Genomic epidemiology, evolution, and transmission dynamics of porcine deltacoronavirus

ABSTRACT

The emergence of severe acute respiratory syndrome virus (SARS)-CoV-2 has shown once again that coronaviruses (CoVs) in animals are potential sources for epidemics in humans. Porcine deltacoronavirus (PDCoV) is an emerging enteropathogen of swine with a worldwide distribution. Here, we implemented and described an approach to analyze the epidemiology of PDCoV following its emergence in the pig population. We performed an integrated analysis of full genome sequence data from 21 newly-sequenced viruses, along with comprehensive epidemiological surveillance data collected globally over the last 15 years. We found four distinct phylogenetic lineages of PDCoV, which differ in their geographic circulation patterns. Interestingly, we identified more frequent intra- and inter-lineage recombination and higher virus genetic diversity in the Chinese lineages compared with the US lineage where pigs are raised in different farming systems and ecological environments. Most recombination breakpoints are located in the ORF1ab gene rather than in genes encoding structural proteins. We also identified five amino acids under positive selection in the spike protein suggesting a role for adaptive evolution. According to structural mapping, three positively selected sites are located in the N-terminal domain of the S1 subunit, which is the most likely involved in binding to a carbohydrate receptor, while the other two are located in or near the fusion peptide of the S2 subunit and thus might affect membrane fusion. Finally, our phylogeographic investigations highlighted notable South-North transmission as well as frequent long-distance dispersal events in China that could implicate human-mediated transmission. Our findings provide new insights into the evolution and dispersal of PDCoV that contribute to our understanding of the critical factors involved in coronaviruses emergence. Significance Coronaviruses (CoVs) exhibit a pronounced propensity for interspecies transmission as illustrated by important emerging viruses in humans such as severe acute respiratory syndrome virus (SARS)-CoV and Middle East respiratory syndrome virus (MERS)-CoV, as well as the recent SARS-CoV-2 that is causing a major human pandemic. A better understanding of the evolutionary process leading to viral emergence may help unravel the principles of cross-species transmission and therefore assist in preventing future introductions into new host populations. Here, we examined the evolution and spread of an emerging coronavirus that likely transmitted from birds to pigs and caused sustained epidemics in Asia and the United States. We integrated viral full genome sequence analysis and comprehensive surveillance data to examine the evolution of emerging porcine deltacoronavirus (PDCoV), and in particular the factors driving ongoing circulation and recent cases in China. We found evidence for adaptive evolution of this emerging virus in the absence of vaccine immune pressure, with important amino acids under positive selection, as well as frequent inter- and intra-lineage recombination events in the Asian lineages. Breeding patterns and ecological environment could play an important role in swine coronavirus evolution, leading to differences in recombination and population diversity. Using phylogeographic approaches, we further shed light on the dispersal history and dynamics of the China lineage of PDCoV. Our study provides a deeper understanding of the geographic dispersal of genetic lineages of PDCoV in China and suggests that southern China acted as a source of transmission. Modeling how the virus spread in China will allow the prioritization of areas for swine coronavirus surveillance in the future. These findings have important implications for preventing the emergence of coronaviruses in livestock and for controlling their spread in Asian countries.