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. 2018 Jul 17;92(15):e00265-18.
doi: 10.1128/JVI.00265-18. Print 2018 Aug 1.

Discovery and Sequence Analysis of Four Deltacoronaviruses from Birds in the Middle East Reveal Interspecies Jumping with Recombination as a Potential Mechanism for Avian-to-Avian and Avian-to-Mammalian Transmission

Susanna K P Lau  1   2   3   4   5 , Emily Y M Wong  1 , Chi-Ching Tsang  1 , Syed Shakeel Ahmed  1 , Rex K H Au-Yeung  6 , Kwok-Yung Yuen  1   2   3   4   5 , Ulrich Wernery  7 , Patrick C Y Woo  8   2   3   4   5
Affiliations

Discovery and Sequence Analysis of Four Deltacoronaviruses from Birds in the Middle East Reveal Interspecies Jumping with Recombination as a Potential Mechanism for Avian-to-Avian and Avian-to-Mammalian Transmission

Susanna K P Lau et al. J Virol. .

Abstract

The emergence of Middle East respiratory syndrome showed once again that coronaviruses (CoVs) in animals are potential source for epidemics in humans. To explore the diversity of deltacoronaviruses in animals in the Middle East, we tested fecal samples from 1,356 mammals and birds in Dubai, The United Arab Emirates. Four novel deltacoronaviruses were detected from eight birds of four species by reverse transcription-PCR (RT-PCR): FalCoV UAE-HKU27 from a falcon, HouCoV UAE-HKU28 from a houbara bustard, PiCoV UAE-HKU29 from a pigeon, and QuaCoV UAE-HKU30 from five quails. Complete genome sequencing showed that FalCoV UAE-HKU27, HouCoV UAE-HKU28, and PiCoV UAE-HKU29 belong to the same CoV species, suggesting recent interspecies transmission between falcons and their prey, houbara bustards and pigeons, possibly along the food chain. Western blotting detected specific anti-FalCoV UAE-HKU27 antibodies in 33 (75%) of 44 falcon serum samples, supporting genuine infection in falcons after virus acquisition. QuaCoV UAE-HKU30 belongs to the same CoV species as porcine coronavirus HKU15 (PorCoV HKU15) and sparrow coronavirus HKU17 (SpCoV HKU17), discovered previously from swine and tree sparrows, respectively, supporting avian-to-swine transmission. Recombination involving the spike protein is common among deltacoronaviruses, which may facilitate cross-species transmission. FalCoV UAE-HKU27, HouCoV UAE-HKU28, and PiCoV UAE-HKU29 originated from recombination between white-eye coronavirus HKU16 (WECoV HKU16) and magpie robin coronavirus HKU18 (MRCoV HKU18), QuaCoV UAE-HKU30 from recombination between PorCoV HKU15/SpCoV HKU17 and munia coronavirus HKU13 (MunCoV HKU13), and PorCoV HKU15 from recombination between SpCoV HKU17 and bulbul coronavirus HKU11 (BuCoV HKU11). Birds in the Middle East are hosts for diverse deltacoronaviruses with potential for interspecies transmission.IMPORTANCE During an attempt to explore the diversity of deltacoronaviruses among mammals and birds in Dubai, four novel deltacoronaviruses were detected in fecal samples from eight birds of four different species: FalCoV UAE-HKU27 from a falcon, HouCoV UAE-HKU28 from a houbara bustard, PiCoV UAE-HKU29 from a pigeon, and QuaCoV UAE-HKU30 from five quails. Genome analysis revealed evidence of recent interspecies transmission between falcons and their prey, houbara bustards and pigeons, possibly along the food chain, as well as avian-to-swine transmission. Recombination, which is known to occur frequently in some coronaviruses, was also common among these deltacoronaviruses and occurred predominantly at the spike region. Such recombination, involving the receptor binding protein, may contribute to the emergence of new viruses capable of infecting new hosts. Birds in the Middle East are hosts for diverse deltacoronaviruses with potential for interspecies transmission.

Keywords: Middle East; coronavirus; deltacoronavirus; falcon; houbara bustard; interspecies jumping; pigeon; quail.

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Figures

FIG 1
FIG 1
Phylogenetic analysis of amino acid sequences of the 371-bp fragments (excluding primer sequences) of RNA-dependent RNA polymerases (RdRps) of coronaviruses (CoVs) identified from birds from Dubai in the present study. The tree was reconstructed by the maximum-likelihood method using PhyML 3.0 with the substitution model general time reversible with gamma distributed rate variation and estimated proportion of invariable sites (GTR+G+I). Bootstrap values were calculated from 1,000 trees. The scale bar indicates the number of nucleotide substitutions per site. The eight newly identified coronaviruses are shown in bold. The viruses and their respective DDBJ/ENA/GenBank accession numbers are as follow: ALCCoV, Asian leopard cat coronavirus (EF584908); Badger SARS-CoV, SARS-related Chinese ferret badger CoV (AY545919); BCoV, bovine CoV (NC_003045); BdCoV HKU22, bottlenose dolphin CoV HKU22 (KF793826); BuCoV HKU11, bulbul CoV HKU11 (FJ376619); BWCoV SW1, Beluga whale CoV SW1 (NC_010646); Camel MERS-CoV, camel Middle East respiratory syndrome CoV (KT751244); ChRCoV HKU24, China Rattus CoV HKU24 (KM349742); Civet SARS-CoV, SARS-related palm civet CoV (AY304488); CMCoV HKU21, common-moorhen CoV HKU21 (NC_016996); DcCoV HKU23, dromedary camel CoV HKU23 (KF906251); FalCoV UAE-HKU27, falcon CoV UAE-HKU27; FIPV, feline infectious peritonitis virus (AY994055); GiCoV, giraffe CoV (EF424622); HouCoV UAE-HKU28, houbara CoV UAE-HKU28; HCoV 229E, human CoV 229E (NC_002645); HCoV HKU1, human CoV HKU1 (NC_006577); HCoV NL63, human CoV NL63 (NC_005831); HCoV OC43, human CoV OC43 (NC_005147); Human MERS-CoV, human Middle East respiratory syndrome CoV (JX869059); Human SARS-CoV, severe acute respiratory syndrome-related human CoV (NC_004718); IBV, infectious bronchitis virus (NC_001451); IBV-partridge, partridge coronavirus (AY646283); IBV-peafowl, peafowl coronavirus (AY641576); MHV, murine hepatitis virus (NC_001846); MRCoV HKU18, magpie robin CoV HKU18 (NC_016993); MunCoV HKU13, munia CoV HKU13 (FJ376622); NHCoV HKU19, night-heron CoV HKU19 (NC_016994); PEDV, porcine epidemic diarrhea virus (NC_003436); PHEV, porcine hemagglutinating encephalomyelitis virus (NC_007732); PiCoV UAE-HKU29, pigeon CoV UAE-HKU29; Pi-BatCoV HKU5, Pipistrellus bat CoV HKU5 (NC_009020); PorCoV HKU15, porcine CoV HKU15 (NC_016990); PRCV, porcine respiratory CoV (DQ811787); QuaCoV UAE-HKU30, quail CoV UAE-HKU30; RbCoV HKU14, rabbit CoV HKU14 (JN874559); Rh-BatCoV HKU2, Rhinolophus bat CoV HKU2 (EF203064); Ro-BatCoV HKU9, Rousettus bat CoV HKU9 (NC_009021); SACoV, sable antelope CoV (EF424621); SARSr-Rs-BatCoV HKU3, SARS-related Rhinolophus bat CoV HKU3 (DQ022305); Sc-BatCoV 512, Scotophilus bat CoV 512 (NC_009657); SpCoV HKU17, sparrow CoV HKU17 (NC_016992); TGEV, transmissible gastroenteritis virus (AJ271965); ThCoV HKU12, thrush CoV HKU12 (FJ376621); Ty-BatCoV HKU4, Tylonycteris bat CoV HKU4 (NC_009019); WECoV HKU16, white-eye CoV HKU16 (NC_016991); WiCoV HKU20, wigeon CoV HKU20 (NC_016995).
FIG 2
FIG 2
Genome organization of members of Deltacoronavirus. Open reading frames downstream of spike (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) genes are represented by green boxes. S, envelope (E), membrane (M), and nucleocapsid (N) genes are represented by orange boxes. Putative accessory proteins are represented by blue boxes. The novel coronaviruses discovered in this study are shown in bold. Abbreviations for the viruses are the same as those in Fig. 1.
FIG 3
FIG 3
Phylogenetic analyses of chymotrypsin-like protease (3CLpro), RNA-dependent RNA polymerase (RdRp), helicase (Hel), spike (S) protein, and nucleocapsid (N) protein of falcon CoV-HKU27, houbara CoV-HKU28, pigeon CoV-HKU29, and quail CoV-HKU30. The trees were reconstructed by the maximum-likelihood method using PhyML 3.0 with the following substitution models: Le and Gascuel (LG) with gamma distributed rate variation (G) (3CLpro); LG with G, estimated proportion of invariable sites (I), and empirical frequencies (F) (RdRp); LG+G+F (Hel and N); and Whelan and Goldman (WAG)+G+I+F (S). Bootstrap values were calculated from 1,000 trees, and 314, 944, 599, 1,561, and 392 amino acid positions in 3CLpro, RdRp, Hel, S, and N, respectively, were included in the analyses. The scale bars indicate the number of amino acid substitutions per site. Viruses characterized in this study are in bold. Abbreviations for the viruses are the same as those in Fig. 1.
FIG 4
FIG 4
Detection of possible recombination by bootscan analysis. Bootscanning was conducted with Simplot version 3.5.1 (F84 model; window size, 1,000 bp; step, 200 bp). (A) Falcon CoV UAE-HKU27 (FalCoV UAE-HKU27) was used as the query sequence and compared with the genome sequences of white-eye coronavirus HKU16 (WECoV HKU16), magpie robin coronavirus HKU18 (MRCoV HKU18), and ThCoV HKU12 thrush coronavirus HKU12 (ThCoV HKU12). (B) Quail CoV UAE-HKU30 (QuaCoV UAE-HKU30) was used as the query sequence and compared with the genome sequences of sparrow coronavirus HKU17 (SpCoV HKU17), munia coronavirus HKU13 (MunCoV HKU13), and ThCoV HKU12.
FIG 5
FIG 5
Estimation of the mean time to the most recent common ancestor (tMRCA) for Deltacoronavirus. The time-scaled phylogeny was summarized from all Markov chain Monte Carlo (MCMC) phylogenies of the RNA-dependent RNA polymerase (RdRp) gene data set analyzed under the relaxed-clock model with an uncorrelated log-normal distribution in BEAST version 1.7.4. Viruses characterized in this study are in bold. Abbreviations for the viruses are the same as those in Fig. 1.
FIG 6
FIG 6
Western blot analysis of falcon CoV UAE-HKU27 (FalCoV UAE-HKU27) using nucleocapsid (N) protein expressed in Escherichia coli. Lane 1, positive control; lane 2, falcon serum sample (FS7) strongly positive for antibodies against FalCoV UAE-HKU27 N protein; lane 3: falcon serum sample (FS5) negative for antibodies against FalCoV UAE-HKU27 N protein.
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