Bat coronaviruses: diversity, evolution and interspecies transmission

Abstract

Coronaviruses (CoVs) are traditionally classified into groups 1, 2 and 3, which are now replaced by the three genera, Alphacoronavirus, Betacoronavirus and Gammacoronavirus, with the addition of a new genus, Deltacoronavirus. The existence of CoVs in bats was unknown until the SARS epidemic which has boosted the search for the animal origin of SARS-CoV (Betacoronavirus lineage B). While civet was found to be an immediate ancestor of SARS-CoV soon after the 2003 epidemic, horseshoe bats were only identified as the natural reservoir of SARS-related batCoVs in 2005. Such findings have awakened the world on the role of bats as an important reservoir for CoVs. Since then, a large diversity of novel bat CoVs have been identified, including viruses belonging to two novel subgroups, Betacoronavirus lineages C and D. Phylogenetic analysis suggested that bats and birds are the two major hosts for the gene source for Alphacoronavirus/Betacoronavirus and Gammacoronvirus/Deltacoronavirus respectively, which can fuel CoV evolution and dissemination. While our understanding on bat CoVs was only beginning to unwind, another novel CoV, MERS-CoV (Betacoronavirus lineage C), has emerged in the Middle East since 2012, having affected >600 people with >200 deaths so far. Although camels have recently been identified as the direct animal origin of MERS-CoV, the virus is also closely related to lineage C betaCoVs including batCoV HKU4 and HKU5 previously discovered in lesser bamboo bat and Japanese pipistrelle, respectively. Despite our expanded knowledge on bat CoVs, their evolution and interspecies transmission are still poorly understood. For SARSrelated batCoVs, horseshoe bats, as the primary reservoir, can fuel recombination, and civet SARS-CoV is likely a recombinant virus arisen from horseshoe bats of different geographical locations. For MERS-CoV, it remains unknown if Pipistrellus bats are the natural reservoir of its ancestor viruses, similar to the situation in SARS-CoV. For Betacoronavirus lineage D, different genotypes of Rousettus batCoV HKU9 have been identified in the same bat individual. Moreover, recombination events were detected between strains from different bat individuals, which may facilitate viral evolution to generate different genotypes. As for Alphacoronavirus, evidence for recent interspecies transmission of batCoV HKU10 has been identified between bats of different suborders, from Leschenault's rousettes to pomona leaf-nosed bats. More studies are eagerly awaited to unravel the evolutionary mechanisms governing the interspecies transmission of batCoVs, and hence their potential for emergence.