Regional antimicrobial resistance gene flow among the One Health sectors in China
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 antimic...
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BMC
2025-01-01
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| Series: | Microbiome |
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| Online Access: | https://doi.org/10.1186/s40168-024-01983-x |
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| author | 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 |
| author_facet | 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 |
| author_sort | Yuqing Feng |
| collection | DOAJ |
| description | 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 |
| format | Article |
| id | doaj-art-ce89b3eba1ba4fbb9da959ddce0e05b0 |
| institution | Kabale University |
| issn | 2049-2618 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | Microbiome |
| spelling | doaj-art-ce89b3eba1ba4fbb9da959ddce0e05b02025-01-12T12:32:21ZengBMCMicrobiome2049-26182025-01-0113111810.1186/s40168-024-01983-xRegional antimicrobial resistance gene flow among the One Health sectors in ChinaYuqing Feng0Xin Lu1Jiayong Zhao2Hongmin Li3Jialiang Xu4Zhenpeng Li5Mengyu Wang6Yao Peng7Tian Tian8Gailing Yuan9Yuan Zhang10Jiaqi Liu11Meihong Zhang12A La Teng Zhu La13Geruo Qu14Yujiao Mu15Wanshen Guo16Yongning Wu17Yuyu Zhang18Dexiang Wang19Yongfei Hu20Biao Kan21State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and PreventionInstitute of Infectious Disease Prevention and Control, Henan Center for Disease Control and PreventionDengfeng Center for Disease Control and PreventionSchool of Light Industry Science and Engineering, Beijing Technology and Business UniversityNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and PreventionNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and PreventionNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and PreventionDengfeng Center for Disease Control and PreventionDengfeng Center for Disease Control and PreventionNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and PreventionNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and PreventionState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and PreventionInstitute of Infectious Disease Prevention and Control, Henan Center for Disease Control and PreventionInstitute of Infectious Disease Prevention and Control, Henan Center for Disease Control and PreventionNHC Key Laboratory of Food Safety Risk Assessment, China National Center for Food Safety Risk AssessmentSchool of Light Industry Science and Engineering, Beijing Technology and Business UniversityDengfeng Center for Disease Control and PreventionState Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural UniversityNational Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute for Communicable Disease Control and Prevention, Chinese Center for Disease Control and PreventionAbstract 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 Abstracthttps://doi.org/10.1186/s40168-024-01983-xOne HealthAntimicrobial resistance geneMobile genetic elementTransmission pathwayCarbapenemase |
| spellingShingle | 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 Regional antimicrobial resistance gene flow among the One Health sectors in China Microbiome One Health Antimicrobial resistance gene Mobile genetic element Transmission pathway Carbapenemase |
| title | Regional antimicrobial resistance gene flow among the One Health sectors in China |
| title_full | Regional antimicrobial resistance gene flow among the One Health sectors in China |
| title_fullStr | Regional antimicrobial resistance gene flow among the One Health sectors in China |
| title_full_unstemmed | Regional antimicrobial resistance gene flow among the One Health sectors in China |
| title_short | Regional antimicrobial resistance gene flow among the One Health sectors in China |
| title_sort | regional antimicrobial resistance gene flow among the one health sectors in china |
| topic | One Health Antimicrobial resistance gene Mobile genetic element Transmission pathway Carbapenemase |
| url | https://doi.org/10.1186/s40168-024-01983-x |
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