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Assessing antimicrobial resistance connectivity across One Health sectors

Nature Water volume 3, pages 1100–1113 (2025)Cite this article

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Abstract

The first therapeutic use of antimicrobial agents initiated their endless arms race with antimicrobial resistance (AMR). Although the genes encoding antimicrobial resistance are ancient and ubiquitous in various environmental compartments, including aquatic environments, over eight decades of exposure to selective pressure has changed the way antimicrobial resistance genes (ARGs) emerge and transmit among the three One Health sectors (that is, the intersected sectors of humans, animals and the environment). The dissemination of ARGs has been facilitated by the widespread use of antimicrobials, along with direct and secondary pollution pathways. Current global consensus dictates that AMR should be addressed under a One Health framework. AMR National Action Plans have frequently been formulated. However, the capacity for implementation is not ready in most countries, especially in low- and middle-income regions. This is in part due to the substantial challenges in documenting and controlling cross-sector AMR connectivity. Here we describe the past and current status of AMR, emphasizing the contribution of connectivity to global AMR burden. We discuss connectivity at ecological, microbial and genetic levels; propose an approach based on genomics and metagenomics to assess connectivity; and finally advocate for cross-sector studies to better understand AMR connectivity and mitigate dissemination. We believe that such harmonized connectivity studies will facilitate coordinated actions and investments across sectors and regions to scale up AMR management globally.

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Fig. 1: Development of AMR connectivity between the sectors of humans, animals and the environment.
Fig. 2: Approaches to assess AMR connectivity at different levels.
Fig. 3: Examining AMR connectivity within and between habitats.
Fig. 4: AMR connectivity between humans, animals and the environment and trends over time under different scenarios of the control strategy implementation.

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Acknowledgements

This work is supported by the General Research Fund (17202522), the National Natural Science Foundation of China (22193062) and the Theme-based Research Scheme of Research Grants Council of Hong Kong (T21–705/20-N).

Author information

Authors and Affiliations

  1. Environmental Microbiome Engineering and Biotechnology Laboratory, Center for Environmental Engineering Research, Department of Civil Engineering, The University of Hong Kong, Pokfulam, Hong Kong SAR, China

    Liguan Li, Xiaoqing Xu & Tong Zhang

  2. Department of Science and Environmental Studies, The Education University of Hong Kong, Taipo, Hong Kong SAR, China

    Liguan Li

  3. Shenzhen Engineering Research Laboratory for Sludge and Food Waste Treatment and Resource Recovery, Tsinghua Shenzhen International Graduate School, Tsinghua University, Shenzhen, China

    Bing Li

  4. School of Civil and Environmental Engineering, Nanyang Technological University, Singapore, Singapore

    Xiaole Yin

  5. School of Environmental Science and Engineering, College of Engineering, Southern University of Science and Technology, Shenzhen, China

    Yu Xia

  6. Center for Microbial Communities, Department of Chemistry and Bioscience, Aalborg University, Aalborg, Denmark

    Yu Yang, Per Halkjær Nielsen & Mark van Loosdrecht

  7. State Key Laboratory of Emerging Infectious Diseases, School of Public Health, The University of Hong Kong, Pokfulam, Hong Kong SAR, China

    Tommy Tsan-Yuk Lam

  8. Laboratory of Data Discovery for Health Limited, 19W Hong Kong Science & Technology Parks, Pak Shek Kok, Hong Kong SAR, China

    Tommy Tsan-Yuk Lam

  9. State Key Laboratory of Marine Environmental Health and Department of Chemistry, City University of Hong Kong, Kowloon Tong, Hong Kong SAR, China

    Kenneth M. Y. Leung

  10. Global Health Program, Duke Kunshan University, Kunshan, Jiangsu, China

    Fujie Xu

  11. State Key Laboratory of Pollution Control and Resource Reuse, School of the Environment, Nanjing University, Nanjing, China

    Xuxiang Zhang & Yi Luo

  12. Australian Centre for Water and Environmental Biotechnology, The University of Queensland, Brisbane, Queensland, Australia

    Jianhua Guo

  13. Centre for Zoonoses and Environmental Microbiology-Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), Bilthoven, The Netherlands

    Heike Schmitt

  14. Department of Biotechnology, Delft University of Technology, Delft, The Netherlands

    Heike Schmitt & Mark van Loosdrecht

  15. Michael G. DeGroote Institute for Infectious Disease Research, McMaster University, Hamilton, Ontario, Canada

    Gerard D. Wright

  16. Wellcome Trust, London, UK

    Janet Midega

  17. Unit for Environmental Sciences and Management (UESM)—Microbiology, North-West University, Potchefstroom, South Africa

    Carlos Bezuidenhout

  18. Department of Hydrobiology, Federal University of São Carlos, São Carlos, Brazil

    Renata C. Picão

  19. Medical Microbiology Department, Paulo de Góes Microbiology Institute, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil

    Renata C. Picão

  20. Department of Biochemical Engineering & Biotechnology, Indian Institute of Technology Delhi, Hauz Khas, New Delhi, India

    Shaikh Z. Ahammad

  21. Julius Kühn Institute (JKI) Federal Research Centre for Cultivated Plants, Institute for Epidemiology and Pathogen Diagnostics, Braunschweig, Germany

    Kornelia Smalla

  22. Australian Institute for Microbiology and Infection, University of Technology Sydney, Ultimo, New South Wales, Australia

    Steven P. Djordjevic

  23. Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA, USA

    Amy Pruden & Peter Vikesland

  24. Department of Civil Engineering, McGill University, Montreal, Quebec, Canada

    Dominic Frigon

  25. Department of Biology, Maynooth University, Kildare, Ireland

    Fiona Walsh

  26. Institute for Hydrobiology, Technische Universität Dresden, Dresden, Germany

    Thomas U. Berendonk

  27. Molecular Ecology Group (MEG), Water Research Institute, National Research Council of Italy (CNR-IRSA), Verbania, Italy

    Gianluca Corno

  28. Department of Civil and Environmental Engineering and Nireas International Water Research Center, University of Cyprus, Nicosia, Cyprus

    Despo Fatta-Kassinos

  29. Department of Systems Biotechnology and Center for Antibiotic Resistome, Chung-Ang University, Anseong, Republic of Korea

    Chang-Jun Cha

  30. Future Industries Institute, University of South Australia, Mawson Lakes, South Australia, Australia

    Nicholas Ashbolt & Erica Donner

  31. Cooperative Research Centre for Solving Antimicrobial Resistance in Agribusiness, Food and Environments (CRC SAAFE), Mawson Lakes, South Australia, Australia

    Nicholas Ashbolt & Erica Donner

  32. School of Environment, South China Normal University, Guangzhou, China

    Guangguo Ying

  33. College of Environmental Science and Engineering, Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria, Nankai University, Tianjin, China

    Yi Luo

  34. National Key Laboratory of Veterinary Public Health Security, College of Veterinary Medicine, China Agricultural University, Beijing, China

    Yang Wang & Jianzhong Shen

  35. National Engineering Research Center of Industrial Wastewater Detoxication and Resource Recovery, Research Center for Eco-Environmental Sciences, University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing, China

    Yu Zhang & Min Yang

  36. Department of Civil and Environmental Engineering, The Hong Kong Polytechnic University, Kowloon, Hong Kong SAR, China

    Xiangdong Li

  37. Department of Environmental Engineering, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, China

    Baolan Hu

  38. Department of Environmental Science, College of Environmental and Resource Sciences, Zhejiang University, Hangzhou, China

    Lizhong Zhu

  39. Research Unit of Food Safety, Chinese Academy of Medical Sciences, NHC Key Laboratory of Food Safety Risk Assessment, China National Center for Food Safety Risk Assessment, Beijing, China

    Yongning Wu

  40. National Key Laboratory of Intelligent Tracking and Forecasting for Infectious Diseases, National Institute of Environmental Health, Chinese Center for Disease Control and Prevention, Beijing, China

    Song Tang

  41. 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, Beijing, China

    Biao Kan

  42. Research Center for Eco-environmental Sciences, Chinese Academy of Sciences, Beijing, China

    Yong-Guan Zhu

  43. Department of Biological and Chemical Engineering, Aarhus University, Aarhus, Denmark

    Barth F. Smets

  44. Department of Biosciences, Durham University, Durham, UK

    David Graham

  45. Faculty of Geosciences and Civil Engineering, Kanazawa University, Kakuma-machi, Kanazawa, Japan

    Ryo Honda

  46. Department of Soil Chemistry, Plant Nutrition and Microbiology, Institute of Soil, Water and Environmental Sciences, The Volcani Institute, Agricultural Research Organization, Rishon LeZion, Israel

    Eddie Cytryn

  47. ARC Centre of Excellence in Synthetic Biology, Faculty of Science and Engineering, Macquarie University, Sydney, New South Wales, Australia

    Michael R. Gillings

  48. University of Exeter Medical School, Environment and Sustainability Institute, University of Exeter, Exeter, UK

    William Gaze

  49. Universidade Católica Portuguesa, CBQF-Centro de Biotecnologia e Química Fina-Laboratório Associado, Escola Superior de Biotecnologia, Porto, Portugal

    Célia M. Manaia

  50. Department of Civil and Environmental Engineering, Rice University, Houston, TX, USA

    Pedro J. J. Alvarez

  51. Center for Advanced Biotechnology and Medicine, Rutgers University, Piscataway, NJ, USA

    Martin J. Blaser

  52. Agroecology Mixed Research Unit, INRAE, Dijon, France

    Edward Topp

  53. Department of Biology, University of Western Ontario, London, Ontario, Canada

    Edward Topp

  54. School of Public Health, The University of Hong Kong, Pokfulam, Hong Kong SAR, China

    Tong Zhang

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Contributions

T.Z., L.L., B.L., X.Y. and E.T. conceptualized the study. T.Z. provided supervision and guided the overall direction. L.L. designed the figures and wrote the manuscript, with input from all authors. Y.X., Y.Y. and X.X. contributed to visualization. M.R.G., W.G., M.J.B., C.M.M., D.G., K.S., S.P.D., A.P., P.V., E.C., E.D., N.A., G.C., D.F.-K., F.W. and T.U.B. contributed to discussion of the content, and writing and editing of the manuscript. P.J.J.A., M.v.L., P.H.N., R.H., B.F.S., D.F., T.T.-Y.L., K.M.Y.L., F.X., X.Z., J.G., H.S., G.D.W., J.M., C.B., R.C.P., S.Z.A., C.-J.C., G.Y., Y.L., Y.W., J.S., Y.Z., M.Y., X.L., B.H., L.Z., Y.W., S.T., B.K. and Y.-G.Z. commented on the paper. All authors read and approved the final version of the manuscript.

Corresponding author

Correspondence to Tong Zhang.

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Nature Water thanks Davida Smyth and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Li, L., Li, B., Yin, X. et al. Assessing antimicrobial resistance connectivity across One Health sectors. Nat Water 3, 1100–1113 (2025). https://doi.org/10.1038/s44221-025-00514-8

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