Swine manure facilitates the spread of antibiotic resistome including tigecycline-resistant tet(X) variants to farm workers and receiving environment

Abstract

The prevalence of antibiotic resistance genes (ARGs) in livestock and poultry manure is a severe threat to human health. However, the comprehensive characterization of antibiotic resistance in swine, workers, and the receiving environment is still lacking in the actual breeding environment. Hence, the ARG profile and the potential bacterial hosts producing among swine manure (including sows, piglets, finishing pigs, and nursery pigs), worker feces, and the receiving environment (including sediment and vegetable soil) were comprehensively analyzed based on the metagenomic method. The results showed that swine manure exhibited the high levels of richness and diversity of ARGs. Inactivating tetracycline resistance genes such as tet(X), tet(X1), and tet(X10) were prevalent on swine farms. Workers and the environment were the primary recipients of ARGs, and shared ARGs accounted for at least 90% of their ARG abundances. Network analysis revealed that Escherichia, Acinetobacter, and Erysipelothrix were the most dominant genera co-occurring with specific shared ARGs. The abundance of coexisting ARGs in swine at different developmental stages accounted for 76.4% to 90.8% of the shared ARGs in swine, workers, and environmental samples. The Mantel test revealed that Firmicutes and Proteobacteria had a significant correlation with the ARG profiles. In addition, variation partitioning analysis (VPA) showed that the joint effects of mobile genetic elements (MGEs) and bacterial communities accounted for 24.7% of the resistome variation and played a significant role in the ARG profiles. These results improve our understanding of the transmission and persistence of ARGs in the actual breeding environment.