Regional antimicrobial resistance gene flow among the One Health sectors in China
Yuqing Feng,
Xin Lu,
Jiayong Zhao,
Hongmin Li,
Jialiang Xu,
Zhenpeng Li,
Mengyu Wang,
Yao Peng,
Tian Tian,
Gailing Yuan,
Yuan Zhang,
Jiaqi Liu,
Meihong Zhang,
A La Teng Zhu La,
Geruo Qu,
Yujiao Mu,
Wanshen Guo,
Yongning Wu,
Yuyu Zhang,
Dexiang Wang,
Yongfei Hu,
Biao Kan
Affiliations
Yuqing Feng
State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural University
Xin Lu
National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention
Jiayong Zhao
Institute of Infectious Disease Prevention and Control, Henan Center for Disease Control and Prevention
Hongmin Li
Dengfeng Center for Disease Control and Prevention
Jialiang Xu
School of Light Industry Science and Engineering, Beijing Technology and Business University
Zhenpeng Li
National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention
Mengyu Wang
National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention
Yao Peng
National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention
Tian Tian
Dengfeng Center for Disease Control and Prevention
Gailing Yuan
Dengfeng Center for Disease Control and Prevention
Yuan Zhang
National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention
Jiaqi Liu
National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention
Meihong Zhang
State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural University
A La Teng Zhu La
State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural University
Geruo Qu
National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention
Yujiao Mu
Institute of Infectious Disease Prevention and Control, Henan Center for Disease Control and Prevention
Wanshen Guo
Institute of Infectious Disease Prevention and Control, Henan Center for Disease Control and Prevention
Yongning Wu
NHC Key Laboratory of Food Safety Risk Assessment, China National Center for Food Safety Risk Assessment
Yuyu Zhang
School of Light Industry Science and Engineering, Beijing Technology and Business University
Dexiang Wang
Dengfeng Center for Disease Control and Prevention
Yongfei Hu
State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural University
Biao Kan
National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and Prevention
Abstract Background Antimicrobial resistance poses a significant threat to global health, with its spread intricately linked across human, animal, and environmental sectors. Revealing the antimicrobial resistance gene (ARG) flow among the One Health sectors is essential for better control of antimicrobial resistance. Results In this study, we investigated regional ARG transmission among humans, food, and the environment in Dengfeng, Henan Province, China by combining large-scale metagenomic sequencing with culturing of resistant bacterial isolates in 592 samples. A total of 40 ARG types and 743 ARG subtypes were identified, with a predominance of multidrug resistance genes. Compared with microbes from human fecal samples, those from food and environmental samples showed a significantly higher load of ARGs. We revealed that dietary habits and occupational exposure significantly affect ARG abundance. Pseudomonadota, particularly Enterobacteriaceae, were identified as the main ARG carriers shaping the resistome. The resistome in food samples was found more affected by mobile genetic elements (MGEs), whereas in environmental samples, it was more associated with the microbial composition. We evidenced that horizontal gene transfer (HGT) mediated by plasmids and phages, together with strain transmission, particularly those associated with the Enterobacteriaceae members, drive regional ARG flow. Lifestyle, dietary habits, and occupational exposure are all correlated with ARG dissemination and flies and food are important potential sources of ARGs to humans. The widespread mobile carbapenemase gene, OXA-347, carried by non-Enterobacteriaceae bacteria in the human gut microbiota, requires particular attention. Finally, we showed that machine learning models based on microbiome profiles were effective in predicting the presence of carbapenem-resistant strains, suggesting a valuable approach for AMR surveillance. Conclusions Our study provides a full picture of regional ARG transmission among the One Health sectors in a county-level city in China, which facilitates a better understanding of the complex routes of ARG transmission and highlights new points of focus for AMR surveillance and control. Video Abstract
