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. 2012 Nov;86(21):11906-18.
doi: 10.1128/JVI.01305-12. Epub 2012 Aug 29.

Recent transmission of a novel alphacoronavirus, bat coronavirus HKU10, from Leschenault's rousettes to pomona leaf-nosed bats: first evidence of interspecies transmission of coronavirus between bats of different suborders

Susanna K P Lau  1 , Kenneth S M Li, Alan K L Tsang, Chung-Tong Shek, Ming Wang, Garnet K Y Choi, Rongtong Guo, Beatrice H L Wong, Rosana W S Poon, Carol S F Lam, Sylvia Y H Wang, Rachel Y Y Fan, Kwok-Hung Chan, Bo-Jian Zheng, Patrick C Y Woo, Kwok-Yung Yuen
Affiliations

Recent transmission of a novel alphacoronavirus, bat coronavirus HKU10, from Leschenault's rousettes to pomona leaf-nosed bats: first evidence of interspecies transmission of coronavirus between bats of different suborders

Susanna K P Lau et al. J Virol. 2012 Nov.

Abstract

Although coronaviruses are known to infect various animals by adapting to new hosts, interspecies transmission events are still poorly understood. During a surveillance study from 2005 to 2010, a novel alphacoronavirus, BatCoV HKU10, was detected in two very different bat species, Ro-BatCoV HKU10 in Leschenault's rousettes (Rousettus leschenaulti) (fruit bats in the suborder Megachiroptera) in Guangdong and Hi-BatCoV HKU10 in Pomona leaf-nosed bats (Hipposideros pomona) (insectivorous bats in the suborder Microchiroptera) in Hong Kong. Although infected bats appeared to be healthy, Pomona leaf-nosed bats carrying Hi-BatCoV HKU10 had lower body weights than uninfected bats. To investigate possible interspecies transmission between the two bat species, the complete genomes of two Ro-BatCoV HKU10 and six Hi-BatCoV HKU10 strains were sequenced. Genome and phylogenetic analyses showed that Ro-BatCoV HKU10 and Hi-BatCoV HKU10 represented a novel alphacoronavirus species, sharing highly similar genomes except in the genes encoding spike proteins, which had only 60.5% amino acid identities. Evolution of the spike protein was also rapid in Hi-BatCoV HKU10 strains from 2005 to 2006 but stabilized thereafter. Molecular-clock analysis dated the most recent common ancestor of all BatCoV HKU10 strains to 1959 (highest posterior density regions at 95% [HPDs], 1886 to 2002) and that of Hi-BatCoV HKU10 to 1986 (HPDs, 1956 to 2004). The data suggested recent interspecies transmission from Leschenault's rousettes to Pomona leaf-nosed bats in southern China. Notably, the rapid adaptive genetic change in BatCoV HKU10 spike protein by ~40% amino acid divergence after recent interspecies transmission was even greater than the ~20% amino acid divergence between spike proteins of severe acute respiratory syndrome-related Rhinolophus bat coronavirus (SARSr-CoV) in bats and civets. This study provided the first evidence for interspecies transmission of coronavirus between bats of different suborders.

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Figures

Fig 1
Fig 1
Genome organizations of Ro-BatCoV HKU10, Hi-BatCoV HKU10, and representative CoVs from each group. Genes for papain-like proteases (PL1pro, PL2pro, and PLpro), 3C-like protease (3CLpro), and RNA-dependent RNA polymerase (RdRp) are represented by orange boxes. Genes for hemagglutinin esterase (HE), spike protein (S), envelope protein (E), membrane protein (M), and nucleocapsid protein (N) are represented by green boxes. Genes for putative accessory proteins are represented by blue boxes. BatCoV HKU10 strains detected in this study are shown in bold.
Fig 2
Fig 2
Phylogenetic analysis of RdRp, Hel, S, and N of Hi-BatCoV HKU10 and Ro-BatCoV HKU10. The trees were constructed by the maximum-likelihood method with bootstrap values calculated from 100 trees. A total of 951, 609, 1,899 and 572 amino acid positions in RdRp, Hel, S, and N, respectively, were included in the analysis. The scale bars indicate the estimated number of substitutions per 5 or 10 aa. HCoV 229E, human coronavirus 229E; PEDV, porcine epidemic diarrhea virus; TGEV, porcine transmissible gastroenteritis virus; FIPV, feline infectious peritonitis virus; PRCV, porcine respiratory coronavirus; HCoV NL63, human coronavirus NL63; Rh-BatCoV HKU2, Rhinolophus bat coronavirus HKU2; Mi-BatCoV 1A, Miniopterus bat coronavirus 1A; Mi-BatCoV 1B, Miniopterus bat coronavirus 1B; Mi-BatCoV HKU8, Miniopterus bat coronavirus HKU8; Sc-BatCoV 512, Scotophilus bat coronavirus 512; HCoV HKU1, human coronavirus HKU1, HCoV OC43, human coronavirus OC43; MHV, murine hepatitis virus; BCoV, bovine coronavirus; PHEV, porcine hemagglutinating encephalomyelitis virus; GiCoV, giraffe coronavirus; SARS-CoV, SARS coronavirus; SARSr-Rh-BatCoV HKU3, SARS-related Rhinolophus bat coronavirus HKU3; Ty-BatCoV HKU4, Tylonycteris bat coronavirus HKU4; Pi-BatCoV HKU5, Pipistrellus bat coronavirus HKU5; Ro-BatCoV HKU9, Rousettus bat coronavirus HKU9; IBV, infectious bronchitis virus; BWCoV SW1, beluga whale coronavirus SW1; BuCoV HKU11, bulbul coronavirus HKU11; ThCoV HKU12, thrush coronavirus HKU12; MunCoV HKU13, munia coronavirus HKU13; PorCoV HKU15, porcine coronavirus HKU15.
Fig 3
Fig 3
Selection pressure analysis of the S genes of BatCoV HKU10. (A) Detection of lineage-specific selection pressure. The branch with a P value of <0.01 is highlighted. ω+, strength of positive selection; q+, proportion of the total branch length influenced by the selective pressure. The scale bar indicates the estimated number of substitutions per 20 nucleotides. (B) Distribution of positively selected sites in S protein genes identified using REL among Hi-BatCoV HKU10 strains from 2005–2010. The receptor-binding domains (RBD) of the S proteins of TGEV, HCoV NL63, and HCoV 229E were mapped previously (3, 14, 74). Homology modeling of the RBD in the S proteins of Ro-BatCoV HKU10 and Hi-BatCoV HKU10 was performed using SwissModel in automated mode (52). The heptad repeat (HR) regions were predicted by using the coiled-coil prediction program MultiCoil2 (61).
Fig 4
Fig 4
Estimation of the tMRCA of BatCoV HKU10. The time-scaled phylogeny was summarized from all MCMC phylogenies of the RdRp gene data set analyzed under the relaxed-clock model with an exponential distribution (Uced) in BEAST version 1.6.2. Viruses characterized in this study are in bold.
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