Metagenomic insights into correlation of microbiota and antibiotic resistance genes in the worker-pig-soil interface: A One Health surveillance on Chongming Island, China

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• ARGs exhibited high diversity and abundance in soil. • Acidobacteria, Proteobacteria, Firmicutes, Chloroflexota , and Actinobacteria were potential ARGs hosts. • tet(X), tet(X3) , and tet(X6) spanned interfaces of human, pig, and soil. • The correlations between resistance genes for copper, zinc, and lead and various ARGs and mobile genetic elements emphasize the influence of disinfectants and metals on the dissemination of ARGs. Surveillance of antimicrobial resistance (AMR) is necessary and urgent. This study emphasizes the critical role of One Health surveillance in monitoring AMR, integrating metagenomics to assess microbiota and antibiotic resistance genes (ARGs) across human, pig, and soil ecosystems in swine farms. The human and pig gut microbiota are predominantly composed of the phyla Firmicutes, Bacteroidota, Proteobacteria , and Actinobacteria , whereas the soil microbiota exhibits a distinct profile, with Proteobacteria, Acidobacteria, Actinobacteria , and Planctomycetes being the most prevalent. A diverse array of ARGs is identified, including multidrug resistance, with Acidobacteria and Proteobacteria as potential ARG hosts. The study reveals shared ARGs and mobile genetic elements (MGEs) among human, pig, and soil, indicating microbial interdependence and potential for horizontal gene transfer. A positive correlation between biocide and metal resistance genes (BMRGs) and MGEs suggests the role of disinfectants and metals in ARG selection and dissemination. Network analysis of BMRGs, MGEs, and ARGs finds positive associations between copper resistance genes ( corR ), zinc and lead resistance genes ( zraR/hydH, zraS/hydG ), and ARGs such as macB, tetA(58), mlaF , and mtrA . This correlation is also evident with insertion sequences like ISAcba1 and ISArsp9. The findings reveal the potential for horizontal gene transfer and the influence of disinfectants and metals on ARG selection and dissemination, advancing the application of metagenomic monitoring within the One Health framework. This research underscores the need for integrated strategies to mitigate antibiotic resistance and informs sustainable agricultural practices.

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