AHMED, SS

Ahmed, Z

Lau, SKP

Mahbub, AM

Tsang, KL

Wong, CP

Woo, PCY

Yuen, KY

New Microbes and New Infections

HKU Scholars Hub

Title First genome sequences of buffalo coronavirus from waterbuffaloes in BangladeshAuthor(s) Lau, SKP; Tsang, KL; AHMED, SS; Mahbub, AM; Ahmed, Z;Wong, CP; Yuen, KY; Woo, PCYCitation New Microbes and New Infection, 2016, v. 11, p. 54-56Issued Date 2016URL http://hdl.handle.net/10722/229339Rights This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.TAXONOGENOMICS: GENOME OF A NEW ORGANISMFirst genome sequences of buffalo coronavirus from water buffaloes inBangladeshS. K. P. Lau1,2,3,4, A. K. L. Tsang1, S. Shakeel Ahmed1, M. Mahbub Alam5, Z. Ahmed6, P.-C. Wong1, K.-Y. Yuen1,2,3,4 andP. C. Y. Woo1,2,3,41) Department of Microbiology, 2) State Key Laboratory of Emerging Infectious Diseases, 3) Research Centre of Infection and Immunology, 4) Carol Yu Centre forInfection, The University of Hong Kong, Hong Kong, China, 5) United Hospital Limited and 6) BRAC Dairy and Food Project, BRAC Enterprises, Dhaka, BangladeshAbstractWe report the complete genome sequences of a buffalo coronavirus (BufCoV HKU26) detected from the faecal samples of two domesticwater buffaloes (Bubalus bubalis) in Bangladesh. They possessed 98–99% nucleotide identities to bovine coronavirus (BCoV) genomes,supporting BufCoV HKU26 as a member of Betacoronavirus 1. Nevertheless, BufCoV HKU26 possessed distinct accessory proteinsbetween spike and envelope compared to BCoV. Sugar-binding residues in the N-terminal domain of S protein in BCoV are conserved inBufCoV HKU26.New Microbes and New Infections © 2016 The Authors. Published by Elsevier Ltd on behalf of European Society of Clinical Microbiology andInfectious Diseases.Keywords: Coronavirus, water buffaloOriginal Submission: 29 January 2016; Accepted: 23 February 2016Article published online: 3 March 2016NeNeThhttCorresponding authors: S. K. P. Lau and P. C. Y. Woo,Department of Microbiology, The University of Hong Kong, Room423, University Pathology Building, Queen Mary Hospital Compound,Pokfulam Road, Hong Kong, ChinaE-mails: skplau@hku.hk (S.K.P. Lau), pcywoo@hku.hk(P.C.Y. Woo)The ﬁrst two authors contributed equally to this article, and bothshould be considered ﬁrst author.Coronaviruses are classiﬁed into four genera, with bat coro-naviruses known as the gene source of Alphacoronavirus andBetacoronavirus, and avian coronaviruses as the gene source ofGammacoronavirus and Deltacoronavirus [1,2]. However, lineageA Betacoronavirus is unique among the genus in originating inrodents instead of bats [3]. Lineage A Betacoronavirus comprisesseveral coronavirus species, including murine coronavirus, hu-man coronavirus HKU1, Chinese Rattus coronavirus HKU24,rabbit coronavirus HKU14 and Betacoronavirus 1 [3–5]. Beta-coronavirus 1 is best known for its tendency for recombinationand interspecies transmission among various mammalian spe-cies [3,6,7]. In particular, human coronavirus OC43 (HCoVOC43) likely originated from a relatively recent zoonoticw Microbe and New Infect 2016; 11: 54–56w Microbes and New Infections © 2016 The Authors. Published by Elsevier Ltd on behalf ofis is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licep://dx.doi.org/10.1016/j.nmni.2016.02.011transmission event, with the most recent common ancestor ofHCoV OC43 and bovine coronavirus (BCoV) dating to around1890 [8]. Besides cattle, BCoV-like viruses have been detectedin various ungulates, including water buffalo calves withgastroenteritis in Italy [9,10]. However, only partial gene se-quences, the longest one being ~9.6 kb spanning ORF1b tonucleocapsid (N), were obtained from the buffalo viruses[9,10].We report the complete genome sequences of a buffalocoronavirus (BufCoV HKU26) detected from the faecal samplesof two domestic adult water buffaloes (Bubalus bubalis) inBangladesh. RT-PCR for coronavirus detection, and completegenome sequencing and analysis were performed as describedpreviously [11,12]. The genomes of BufCoV HKU26 strains B1-24F and B1-28F were 31 021 and 30 975 in length, with G+Ccontent of 40%. They possessed 98–99% nucleotide identitiesto the genomes of BCoVs, supporting the classiﬁcation ofBufCoV HKU26 as a member of the species Betacoronavirus 1(Fig. 1). The genome organization is also characteristic of line-age A Betacoronavirus, with the putative transcription regulatorysequence motif 50-C(U/C)AAAC-30 (Fig. 1). The two BufCoVHKU26 genomes encode ﬁve putative accessory proteinsEuropean Society of Clinical Microbiology and Infectious Diseasesnses/by-nc-nd/4.0/)FIG. 1. Phylogenetic tree constructed from complete genomes of BufCoV and other members of Betacoronavirus lineage A (top). Tree was con-structed by maximum likelihood method using general-time-reversible model including proportion of invariable sites with gamma-distributed sub-stitution rates and bootstrap values calculated from 100 trees. Betacoronavirus 1 indicated at right. Boldface type indicates 2 strains of BufCoV withcomplete genomes sequenced in this study. SACoV, sable antelope coronavirus (EF424621); GiCoV, giraffe coronavirus (EF424623); ACoV, alpacacoronavirus (DQ915164); WtDCoV, white-tailed deer coronavirus (FJ425187); SDCoV, sambar deer coronavirus (FJ425189); WbCoV, waterbuckcoronavirus (FJ425186); BCoV, bovine coronavirus (DQ811784); BufCoV, buffalo coronavirus; DcCoV, dromedary camel coronavirus (KF906249);CRCoV, canine respiratory coronavirus (JX860640); HCoV OC43, human coronavirus OC43 (AY391777); PHEV, porcine haemagglutinatingencephalomyelitis virus (DQ011855); ECoV, equine coronavirus (EF446615); RbCoV HKU14, rabbit coronavirus HKU14 (JN874559); ChRCoV,China Rattus coronavirus HKU24 (KM349742); HCoV HKU1, human coronavirus HKU1 (AY597011); MHV, murine hepatitis virus (FJ647223); RCoV,rat coronavirus (FJ938068). Genome organization of BufCoV (bottom). Position of transcriptional regulatory sequences of each gene is indicated.ORFs between spike (S) and envelope (E) gene are magniﬁed to show differences between two BufCoVs. ORF1ab are represented by green boxes.Haemagglutinin-esterase (HE), S, E, membrane (M) and nucleocapsid (N) are represented by red boxes. Putative accessory proteins are represented byblue boxes.NMNI Lau et al. Water buffalo coronavirus genomes 55New Microbes and New Infections © 2016 The Authors. Published by Elsevier Ltd on behalf of European Society of Clinical Microbiology and Infectious Diseases, NMNI, 11, 54–56This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/)56 New Microbes and New Infections, Volume 11 Number C, May 2016 NMNIconserved among most members of Betacoronavirus 1, includinga 32 kDa protein between ORF1ab and haemagglutinin-esterase, three proteins between spike (S) and envelope (E)and one internal protein overlapping with N. In BCoV, thethree proteins between S and E were of typical size: 4.9, 4.8 and12.8 kDa respectively. In BufCoV, the 4.9 kDa protein isreplaced by a 2.9 kDa protein (25 aa) due to a premature stopcodon. The 4.8 kDa protein of BufCoV HKU26 was alsodifferent from that of BCoVs, with a smaller protein of 29 aa instrain B1-24F and a protein of 44 aa in strain B1-28F due to aframeshift mutation caused by a single nucleotide deletion afterthe original start codon. Compared to other BCoV-like viruses,BufCoV HKU26 possessed a unique serine/asparagine sub-stitution at position 354 of N protein. In contrast to murinecoronavirus, which utilizes carcinoembryonic antigen–relatedcell adhesion molecule 1 as a receptor, BCoV and HCoV OC43bind to N-acetyl-9-O acetyl neuraminic acid for cell entry[13,14]. All the known critical and noncritical sugar-bindingresidues in the N-terminal domain of S protein in BCoV areconserved in BufCoV HKU26 [15]. The genome sequences ofBufCoV HKU26 have been lodged at GenBank under accessionnumbers KU558922 and KU558923.Conﬂict of InterestNone declared.AcknowledgementsWe are grateful for the generous support of C. Yu, R. Yu, H.Hoy and H. Ming in the genomic sequencing platform. Sup-ported in part by Theme-Based Research Scheme (project T11/707/15) and Research Grant Council Grant, University GrantCouncil; Strategic Research Theme Fund, University Develop-ment Fund and Special Research Achievement Award, TheUniversity of Hong Kong; and Croucher Senior MedicalResearch Fellowships.References[1] de Groot RJ, Baker SC, Baric R, Enjuanes L, Gorbalenya A, Holmes KB,et al. Coronaviridae. In: King AMQ, Adams MJ, Carstens EB,New Microbes and New Infections © 2016 The Authors. Published by Elsevier Ltd on behalf ofThis is an open access article under the CC BY-NC-ND license (http://creativecommons.org/liceLefkowitz EJ, editors. Virus taxonomy, classiﬁcation and nomenclatureof viruses: ninth report of the International Committee on Taxonomyof Viruses, International Union of Microbiological Societies, VirologyDivision. Amsterdam: Elsevier Academic Press; 2011. p. 806–8.[2] Woo PC, Lau SK, Lam CS, Lau CC, Tsang AK, Lau JH, et al. Discoveryof seven novel mammalian and avian coronaviruses in the genus del-tacoronavirus supports bat coronaviruses as the gene source ofalphacoronavirus and betacoronavirus and avian coronaviruses as thegene source of gammacoronavirus and deltacoronavirus. J Virol2012;86:3995–4008.[3] Lau SK, Woo PC, Li KS, Tsang AK, Fan RY, Luk HK, et al. Discovery ofa novel coronavirus, China Rattus coronavirus HKU24, from Norwayrats supports the murine origin of Betacoronavirus 1 and has implica-tions for the ancestor of Betacoronavirus lineage A. J Virol 2015;89:3076–92.[4] Lau SK, Woo PC, Yip CC, Fan RY, Huang Y, Wang M, et al. Isolationand characterization of a novel Betacoronavirus subgroup A corona-virus, rabbit coronavirus HKU14, from domestic rabbits. J Virol2012;86:5481–96.[5] Woo PC, Lau SK, Chu CM, Chan KH, Tsoi HW, Huang Y, et al.Characterization and complete genome sequence of a novel corona-virus, coronavirus HKU1, from patients with pneumonia. J Virol2005;79:884–95.[6] Woo PC, Lau SK, Wernery U, Wong EY, Tsang AK, Johnson B, et al.Novel betacoronavirus in dromedaries of the Middle East, 2013. EmergInfect Dis 2014;20:560–72.[7] Lau SK, Lee P, Tsang AK, Yip CC, Tse H, Lee RA, et al. Molecularepidemiology of human coronavirus OC43 reveals evolution ofdifferent genotypes over time and recent emergence of a novel ge-notype due to natural recombination. J Virol 2011;85:11325–37.[8] Vijgen L, Keyaerts E, Moes E, Thoelen I, Wollants E, Lemey P, et al.Complete genomic sequence of human coronavirus OC43: molecularclock analysis suggests a relatively recent zoonotic coronavirus trans-mission event. J Virol 2005;79:1595–604.[9] Decaro N, Cirone F, Mari V, Nava D, Tinelli A, Elia G, et al. Char-acterisation of bubaline coronavirus strains associated with gastroen-teritis in water buffalo (Bubalus bubalis) calves. Vet Microbiol 2010;145:245–51.[10] Decaro N, Martella V, Elia G, Campolo M, Mari V, Desario C, et al.Biological and genetic analysis of a bovine-like coronavirus isolatedfrom water buffalo (Bubalus bubalis) calves. Virology 2008;5(370):213–22.[11] Lau SK, Woo PC, Li KS, Huang Y, Wang M, Lam CS, et al. Completegenome sequence of bat coronavirus HKU2 from Chinese horseshoebats revealed a much smaller spike gene with a different evolutionarylineage from the rest of the genome. Virology 2007;367:428–39.[12] Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW, Wong BH, et al. Severeacute respiratory syndrome coronavirus-like virus in Chinese horse-shoe bats. Proc Natl Acad Sci U S A 2005;27(102):14040–5.[13] Vlasak R, Luytjes W, Spaan W, Palese P. Human and bovine corona-viruses recognize sialic acid–containing receptors similar to those ofinﬂuenza C viruses. Proc Natl Acad Sci U S A 1988;85:4526–9.[14] Williams RK, Jiang GS, Holmes KV. Receptor for mouse hepatitis virusis a member of the carcinoembryonic antigen family of glycoproteins.Proc Natl Acad Sci U S A 1991;88:5533–6.[15] Peng G, Xu L, Lin YL, Chen L, Pasquarella JR, Holmes KV, et al. Crystalstructure of bovine coronavirus spike protein lectin domain. J BiolChem 2012;287:41931–8.European Society of Clinical Microbiology and Infectious Diseases, NMNI, 11, 54–56nses/by-nc-nd/4.0/)

First genome sequences of buffalo coronavirus from water buffaloes in Bangladesh

First genome sequences of buffalo coronavirus from water buffaloes in Bangladesh

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