An outbreak of canine coronavirus type 2 in captive snow leopards (Panthera uncia) demonstrates a possible role for felids as mixing vessels for alphacoronaviruses

Coronaviruses are endemic and can cause disease in a wide range of domestic animal and wildlife species. The virus species Alphacoronavirus-1 comprises a set of diverse viruses that are highly recombinogenic, including feline coronavirus type 2 (FCoV-2), which is a recombinant genotype of feline coronavirus type 1 (FCoV-1) and canine coronavirus type 2 (CCoV-2). Co-infection within a host promotes viral recombination; thus, to understand the origin of novel variants, it is crucial to identify hosts that can be infected with multiple alphacoronaviruses. The receptor for FCoV-2 and CCoV-2 is aminopeptidase N (APN), with the APN of the domestic cat (Felis catus) allowing entry of FCoV-2, CCoV-2, and other alphacoronaviruses. As wild felids are genetically closely related to the domestic cat, they may also be susceptible to these alphacoronaviruses. However, to date, natural infection with CCoV-2 has been reported exclusively in canids, not in felids. In this study, we retrospectively investigated a localized outbreak of enteritis in three captive snow leopards (Panthera uncia) at the Bronx Zoo (New York City, U.S.). Whole genome sequencing revealed shedding of CCoV-2 in the feces of the sick leopards. Phylogenetic analyses revealed it is related to highly pathogenic variants of CCoV-2 circulating in the U.S. and Europe. Comparative genetic analyses of the APN gene from five Asian wild felids, including the snow leopard, revealed a high percentage of identity to the APN of the domestic cat (>95.7%). These results emphasize the central role of domestic and wild felids in the emergence of recombinant alphacoronavirus.