Complete genome analysis of a SARS-like bat coronavirus identified in the Republic of Korea
Identifieur interne : 000070 ( Pmc/Corpus ); précédent : 000069; suivant : 000071Complete genome analysis of a SARS-like bat coronavirus identified in the Republic of Korea
Auteurs : Yongkwan Kim ; Kidong Son ; Young-Sik Kim ; Sook-Young Lee ; Weonhwa Jheong ; Jae-Ku OemSource :
- Virus Genes [ 0920-8569 ] ; 2019.
Abstract
Bats have been widely known as natural reservoir hosts of zoonotic diseases, such as severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) caused by coronaviruses (CoVs). In the present study, we investigated the whole genomic sequence of a SARS-like bat CoV (16BO133) and found it to be 29,075 nt in length with a 40.9% G+C content. Phylogenetic analysis using amino acid sequences of the ORF 1ab and the spike gene showed that the bat coronavirus strain 16BO133 was grouped with the Beta-CoV lineage B and was closely related to the JTMC15 strain isolated from
The online version of this article (10.1007/s11262-019-01668-w) contains supplementary material, which is available to authorized users.
Url:
DOI: 10.1007/s11262-019-01668-w
PubMed: 31076983
PubMed Central: 7089380
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PMC:7089380Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Complete genome analysis of a SARS-like bat coronavirus identified in the Republic of Korea</title><author><name sortKey="Kim, Yongkwan" sort="Kim, Yongkwan" uniqKey="Kim Y" first="Yongkwan" last="Kim">Yongkwan Kim</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0647 9913</institution-id><institution-id institution-id-type="GRID">grid.419585.4</institution-id><institution>Environmental Health Research Department,</institution><institution>National Institute of Environmental Research,</institution></institution-wrap>Hwangyeong-ro 42, Seo-gu, Incheon, Republic of Korea</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Son, Kidong" sort="Son, Kidong" uniqKey="Son K" first="Kidong" last="Son">Kidong Son</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0647 9913</institution-id><institution-id institution-id-type="GRID">grid.419585.4</institution-id><institution>Environmental Health Research Department,</institution><institution>National Institute of Environmental Research,</institution></institution-wrap>Hwangyeong-ro 42, Seo-gu, Incheon, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Kim, Young Sik" sort="Kim, Young Sik" uniqKey="Kim Y" first="Young-Sik" last="Kim">Young-Sik Kim</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Lee, Sook Young" sort="Lee, Sook Young" uniqKey="Lee S" first="Sook-Young" last="Lee">Sook-Young Lee</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Jheong, Weonhwa" sort="Jheong, Weonhwa" uniqKey="Jheong W" first="Weonhwa" last="Jheong">Weonhwa Jheong</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0647 9913</institution-id><institution-id institution-id-type="GRID">grid.419585.4</institution-id><institution>Environmental Health Research Department,</institution><institution>National Institute of Environmental Research,</institution></institution-wrap>Hwangyeong-ro 42, Seo-gu, Incheon, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Oem, Jae Ku" sort="Oem, Jae Ku" uniqKey="Oem J" first="Jae-Ku" last="Oem">Jae-Ku Oem</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31076983</idno><idno type="pmc">7089380</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7089380</idno><idno type="RBID">PMC:7089380</idno><idno type="doi">10.1007/s11262-019-01668-w</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000070</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000070</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Complete genome analysis of a SARS-like bat coronavirus identified in the Republic of Korea</title><author><name sortKey="Kim, Yongkwan" sort="Kim, Yongkwan" uniqKey="Kim Y" first="Yongkwan" last="Kim">Yongkwan Kim</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0647 9913</institution-id><institution-id institution-id-type="GRID">grid.419585.4</institution-id><institution>Environmental Health Research Department,</institution><institution>National Institute of Environmental Research,</institution></institution-wrap>Hwangyeong-ro 42, Seo-gu, Incheon, Republic of Korea</nlm:aff></affiliation><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Son, Kidong" sort="Son, Kidong" uniqKey="Son K" first="Kidong" last="Son">Kidong Son</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0647 9913</institution-id><institution-id institution-id-type="GRID">grid.419585.4</institution-id><institution>Environmental Health Research Department,</institution><institution>National Institute of Environmental Research,</institution></institution-wrap>Hwangyeong-ro 42, Seo-gu, Incheon, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Kim, Young Sik" sort="Kim, Young Sik" uniqKey="Kim Y" first="Young-Sik" last="Kim">Young-Sik Kim</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Lee, Sook Young" sort="Lee, Sook Young" uniqKey="Lee S" first="Sook-Young" last="Lee">Sook-Young Lee</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Jheong, Weonhwa" sort="Jheong, Weonhwa" uniqKey="Jheong W" first="Weonhwa" last="Jheong">Weonhwa Jheong</name><affiliation><nlm:aff id="Aff1"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0647 9913</institution-id><institution-id institution-id-type="GRID">grid.419585.4</institution-id><institution>Environmental Health Research Department,</institution><institution>National Institute of Environmental Research,</institution></institution-wrap>Hwangyeong-ro 42, Seo-gu, Incheon, Republic of Korea</nlm:aff></affiliation></author><author><name sortKey="Oem, Jae Ku" sort="Oem, Jae Ku" uniqKey="Oem J" first="Jae-Ku" last="Oem">Jae-Ku Oem</name><affiliation><nlm:aff id="Aff2"><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</nlm:aff></affiliation></author></analytic><series><title level="j">Virus Genes</title><idno type="ISSN">0920-8569</idno><idno type="eISSN">1572-994X</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p id="Par1">Bats have been widely known as natural reservoir hosts of zoonotic diseases, such as severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) caused by coronaviruses (CoVs). In the present study, we investigated the whole genomic sequence of a SARS-like bat CoV (16BO133) and found it to be 29,075 nt in length with a 40.9% G+C content. Phylogenetic analysis using amino acid sequences of the ORF 1ab and the spike gene showed that the bat coronavirus strain 16BO133 was grouped with the Beta-CoV lineage B and was closely related to the JTMC15 strain isolated from <italic>Rhinolophus ferrumequinum</italic> in China. However, 16BO133 was distinctly located in the phylogenetic topology of the human SARS CoV strain (Tor2). Interestingly, 16BO133 showed complete elimination of ORF8 regions induced by a frame shift of the stop codon in ORF7b. The lowest amino acid identity of 16BO133 was identified at the spike region among various ORFs. The spike region of 16BO133 showed 84.7% and 75.2% amino acid identity with Rf1 (SARS-like bat CoV) and Tor2 (human SARS CoV), respectively. In addition, the S gene of 16BO133 was found to contain the amino acid substitution of two critical residues (N479S and T487 V) associated with human infection. In conclusion, we firstly carried out whole genome characterization of the SARS-like bat coronavirus discovered in the Republic of Korea; however, it presumably has no human infectivity. However, continuous surveillance and genomic characterization of coronaviruses from bats are necessary due to potential risks of human infection induced by genetic mutation.</p><sec><title>Electronic supplementary material</title><p>The online version of this article (10.1007/s11262-019-01668-w) contains supplementary material, which is available to authorized users.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Brian, Da" uniqKey="Brian D">DA Brian</name></author><author><name sortKey="Baric, Rs" uniqKey="Baric R">RS Baric</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gonzalez, Jm" uniqKey="Gonzalez J">JM Gonzalez</name></author><author><name sortKey="Gomez Puertas, P" uniqKey="Gomez Puertas P">P Gomez-Puertas</name></author><author><name sortKey="Cavanagh, D" uniqKey="Cavanagh D">D Cavanagh</name></author><author><name sortKey="Gorbalenya, Ae" uniqKey="Gorbalenya A">AE 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Virus Genes</journal-id><journal-id journal-id-type="iso-abbrev">Virus Genes</journal-id><journal-title-group><journal-title>Virus Genes</journal-title></journal-title-group><issn pub-type="ppub">0920-8569</issn><issn pub-type="epub">1572-994X</issn><publisher><publisher-name>Springer US</publisher-name><publisher-loc>New York</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31076983</article-id><article-id pub-id-type="pmc">7089380</article-id><article-id pub-id-type="publisher-id">1668</article-id><article-id pub-id-type="doi">10.1007/s11262-019-01668-w</article-id><article-categories><subj-group subj-group-type="heading"><subject>Short Report</subject></subj-group></article-categories><title-group><article-title>Complete genome analysis of a SARS-like bat coronavirus identified in the Republic of Korea</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Kim</surname><given-names>Yongkwan</given-names></name><xref ref-type="aff" rid="Aff1">1</xref><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Son</surname><given-names>Kidong</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author"><name><surname>Kim</surname><given-names>Young-Sik</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Lee</surname><given-names>Sook-Young</given-names></name><xref ref-type="aff" rid="Aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Jheong</surname><given-names>Weonhwa</given-names></name><xref ref-type="aff" rid="Aff1">1</xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Oem</surname><given-names>Jae-Ku</given-names></name><address><phone>+82-63-850-0933</phone><email>jku0623@jbnu.ac.kr</email></address><xref ref-type="aff" rid="Aff2">2</xref></contrib><aff id="Aff1"><label>1</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0647 9913</institution-id><institution-id institution-id-type="GRID">grid.419585.4</institution-id><institution>Environmental Health Research Department,</institution><institution>National Institute of Environmental Research,</institution></institution-wrap>Hwangyeong-ro 42, Seo-gu, Incheon, Republic of Korea</aff><aff id="Aff2"><label>2</label><institution-wrap><institution-id institution-id-type="ISNI">0000 0004 0470 4320</institution-id><institution-id institution-id-type="GRID">grid.411545.0</institution-id><institution>Department of Veterinary Infectious Diseases, College of Veterinary Medicine,</institution><institution>Chonbuk National University,</institution></institution-wrap>Jeonju, Republic of Korea</aff></contrib-group><pub-date pub-type="epub"><day>10</day><month>5</month><year>2019</year></pub-date><pub-date pub-type="ppub"><year>2019</year></pub-date><volume>55</volume><issue>4</issue><fpage>545</fpage><lpage>549</lpage><history><date date-type="received"><day>22</day><month>2</month><year>2019</year></date><date date-type="accepted"><day>30</day><month>4</month><year>2019</year></date></history><permissions><copyright-statement>© Springer Science+Business Media, LLC, part of Springer Nature 2019</copyright-statement><license><license-p>This article is made available via the PMC Open Access Subset for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.</license-p></license></permissions><abstract id="Abs1"><p id="Par1">Bats have been widely known as natural reservoir hosts of zoonotic diseases, such as severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) caused by coronaviruses (CoVs). In the present study, we investigated the whole genomic sequence of a SARS-like bat CoV (16BO133) and found it to be 29,075 nt in length with a 40.9% G+C content. Phylogenetic analysis using amino acid sequences of the ORF 1ab and the spike gene showed that the bat coronavirus strain 16BO133 was grouped with the Beta-CoV lineage B and was closely related to the JTMC15 strain isolated from <italic>Rhinolophus ferrumequinum</italic> in China. However, 16BO133 was distinctly located in the phylogenetic topology of the human SARS CoV strain (Tor2). Interestingly, 16BO133 showed complete elimination of ORF8 regions induced by a frame shift of the stop codon in ORF7b. The lowest amino acid identity of 16BO133 was identified at the spike region among various ORFs. The spike region of 16BO133 showed 84.7% and 75.2% amino acid identity with Rf1 (SARS-like bat CoV) and Tor2 (human SARS CoV), respectively. In addition, the S gene of 16BO133 was found to contain the amino acid substitution of two critical residues (N479S and T487 V) associated with human infection. In conclusion, we firstly carried out whole genome characterization of the SARS-like bat coronavirus discovered in the Republic of Korea; however, it presumably has no human infectivity. However, continuous surveillance and genomic characterization of coronaviruses from bats are necessary due to potential risks of human infection induced by genetic mutation.</p><sec><title>Electronic supplementary material</title><p>The online version of this article (10.1007/s11262-019-01668-w) contains supplementary material, which is available to authorized users.</p></sec></abstract><kwd-group xml:lang="en"><title>Keywords</title><kwd>Bat</kwd><kwd>SARS-like coronavirus</kwd><kwd>Zoonotic disease</kwd><kwd>Frame shift</kwd><kwd>Whole genome</kwd></kwd-group><funding-group><award-group><funding-source><institution>National Research Foundation of Korea</institution></funding-source><award-id>NRF-2018R1D1A1B07041764</award-id><principal-award-recipient><name><surname>Oem</surname><given-names>Jae-Ku</given-names></name></principal-award-recipient></award-group></funding-group><custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name><meta-value>© Springer Science+Business Media, LLC, part of Springer Nature 2019</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="Sec1" sec-type="introduction"><title>Introduction</title><p id="Par2">Coronaviruses (CoVs) are enveloped viruses containing a single-stranded, positive-sense RNA genome of approximately 27–32 kb [<xref ref-type="bibr" rid="CR1">1</xref>]. Currently, CoVs are grouped under four distinct genera: <italic>Alphacoronavirus</italic>, <italic>Betacoronavirus</italic>, <italic>Gammacoronavirus</italic>, and <italic>Deltacoronavirus</italic> [<xref ref-type="bibr" rid="CR2">2</xref>, <xref ref-type="bibr" rid="CR3">3</xref>].</p><p id="Par3">Bat species have been recognized as major reservoirs of several emerging infectious diseases, such as severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS) [<xref ref-type="bibr" rid="CR4">4</xref>–<xref ref-type="bibr" rid="CR6">6</xref>]. SARS is caused by a member of the <italic>Betacoronavirus</italic> genus and is the first global pandemic disease that has emerged in the Guangdong Province of China in 2002. SARS has spread to 25 countries across five continents, infecting 8096 people worldwide with a 9.5% (774/8096) fatality [<xref ref-type="bibr" rid="CR7">7</xref>–<xref ref-type="bibr" rid="CR9">9</xref>].</p><p id="Par4">The four structural proteins (S, E, M, and N) are essential for viral entry and assembly. The S gene is the most important structural protein. The receptor-binding motif (RBM) within the receptor-binding domain (RBD) located in the S gene determines host tropism by binding angiotensin-converting enzyme 2 (ACE2) receptor [<xref ref-type="bibr" rid="CR10">10</xref>, <xref ref-type="bibr" rid="CR11">11</xref>]. The RBD has two critical residues (N479 and T487) that play key roles in ACE2 receptor recognition and binding associated with human transmission [<xref ref-type="bibr" rid="CR7">7</xref>, <xref ref-type="bibr" rid="CR12">12</xref>].</p><p id="Par5">Novel coronaviruses are continuously being discovered in bat species around the world, especially in China [<xref ref-type="bibr" rid="CR7">7</xref>, <xref ref-type="bibr" rid="CR13">13</xref>]. Due to relatively close geographic locations of bat species between China and the Republic of Korea, the surveillance of CoV prevalence and the analysis of their genetic information may be crucial for preventing a future outbreak [<xref ref-type="bibr" rid="CR14">14</xref>]. However, there have been few investigations into SARS-related bat Beta-CoV prevalence [<xref ref-type="bibr" rid="CR4">4</xref>]. In addition, whole genome analysis of SARS-related bat Beta-CoV has not yet been carried out in the Republic of Korea.</p><p id="Par6">Together with the fact that bats are reservoirs of CoVs, genetic information about these CoVs may provide valuable information regarding the possible risk of these viruses infecting humans. In the present study, the complete genome sequence of SARS-related Beta-CoV (16BO133) isolated from <italic>Rhinolophus ferrumequinum</italic> was first characterized. The genome of 16BO133 was then compared with that of reference CoVs to demonstrate genetic diversity and a potential genetic feature associated with host tropism.</p></sec><sec id="Sec2"><title>Results and discussion</title><p id="Par7">An oral swab was collected from bats living in their natural habitat in 2016. Bats were captured using a net for collection of oral swabs and were released immediately after sampling. Oral swab samples were kept in a viral transport medium at 4 °C. The oral swab sample was suspended in 1% antibiotic–antimycotic solution (Corning, USA) diluted in phosphate-buffered saline (PBS), and clarified by centrifugation at 3500×<italic>g</italic> for 10 min. RNA from the 200 μL sample was extracted with the QIAamp<sup>®</sup> Viral RNA mini kit (Qiagen, Germany) and eluted in 60 μL RNase-free water. cDNA was synthesized using a PrimeScript First Strand cDNA Synthesis kit (Takara, Japan) according to the manufacturer’s instructions. Bat-CoV screening was performed by a pancoronavirus PCR method based on primers as follows: (Corona forward, 5′-GGTTGGGACTATCCTAAGTGTGA-3′ and Corona reverse, 5′-CCATCATCAGATAG AATCATCATA-3′). The pancoronavirus primers were used to amplify and sequence a 440-bp segment of the highly conserved RNA-dependent RNA polymerase (RdRp) gene. Fifty-nine pairs of primers were synthesized by the Genotech corporation (Daejeon, Korea) and PCR was performed using an ABI 9800 GeneAmp system (Applied Biosystems, Foster City, CA, USA). The products were purified using a QIAquick gel extraction kit (Qiagen, Germany) according to the manufacturer’s instructions. The purified PCR products were sequenced using the BigDye<sup>®</sup> Terminator Cycle Sequencing kit version 1.1 (Applied Biosystems, Foster City, CA, USA) and an ABI 3730 DNA sequencer (Applied Biosystems, Foster City, CA, USA). Whole genome sequences were submitted to GenBank (accession number KY938558). The nucleotide and amino acid sequences were aligned and compared to CoV sequences available from the GenBank database using ClustalW software implemented in BioEdit version 7.0.9.0. The phylogenetic trees were drawn using the neighboring joining method using the maximum composite likelihood model with MEGA 7 software. The bootstrap values were calculated with 1000 replicates.</p><p id="Par8">The amino acid sequences of ORF 1ab and spike gene were analyzed for phylogenetic characterization. 16BO133 was grouped with the SARS-related Beta-CoV lineage B, not only due to sequence similarity with ORF 1ab but also with the spike gene (Fig. <xref rid="Fig1" ref-type="fig">1</xref>). The RF 1ab and spike amino acids were closely related to JTMC15. However, 16BO133 was distinctly located in the phylogenetic topology of the human SARS CoV strain (Tor2, Urbani, Frankfurt1, and ShanghaiQXC1).<fig id="Fig1"><label>Fig. 1</label><caption><p>Phylogenetic analysis using whole genome sequences of ORF 1ab with reference strains. The phylogenetic trees were drawn using the neighboring joining method using the maximum composite likelihood model with MEGA 7 software. The bootstrap values were calculated with 1000 replicates. Phylogenetic analysis using whole genome sequences of the spike region with reference strains. The phylogenetic trees were drawn using the neighboring joining method using the maximum composite likelihood model with MEGA 7 software. The bootstrap values were calculated with 1000 replicates</p></caption><graphic xlink:href="11262_2019_1668_Fig1_HTML" id="MO1"></graphic></fig></p><p id="Par9">The whole genomic sequence of 16BO133 was 29,075 nt in length with G+C contents of 40.9%. As shown in Table <xref rid="Tab1" ref-type="table">1</xref>, 16BO133 has a similar genome organization to other SARS-related Beta-CoVs, such as JTMC15, Rf1, and Tor2. The 16BO133 showed a high amino acid identity ranging from 93.8% to 100% with JTMC15. However, it showed considerably lower nucleotide identity ranging from 75.2 to 99.5% with Rf1 and Tor2 (Table <xref rid="Tab1" ref-type="table">1</xref>). In addition, a complete deletion of amino acids was observed in the ORF8 region, which is similar to JTMC15 (Table <xref rid="Tab1" ref-type="table">1</xref>). The spike gene nucleotides of 16BO133 showed extensive variations compared to other SARS-related bat Beta-CoV (Rf1) and human SARS CoV (Tor2), thereby resulting in a low amino acid identity. Amino acid identities of 16BO133 spike region with Rf1 and Tor2 were 84.7% and 75.2%, respectively (Table <xref rid="Tab1" ref-type="table">1</xref>).<table-wrap id="Tab1"><label>Table 1</label><caption><p>Comparison of ORF amino acid identities of 16BO133 and other SARS-CoVs</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="2">ORF</th><th align="left">16BO133</th><th align="left" colspan="2">JTMC15</th><th align="left" colspan="2">Rf1</th><th align="left" colspan="2">Tor2</th></tr><tr><th align="left">Length</th><th align="left">Length</th><th align="left">% Identity</th><th align="left">Length</th><th align="left">% Identity</th><th align="left">Length</th><th align="left">% Identity</th></tr></thead><tbody><tr><td align="left">1a</td><td align="left">4184</td><td align="left">4184</td><td align="left">99.3</td><td align="left">4377</td><td align="left">98.2</td><td align="left">4377</td><td align="left">93.4</td></tr><tr><td align="left">1b</td><td align="left">2646</td><td align="left">2646</td><td align="left">99.5</td><td align="left">2628</td><td align="left">98.2</td><td align="left">2641</td><td align="left">98.1</td></tr><tr><td align="left">S</td><td align="left">1236</td><td align="left">1236</td><td align="left">99.4</td><td align="left">1241</td><td align="left">84.7</td><td align="left">1255</td><td align="left">75.2</td></tr><tr><td align="left">3a</td><td align="left">270</td><td align="left">274</td><td align="left">98.5</td><td align="left">274</td><td align="left">97.0</td><td align="left">274 (ORF3)<sup>a</sup></td><td align="left">85.2</td></tr><tr><td align="left">3b</td><td align="left">114</td><td align="left">114</td><td align="left">99.1</td><td align="left">114</td><td align="left">96.5</td><td align="left">154 (ORF4)<sup>a</sup></td><td align="left">89.5</td></tr><tr><td align="left">E</td><td align="left">76</td><td align="left">76</td><td align="left">97.4</td><td align="left">76</td><td align="left">97.4</td><td align="left">76</td><td align="left">98.7</td></tr><tr><td align="left">M</td><td align="left">221</td><td align="left">221</td><td align="left">99.5</td><td align="left">221</td><td align="left">99.5</td><td align="left">221</td><td align="left">97.3</td></tr><tr><td align="left">6</td><td align="left">63</td><td align="left">63</td><td align="left">98.4</td><td align="left">63</td><td align="left">98.4</td><td align="left">63 (ORF7)<sup>a</sup></td><td align="left">92.1</td></tr><tr><td align="left">7a</td><td align="left">122</td><td align="left">122</td><td align="left">97.5</td><td align="left">122</td><td align="left">95.9</td><td align="left">122 (ORF8)<sup>a</sup></td><td align="left">89.3</td></tr><tr><td align="left">7b</td><td align="left">48</td><td align="left">52</td><td align="left">93.75</td><td align="left">44</td><td align="left">97.7</td><td align="left">44 (ORF9)<sup>a</sup></td><td align="left">93.2</td></tr><tr><td align="left">8</td><td align="left">–</td><td align="left">–</td><td align="left">–</td><td align="left">122</td><td align="left">–</td><td align="left">39 (ORF10)<sup>a</sup></td><td align="left">–</td></tr><tr><td align="left">N</td><td align="left">420</td><td align="left">420</td><td align="left">99.3</td><td align="left">421</td><td align="left">97.1</td><td align="left">422</td><td align="left">94.3</td></tr><tr><td align="left">9a</td><td align="left">97</td><td align="left">97</td><td align="left">95.9</td><td align="left">97</td><td align="left">94.8</td><td align="left">98 (ORF13)<sup>a</sup></td><td align="left">75.3</td></tr><tr><td align="left">9b</td><td align="left">70</td><td align="left">70</td><td align="left">100</td><td align="left">70</td><td align="left">94.3</td><td align="left">70 (ORF14)<sup>a</sup></td><td align="left">84.3</td></tr></tbody></table><table-wrap-foot><p>Abbreviation and accession numbers: JTMC15, KU182964; Rf1, DQ412042; Tor2, AY274119</p><p><sup>a</sup>ORF 3a, 3b, 6, 7a, 7b, 8, 9a, and 9b are described as ORF 3, 4, 7, 8, 9, 10, 13, and 14 in Tor2</p></table-wrap-foot></table-wrap></p><p id="Par10">As shown in Supplementary Fig. 1, the RBM (aa 426–518) located in the S protein showed 18 amino acid deletions (aa 433–437 and 457–469) including critical residues, N479S and T487V. The regions corresponding to TGNYN (433–437) and NVPFSPDGKPCTP (457–469) in human SARS CoV (Tor2) were identified as the major deletion sites in 16BO133. In addition, the insertion of the two nucleotides (cytosine and threonine) was observed in front of the stop codon of ORF7b in 16BO133 (Supplementary Fig. 2). This feature induces a frame shift of the stop codon, resulting in the complete elimination of ORF8.
</p><p id="Par11">The bats discovered in the Republic of Korea are considered to be insectivores, and 23 species were reported to exist in this region in a previous study [<xref ref-type="bibr" rid="CR4">4</xref>]. Recently, wildlife and human contact has increased due to the rapid urbanization. People think that bats are not dangerous because they either living in caves or in abandoned mines. In the present study, SARS-related bat Beta-CoV was identified from <italic>R. ferrumequinum</italic> in an abandoned mine at the Jeonbuk province. Recently, some people visited the abandoned mine out of curiosity, not realizing the risk of exposure to CoV infections upon contact with bat carriers. Therefore, people should keep in mind that bats can spread diseases to humans and should refrain from visiting abandoned mines.</p><p id="Par12">The S gene associated with the spike protein is divided into S1 and S2 domains [<xref ref-type="bibr" rid="CR15">15</xref>–<xref ref-type="bibr" rid="CR17">17</xref>]. The S gene is composed of distinct N-terminal (S1) and conserved C-terminal (S2) domains. The S1 domain is prone to have high mutation rates as the virus evolves because it is the major antigenic factor. Therefore, it is thought to be the main reason that the spike protein of 16BO133 has the lowest amino acid identity (75.2%) compared to human SARS CoV (Tor2) within various ORFs.</p><p id="Par13">The S1 domain contains a receptor-binding domain (RBD), which mediates receptor binding of the virus to host cells and determines the host spectrum. The RBM (aa 426 to 518) within the RBD (aa 319 to 518) is the most important motif for recognizing the host receptor, human angiotensin-converting enzyme 2 (ACE2), and it is a major antigenic determinant required to elicit the production of neutralizing antibodies. The RBM has two critical residues, N479 and T487, which play key roles in receptor recognition and binding [<xref ref-type="bibr" rid="CR15">15</xref>]. The substitution of these two critical residues can completely eliminate viral binding to the human ACE2 receptor [<xref ref-type="bibr" rid="CR12">12</xref>]. However, substitution of ether residue alone has no significant impact on human ACE2 binding [<xref ref-type="bibr" rid="CR18">18</xref>]. In the present study, the S gene of 16BO133 (1236 aa) showed a difference of 19 amino acids when compared to SARS CoV (Tor2, 1255 aa) due to 5 aa insertions and 24 aa deletions. Of the 24 aa deletions, 75% (18/24) were located in the RBD. In conclusion, it is thought that 16BO133 may have very low possibility to human infection due to the mutation of two critical residues (N479S and T487V), two major deletion sites (433–437, 457–469) in the RBD and low amino acid identity (75.2%) of S gene with SARS CoV Tor2.</p><p id="Par14">According to previous reports [<xref ref-type="bibr" rid="CR4">4</xref>], B15-21 bat CoV was identified from <italic>R. ferrumequinum</italic> and firstly reported in Republic of Korea. The B15-21 was clustered with the <italic>Betacoronavirus</italic> and grouped with SARS-like bat CoV found in China. The receptor-binding domain (RBD) of B15-21 had two major deletion sites, TGNYN and PFSPDGKPCTPPA, compared to human SARS CoV Tor2. The 16BO133 also had two major deletion sites in RBD, TGNYN (433–437) and NVPFSPDGKPCTP (457–469), compared to human SARS CoV Tor2. The amino acid differences between B15-21 (PFSPDGKPCTPPA) and 16BO133 (NVPFSPDGKPCTP) are evolving evidence of SARS-like bat CoV in Republic of Korea.</p><p id="Par15">The ORF8 region located upstream of the N gene is known to be a “high mutation region” from previous reports [<xref ref-type="bibr" rid="CR3">3</xref>, <xref ref-type="bibr" rid="CR19">19</xref>]. Most human SARS CoVs during epidemic had undergone 29 nucleotides deletion in ORF8 compared to civet SARS CoV, suggesting that this region may be important for interspecies transmission [<xref ref-type="bibr" rid="CR20">20</xref>]. In the present study, a complete deletion of amino acids was observed in the ORF8 region of 16BO133. Interestingly, insertion of two nucleotides (cytosine and threonine) was observed in front of the stop codon of ORF7b. The insertion of two nucleotides induced an ORF frame shift resulting in addition of four amino acids of ORF7b and an elimination of the start codon of ORF8. Further studies are needed on how these changes will influence SARS-like bat CoV.</p><p id="Par16">According to previous reports, SARS-like bat CoV (RP3) was first discovered in China [<xref ref-type="bibr" rid="CR19">19</xref>]. The overall sequence identity between RP3 and human SARS CoV Tor2 was 92%. However, the S1 domain of the S protein showed 64% sequence identity due to amino acid deletions. After the discovery of RP3, two novel SARS-like bat CoVs (Rs3367 and LYRa11) have been described, which are more closely related to human SARS CoV Tor2 [<xref ref-type="bibr" rid="CR7">7</xref>, <xref ref-type="bibr" rid="CR20">20</xref>]. Rs3367 and LYRa11 have high amino acid identities of 89.6% to 89.9%, respectively, with human SARS CoV Tor2, particularly in the RBM region without amino acid deletion. The evolution of the CoV can lead to a novel CoV that is highly contagious in humans, which can lead to a serious problem.</p><p id="Par17">In conclusion, the CoV can possibly be transmitted to human populations due to CoV mutations occurring as a result of high mutation rates as the virus evolves. Therefore, continuous monitoring and genomic sequence characterization of the SARS-like bat CoV should be performed to prevent human infections that may result from genetic variation.</p></sec><sec sec-type="supplementary-material"><title>Electronic supplementary material</title><sec id="Sec3"><p>Below is the link to the electronic supplementary material.
<supplementary-material content-type="local-data" id="MOESM1"><media xlink:href="11262_2019_1668_MOESM1_ESM.pptx"><caption><p>Supplemental Fig. 1. The comparison of amino acids between SARS-like bat CoVs and human SARS CoV in the receptor-binding motif (RBM). Major deletion sites are marked in gray color. The two critical residues (N479 and T487) that play key roles in human ACE2 receptor recognition and binding are marked in asterisks. Supplemental Fig. 2. The comparison of amino acid sequences between ORF7b and ORF8 regions. Insertion of the two nucleotides (cytosine and threonine) is marked by a blue rectangle. The stop codons of ORF7b are marked by red rectangles. The start codon of ORF8 is marked by a black circle above the nucleotide ATG letters. Supplementary material 1 (PPTX 104 kb)</p></caption></media></supplementary-material></p></sec></sec></body><back><fn-group><fn><p>Edited by Zhen F. Fu.</p></fn><fn><p><bold>Publisher's Note</bold></p><p>Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p></fn></fn-group><ack><p>This study was funded (Grant Number. 2016-01-01-033) by the National Institute of Environmental Research (NIER), Ministry of Environment, Republic of Korea. This study was supported by the National Research Foundation of Korea (Grant Number. NRF-2018R1D1A1B07041764).</p></ack><notes notes-type="author-contribution"><title>Author contributions</title><p>YK and JKO conceived and designed the experiments. YK and KS performed the experiments. YK, YSK, SYL, and WJ analyzed the data. JKO and YK wrote the paper. 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