bibr">de Groot et al., 2012</xref>). Furthermore, both approaches do not incorporate any sequence distance-based data from genomic regions encoding the structural proteins. Besides the technical constraints on characterizing these genes that were stated above, this is likely also due to the poor sequence alignments some of these genes entail. The high variability, e.g., of the <italic>Spike</italic> gene, complicates the establishment of criteria applicable to the complete subfamily. Still, incorporation of some of the more conserved structural genes, such as the <italic>Envelope</italic>, <italic>Membrane</italic> or parts of the <italic>Spike</italic> and <italic>Nucleocapsid</italic> genes may prove helpful in carrying out this promising genome-based taxonomic approach.</p><p id="p0190">Regarding mammalian CoV hosts, several questions remain to be answered. First, the complete absence of host-specific CoVs in monkeys or apes impedes our understanding of any putative CoV evolution in other primates than humans. The apparently recent host switches responsible for the generation of HCoVs may indicate that even if CoVs exist in non-human primates (NHP), they may not be relevant for the evolution of their human counterparts. However, the current lack of CoV data from NHPs prevents more definite assertions on this topic.</p><p id="p0195">Second, intermediate hosts adapting bat viruses to humans or other mammals have neither been conclusively found for SARS-CoV, nor for any other HCoV. Despite the high seroprevalence of Chinese animal handlers against SARS-CoV, it is not entirely clear whether civets indeed adapted SARS-CoV for infection in humans (<xref rid="b0245" ref-type="bibr">Graham and Baric, 2010</xref>, <xref rid="b0250" ref-type="bibr">Guan et al., 2003</xref>). Similarly, the high seroprevalence of camels against MERS-CoV suggests that these animals are a potential source of the initial introduction of this virus into the human population (<xref rid="b0535" ref-type="bibr">Reusken et al., 2013</xref>). However, the current lack of MERS-CoV genomic sequences from camels prevents definite conclusions on this putative scenario.</p><p id="p0200">Third, many mammalian orders have not been or are only poorly studied. This is exemplified by the single CoV detected in lagomorphs (rabbit coronavirus HKU14), which likely belongs to the <italic>Betacoronavirus 1</italic> species, and by <italic>Murine Coronavirus</italic> (the former MHV), the only known rodent CoV species. Whether CoVs exist in other mammalian hosts, and to what extent these viruses contribute to our understanding of CoV evolution, for now remain obscure.</p><p id="p0205">Finally, the recent description of distantly related nidoviruses in insects has enabled hypotheses on a putative insect origin of <italic>Coronaviridae</italic> ancestors (<xref rid="b0470" ref-type="bibr">Nga et al., 2011</xref>, <xref rid="b0735" ref-type="bibr">Zirkel et al., 2011</xref>). Interestingly, the number of CoV descriptions from insectivorous bats is large, and a clade c betacoronavirus was recently described from insectivorous hedgehogs (<xref rid="b0100" ref-type="bibr">Corman et al., 2013a</xref>). Insectivorous mammals, such as shrews, moles and hedgehogs from the order <italic>Eulipotyphla</italic> could thus be specifically investigated to bolster hypotheses on the putative ancient insect origins of the CoVs harbored by insectivorous mammalian hosts.</p><p id="p0210">It has been hypothesized previously that large genome size, frequent recombination and high mutation rate make coronaviruses particularly prone to zoonotic host switching (<xref rid="b0670" ref-type="bibr">Woo et al., 2009</xref>). These hallmarks require further consideration. First, the large CoV genomes indeed allow for the accommodation of several genes, putatively enhancing virus pathogenicity. For example, the evolutionary origin of the highly variable SARS-CoV accessory proteins is largely unknown, and deletion of these genes strikingly decreases virulence (<xref rid="b0420" ref-type="bibr">McBride and Fielding, 2012</xref>, <xref rid="b0465" ref-type="bibr">Narayanan et al., 2008</xref>). Similarly, among CoV genomes, only members of the betacoronavirus clade contain a hemagglutinin-esterase related to that of influenza C viruses (<xref rid="b0725" ref-type="bibr">Zeng et al., 2008</xref>), compatible with putative inter-viral gene exchange. Still, little is known about how and when CoVs can incorporate novel genes into their genomes. The technical difficulties observed with the usage of CoV-based vectors for heterologous gene expression indicate that, at least <italic>in vitro</italic>, the introduction of foreign genes into a CoV genome is not an easy task (<xref rid="b0130" ref-type="bibr">de Haan et al., 2005</xref>, <xref rid="b0575" ref-type="bibr">Sola et al., 2003</xref>). Additionally, there are many examples of smaller RNA viruses containing numerous accessory genes that enhance virulence, such as HIV-1 at only a third of the typical CoV genome size (<xref rid="b0410" ref-type="bibr">Malim and Emerman, 2008</xref>).</p><p id="p0215">Second, it should be kept in mind that CoVs possess proofreading enzymes which limit their mutation rates drastically, compared to other RNA viruses (<xref rid="b0190" ref-type="bibr">Eckerle et al., 2010</xref>, <xref rid="b0265" ref-type="bibr">Hanada et al., 2004</xref>, <xref rid="b0435" ref-type="bibr">Minskaia et al., 2006</xref>). CoVs have thus likely evolved a fine balance between necessary mutation rates and RNA proofreading (<xref rid="b0145" ref-type="bibr">Denison et al., 2011</xref>). Assumptions of high CoV mutation rates are therefore probably only adequate in specific scenarios, such as the recent host switches of SARS- and MERS-CoV.</p><p id="p0220">Third, recombination may certainly occur during CoV replication, and the prototype example of the recombinant origins of FIPV type 2 was discussed above (<xref rid="b0275" ref-type="bibr">Herrewegh et al., 1998</xref>, <xref rid="b0485" ref-type="bibr">Pasternak et al., 2006</xref>). It should be noted, however, that other RNA viruses, such as the negative-stranded paramyxoviruses, which probably recombine much less than CoVs, still give rise to a huge number of likely zoonotic host switches from bats and birds into other mammals, at least rivalling the CoVs (<xref rid="b0160" ref-type="bibr">Drexler et al., 2012</xref>).</p><p id="p0225">The cumulative evidence suggests that at least four HCoVs share a likely zoonotic origin: HCoV-OC43 from bovines and HCoV-229E, SARS- and MERS-CoV from bats. In comparison, only three influenza A viruses (H1N1, H2N2 and H3N2) have so far successfully established circulation in the human population (<xref rid="b0480" ref-type="bibr">Palese, 2004</xref>). In contrast to CoVs, influenza A viruses cause regular epidemics or even pandemics. Still, the large number of zoonotic HCoVs emphasizes their potential to infect animals other than their original mammalian hosts, and demonstrates the value of continuous screening of humans and wildlife for potentially emerging pathogens. However, it should be kept in mind that sequence detection alone does not warrant premature conclusions as to the zoonotic potential of such viruses (<xref rid="b0140" ref-type="bibr">Deeks et al., 2013</xref>, <xref rid="b0175" ref-type="bibr">Drosten, 2013</xref>). Authentic risk assessment strategies would, for example, rely on infection experiments employing isolated or synthetically reconstructed viruses. In the specific case of the CoVs, identification of genomic markers associated with the viral potential to switch hosts or with increased pathogenicity may enable alternative studies. These markers could include viral interferon antagonists and the RBD, both of which could be analyzed <italic>in vitro</italic>, even in the absence of virus isolates or completely characterized genomes.</p><p id="p0230">Finally, any attempt to eradicate bats or other wildlife in reaction to virus descriptions should be strongly discouraged, as this counteracts the ecological relevance of these animals, e.g., for pollination and pest reduction (<xref rid="b0055" ref-type="bibr">Boyles et al., 2011</xref>, <xref rid="b0310" ref-type="bibr">Kalka et al., 2008</xref>).</p></sec></body><back><ref-list id="bi0005"><title>References</title><ref id="b0005"><element-citation publication-type="journal" id="h0005"><person-group person-group-type="author"><name><surname>Adams</surname><given-names>M.J.</given-names></name><name><surname>Carstens</surname><given-names>E.B.</given-names></name></person-group><article-title>Ratification vote on taxonomic proposals to the international committee on taxonomy of viruses (2012)</article-title><source>Arch. 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