Viral Metagenome-Based Precision Surveillance of Pig Population at Large Scale Reveals Viromic Signatures of Sample Types and Influence of Farming Management on Pig Virome

Pigs are a major meat source worldwide and a pillar of Chinese animal husbandry; hence, their health and safety are a prioritized concern of the national economy. Although pig viruses have been continuously investigated, the full extent of the pig virome has remained unknown and emerging viruses are still a major threat to the pig industry. Here, we report a comprehensive study to delineate the pig virome of 1,841 healthy weaned pigs from 45 commercial farms collected from 25 major pig-producing regions across China. A viromic sequence data set, named Pigs_VIRES, which matched 96,586 viral genes from at least 249 genera within 66 families and which almost tripled the number of previously published pig viromic genes, was established. The majority of the mammalian viruses were closely related to currently known ones. A comparison with previously published viromes of bovines, avians, and humans has revealed the distinct composition of Pigs_VIRES, which has provided characteristic viromic signatures of serum, pharyngeal, and anal samples that were significantly influenced by farming management and disease control measures. Taken together, Pigs_VIRES has revealed the most complete viromic data set of healthy pigs to date. The compiled data also provide useful guidance to pig viral disease control and prevention and the biosafety management of pig farms. Especially, the established viromic protocol has created a precision surveillance strategy to potentially innovate currently used surveillance methods of animal infectious diseases, particularly by making precision surveillance available to other animal species on a large scale or even during a nationwide surveillance campaign. IMPORTANCE Pigs are deeply involved in human lives; hence, their viruses are associated with public health. Here, we established the most comprehensive virome of healthy piglets to date, which provides a viromic baseline of weaned pigs for disease prevention and control, highlighting that longitudinal viromic monitoring is needed to better understand the dynamics of the virome in pig development and disease occurrence. The present study also shows how high standards of animal farm management with strict biosafety measures can significantly minimize the risk of introduction of pathogenic viruses into pig farms. Particularly, the viromic strategy established, i.e., high-throughput detection and analyses of various known and unknown pathogenic viruses in a single test at large scale, has completely innovated current surveillance measures in provision of timely and precise detection of all potentially existing pathogenic viruses and can be widely applied in other animal species.