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. 2012 Apr;86(7):3995-4008.
doi: 10.1128/JVI.06540-11. Epub 2012 Jan 25.

Discovery of seven novel Mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus

Patrick C Y Woo  1 , Susanna K P Lau, Carol S F Lam, Candy C Y Lau, Alan K L Tsang, John H N Lau, Ru Bai, Jade L L Teng, Chris C C Tsang, Ming Wang, Bo-Jian Zheng, Kwok-Hung Chan, Kwok-Yung Yuen
Affiliations

Discovery of seven novel Mammalian and avian coronaviruses in the genus deltacoronavirus supports bat coronaviruses as the gene source of alphacoronavirus and betacoronavirus and avian coronaviruses as the gene source of gammacoronavirus and deltacoronavirus

Patrick C Y Woo et al. J Virol. 2012 Apr.

Abstract

Recently, we reported the discovery of three novel coronaviruses, bulbul coronavirus HKU11, thrush coronavirus HKU12, and munia coronavirus HKU13, which were identified as representatives of a novel genus, Deltacoronavirus, in the subfamily Coronavirinae. In this territory-wide molecular epidemiology study involving 3,137 mammals and 3,298 birds, we discovered seven additional novel deltacoronaviruses in pigs and birds, which we named porcine coronavirus HKU15, white-eye coronavirus HKU16, sparrow coronavirus HKU17, magpie robin coronavirus HKU18, night heron coronavirus HKU19, wigeon coronavirus HKU20, and common moorhen coronavirus HKU21. Complete genome sequencing and comparative genome analysis showed that the avian and mammalian deltacoronaviruses have similar genome characteristics and structures. They all have relatively small genomes (25.421 to 26.674 kb), the smallest among all coronaviruses. They all have a single papain-like protease domain in the nsp3 gene; an accessory gene, NS6 open reading frame (ORF), located between the M and N genes; and a variable number of accessory genes (up to four) downstream of the N gene. Moreover, they all have the same putative transcription regulatory sequence of ACACCA. Molecular clock analysis showed that the most recent common ancestor of all coronaviruses was estimated at approximately 8100 BC, and those of Alphacoronavirus, Betacoronavirus, Gammacoronavirus, and Deltacoronavirus were at approximately 2400 BC, 3300 BC, 2800 BC, and 3000 BC, respectively. From our studies, it appears that bats and birds, the warm blooded flying vertebrates, are ideal hosts for the coronavirus gene source, bats for Alphacoronavirus and Betacoronavirus and birds for Gammacoronavirus and Deltacoronavirus, to fuel coronavirus evolution and dissemination.

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Figures

Fig 1
Fig 1
Phylogenetic analysis of amino acid sequences of the 228-bp fragment (excluding primer sequences) of RNA-dependent RNA polymerase (RdRp) of CoVs identified from dead wild birds and pigs in the present study. The tree was constructed by the neighbor joining method using Kimura correction and bootstrap values calculated from 1,000 trees. The scale bar indicates the estimated number of substitutions per 20 amino acids. The eight genomes completely sequenced are shown in bold. PEDV, porcine epidemic diarrhea virus (NC_003436); Sc-BatCoV-512, Scotophilus bat coronavirus 512 (NC_009657); TGEV, transmissible gastroenteritis virus (NC_002306); FIPV, feline infectious peritonitis virus (AY994055); CCoV, canine coronavirus (GQ477367); PRCV, porcine respiratory coronavirus (DQ811787); Rh-BatCoV-HKU2, Rhinolophus bat coronavirus HKU2 (EF203064); Mi-BatCoV 1A, Miniopterus bat coronavirus 1A (NC_010437); Mi-BatCoV 1B, Miniopterus bat coronavirus 1B (NC_010436); Mi-BatCoV-HKU8, Miniopterus bat coronavirus HKU8 (NC_010438); HCoV-229E, human coronavirus 229E (NC_002645); HCoV-NL63, human coronavirus NL63 (NC_005831); HCoV OC43, human coronavirus OC43 (NC_005147); BCoV, bovine coronavirus (NC_003045); AntelopeCoV, sable antelope CoV (EF424621); GiCoV, giraffe coronavirus (EF424622); ECoV, equine coronavirus (NC_010327); PHEV, porcine hemagglutinating encephalomyelitis virus (NC_007732); MHV, murine hepatitis virus (NC_001846); RCoV, rat coronavirus (NC_012936); HCoV-HKU1, human coronaivurs HKU1 (NC_006577); Ty-BatCoV-HKU4, Tylonycteris bat coronavirus HKU4 (NC_009019); Pi-BatCoV-HKU5, Pipistrellus bat coronavirus HKU5 (NC_009020); SARS CoV, SARS-related human coronavirus (NC_004718); SARSr-Rh-BatCoV HKU3, SARS-related Rhinolophus bat coronavirus HKU3 (DQ022305); SARSr CoV CFB, SARS-related Chinese ferret badger coronavirus (AY545919); SARSr-CiCoV, SARS-related palm civet coronavirus (AY304488); Ro-BatCoV-HKU9, Rousettus bat coronavirus HKU9 (NC_009021); IBV, infectious bronchitis virus (NC_001451); IBV-partridge, partridge coronavirus (AY646283); TCoV, turkey coronavirus (NC_010800); IBV-peafowl, peafowl coronavirus (AY641576); BWCoV-SW1, beluga whale coronavirus SW1 (NC_010646); ALCCoV, Asian leopard cat coronavirus (EF584908); BuCoV HKU11, bulbul coronavirus HKU11(FJ376619); ThCoV HKU12, thrush coronavirus HKU12 (FJ376621); MunCoV HKU13, munia coronavirus HKU13 (FJ376622); PorCoV HKU15, porcine coronavirus HKU15; WECoV HKU16, white-eye coronavirus HKU16; SpCoV HKU17 (TrSp, tree sparrow), sparrow coronavirus HKU17; MRCoV HKU18 (OMR, oriental magpie robin), magpie robin coronavirus HKU18; NHCoV HKU19 (BlCrNH, black-crowned night heron), night heron coronavirus HKU19; WiCoV HKU20 (EuWi, Eurasian wigeon), wigeon coronavirus HKU20; CMCoV HKU21, common moorhen (CM) coronavirus HKU21. Mu, munia; ChMu, chestnut munia; GbTh, gray-backed thrush; ShBu, sooty-headed bulbul; RwBu, red-whiskered bulbul; ChBu, chestnut bulbul.
Fig 2
Fig 2
Genome organization of members in Deltacoronavirus. ORFs downstream of S gene are magnified to show the differences among the genomes of the 10 CoVs. Papain-like protease (PLpro), chymotrypsin-like protease (3CLpro), and RNA-dependent RNA polymerase (RdRp) are represented by orange boxes. Spike (S), envelope (E), membrane (M), and nucleocapsid (N) are represented by green boxes. Putative accessory proteins are represented by blue boxes. The seven CoVs discovered in this study are shown in bold.
Fig 3
Fig 3
Multiple alignments of conserved s2m of infectious bronchitis virus (IBV), SARS-related human coronavirus (SARS CoV), SARS-related Rhinolophus bat coronavirus HKU3 (SARSr-Rh-BatCoV HKU3), BuCoV HKU11, ThCoV HKU12, MunCoV HKU13, Asian leopard cat coronavirus (ALCCoV), PorCoV HKU15, WECoV HKU16, SpCoV HKU17, MRCoV HKU18, and CMCoV HKU21. Identical nucleotides are marked by asterisks. Acc. No., accession no.
Fig 4
Fig 4
Phylogenetic analyses of 3CLpro, RdRp, helicase (Hel), S, and N proteins of PorCoV HKU15, WECoV HKU16, SpCoV HKU17, MRCoV HKU18, NHCoV HKU19, WiCoV HKU20, and CMCoV HKU21. The trees were constructed by using the neighbor joining method using Kimura correction and bootstrap values calculated from 1,000 trees. Two hundred ninety-five, 892, 590, 802, and 249 amino acid positions in 3CLpro, RdRp, Hel, S, and N, respectively, were included in the analyses. The trees were midpoint rooted. For 3CLpro and S, the scale bar indicates the estimated number of substitutions per 10 amino acids. For RdRp and Hel, the scale bar indicates the estimated number of substitutions per 20 amino acids. For N, the scale bar indicates the estimated number of substitutions per 5 amino acids. Viruses characterized in this study are in bold. Virus name abbreviations are the same as those in the Fig. 1 legend.
Fig 4
Fig 4
Phylogenetic analyses of 3CLpro, RdRp, helicase (Hel), S, and N proteins of PorCoV HKU15, WECoV HKU16, SpCoV HKU17, MRCoV HKU18, NHCoV HKU19, WiCoV HKU20, and CMCoV HKU21. The trees were constructed by using the neighbor joining method using Kimura correction and bootstrap values calculated from 1,000 trees. Two hundred ninety-five, 892, 590, 802, and 249 amino acid positions in 3CLpro, RdRp, Hel, S, and N, respectively, were included in the analyses. The trees were midpoint rooted. For 3CLpro and S, the scale bar indicates the estimated number of substitutions per 10 amino acids. For RdRp and Hel, the scale bar indicates the estimated number of substitutions per 20 amino acids. For N, the scale bar indicates the estimated number of substitutions per 5 amino acids. Viruses characterized in this study are in bold. Virus name abbreviations are the same as those in the Fig. 1 legend.
Fig 4
Fig 4
Phylogenetic analyses of 3CLpro, RdRp, helicase (Hel), S, and N proteins of PorCoV HKU15, WECoV HKU16, SpCoV HKU17, MRCoV HKU18, NHCoV HKU19, WiCoV HKU20, and CMCoV HKU21. The trees were constructed by using the neighbor joining method using Kimura correction and bootstrap values calculated from 1,000 trees. Two hundred ninety-five, 892, 590, 802, and 249 amino acid positions in 3CLpro, RdRp, Hel, S, and N, respectively, were included in the analyses. The trees were midpoint rooted. For 3CLpro and S, the scale bar indicates the estimated number of substitutions per 10 amino acids. For RdRp and Hel, the scale bar indicates the estimated number of substitutions per 20 amino acids. For N, the scale bar indicates the estimated number of substitutions per 5 amino acids. Viruses characterized in this study are in bold. Virus name abbreviations are the same as those in the Fig. 1 legend.
Fig 5
Fig 5
Estimation of the time to the most recent common ancestor for Alphacoronavirus, Betacoronavirus, Gammacoronavirus, and Deltacoronavirus. The time-scaled phylogeny was summarized from all MCMC phylogenies of the RdRp gene data set analyzed under the relaxed-clock model with an uncorrelated log-normal distribution in BEAST version 1.6.1. Viruses characterized in this study are in bold. The numbers indicate number of years ago. This is shown in the scale bar. Virus name abbreviations are the same as those in the legends of Fig. 1.
Fig 6
Fig 6
A model of CoV evolution. CoVs in bats are the gene source of Alphacoronavirus and Betacoronavirus, and CoVs in birds are the gene source of Gammacoronavirus and Deltacoronavirus.
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