Genomic Epidemiology, Evolution, and Transmission Dynamics of Porcine Deltacoronavirus

Author:

He Wan-Ting1,Ji Xiang234ORCID,He Wei1,Dellicour Simon56,Wang Shilei1,Li Gairu1,Zhang Letian1,Gilbert Marius6,Zhu Henan34,Xing Gang7,Veit Michael8,Huang Zhen9,Han Guan-Zhu10,Huang Yaowei7,Suchard Marc A34,Baele Guy5,Lemey Philippe5,Su Shuo1

Affiliation:

1. MOE International Joint Collaborative Research Laboratory for Animal Health & Food Safety, Jiangsu Engineering Laboratory of Animal Immunology, Institute of Immunology, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, China

2. Department of Mathematics, Tulane University, New Orleans, LA

3. Departments of Biomathematics and Human Genetics, David Geffen School of Medicine at UCLA, University of California, Los Angeles, Los Angeles, CA

4. Department of Biostatistics, UCLA Fielding School of Public Health, University of California, Los Angeles, Los Angeles, CA

5. Department of Microbiology, Immunology and Transplantation, Rega Institute, Laboratory for Clinical and Epidemiological Virology, KU Leuven, Leuven, Belgium

6. Spatial Epidemiology Lab (SpELL), Université Libre de Bruxelles, Bruxelles, Belgium

7. Key Laboratory of Animal Virology of Ministry of Agriculture, Zhejiang University, Hangzhou, China

8. Institute for Virology, Center for Infection Medicine, Veterinary Faculty, Free University Berlin, Berlin, Germany

9. Zhengzhou New Channel Agricultural Technology Co., Ltd, Zhengzhou, Henan, China

10. Jiangsu Key Laboratory for Microbes and Functional Genomics, College of Life Sciences, Nanjing Normal University, Nanjing, Jiangsu, China

Abstract

Abstract The emergence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has shown once again that coronavirus (CoV) 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 interlineage recombination and higher virus genetic diversity in the Chinese lineages compared with the USA 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, whereas 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 CoVs emergence.

Funder

National Natural Science Foundation of Outstanding Youth Fund in China

National Key Research and Development Program of China

The Young Top-Notch Talents of National Ten Thousand Talent Program

Fundamental Research Funds for the Central Universities

Six Talent Peaks Project of Jiangsu Province of China

Fonds National de la Recherche Scientifique

FRS-FNRS

National Institutes of Health

Interne Fondsen KU Leuven

Internal Funds KU Leuven

Research Foundation—Flanders

European Research Council under the European Union’s Horizon 2020 research and innovation program

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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