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Landscape of global urban environmental resistome and its association with local socioeconomic and medical status

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Abstract

Antimicrobial resistance (AMR) poses a critical threat to global health and development, with environmental factors—particularly in urban areas—contributing significantly to the spread of antibiotic resistance genes (ARGs). However, most research to date has been conducted at a local level, leaving significant gaps in our understanding of the global status of antibiotic resistance in urban environments. To address this issue, we thoroughly analyzed a total of 86,213 ARGs detected within 4,728 metagenome samples, which were collected by the MetaSUB International Consortium involving diverse urban environments in 60 cities of 27 countries, utilizing a deep-learning based methodology. Our findings demonstrated the strong geographical specificity of urban environmental resistome, and their correlation with various local socioeconomic and medical conditions. We also identified distinctive evolutionary patterns of ARG-related biosynthetic gene clusters (BGCs) across different countries, and discovered that the urban environment represents a rich source of novel antibiotics. Our study provides a comprehensive overview of the global urban environmental resistome, and fills a significant gap in our knowledge of large-scale urban antibiotic resistome analysis.

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Availability of data and material

The MetaSUB sequence data as well as the metadata can be downloaded from https://www.pangeablo.lo/. The analysis pipeline and data are available at https://github.com/Junwu302/Urban_ARGs.

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Acknowledgement

This work was supported by the National Key Research and Development Program of China (2023YFC2706503), the National Natural Science Foundation of China (32370720), Beihang University & Capital Medical University Plan (BHME-201904), the Open Research Fund of Key Laboratory of Advanced Theory and Application in Statistics and Data Science-MOE, ECNU, Key Laboratory of MEA, Ministry of Education, ECNU, Key Laboratory of Ecology and Energy Saving Study of Dense Habitat (Tongji University), Ministry of Education - Shanghai Tongji Urban Planning & Design Institute Co., Ltd Joint Research Project (KY-2022-LH-A03), and Shanghai Tongji Urban Planning & Design Institute Co., Ltd - China Intelligent Urbanization Co-creation Center for High Density Region Research Project (KY-2022-PT-A02). We thank all the members in the MetaSUB consortium for generating the raw data used in this study. We would like to thank the Epigenomics Core Facility at Weill Cornell Medicine, the Scientific Computing Unit (SCU), XSEDE Supercomputing Resources, as well as funding from the Irma T. Hirschl and Monique Weill-Caulier Charitable Trusts, Bert L and N Kuggie Vallee Foundation, the WorldQuant Foundation, The Pershing Square Sohn Cancer Research Alliance, the National Institutes of Health (R01AI151059), the National Science Foundation (1840275), and the Alfred P. Sloan Foundation (G-2015-13964).

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Authors and Affiliations

  1. Center for Bioinformatics and Computational Biology, and the Institute of Biomedical Sciences, School of Life Sciences, East China Normal University, Shanghai, 200241, China

    Jun Wu, Yige Hu & Tieliu Shi

  2. Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, 40292, USA

    Michael H. Perlin

  3. Weill Cornell Medicine, New York, 10065, USA

    David Danko, Maria A. Sierra & Christopher E. Mason

  4. The Bin Talal Bin Abdulaziz Alsaud Institute for Computational Biomedicine, New York, 10065, USA

    David Danko, Maria A. Sierra & Christopher E. Mason

  5. Department of Pulmonary Medicine, Shanghai Chest Hospital, Shanghai Jiao Tong University, Shanghai, 200025, China

    Jun Lu

  6. i3S - Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, 4050-290, Portugal

    Manuela Oliveira

  7. Ipatimup - Instituto de Patologia e Imunologia Molecular da Universidade do Porto, Porto, 4200-465, Portugal

    Manuela Oliveira

  8. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, 4050-290, Portugal

    Manuela Oliveira

  9. High Performance and Cloud Computing Group, Zentrum für Datenverarbeitung (ZDV), Eberhard Karls University of Tübingen, Wächterstraße 76, 72074, Tübingen, Germany

    Johannes Werner

  10. Corporación Corpogen Research Center, Bogotá, 110311, Colombia

    Maria M. Zambrano

  11. Applied Environmental Metagenomics and Infectious Diseases Research (AEMIDR), Department of Biological Sciences, Elizade University, Ilara-Mokin, 340271, Nigeria

    Olayinka O. Osuolale

  12. Maopolska Centre of Biotechnology, Jagiellonian University, Kraków, 30-005, Poland

    Paweł Łabaj

  13. Aix-Marseille Université, Mediterranean Institute of Oceanology, Université de Toulon, CNRS, IRD, UM 110, Marseille, 83041, France

    Nicolás Rascovan

  14. Department of Biological Sciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia UKM, 43600, Bangi, Selangor, Malaysia

    Nur Hazlin Hazrin-Chong

  15. Institut Pasteur Korea, Seoul, 13488, Republic of Korea

    Soojin Jang

  16. Faculty of Environment and Information Studies, Keio University, Fujisawa, Kanagawa, 252-0882, Japan

    Haruo Suzuki

  17. Civil, Environmental and Architectural Department, University of Colorado at Boulder, Boulder, 80303, USA

    Marina Nieto-Caballero

  18. Brooklyn College of the City University of New York, Brooklyn, 11210, USA

    Bharath Prithiviraj

  19. School of Energy and Environment, City University of Hong Kong, Hong Kong, 999077, China

    Patrick K. H. Lee

  20. Department of Microbiology, Faculty of Medicine, Jagiellonian University, Krakow, 30-005, Poland

    Agnieszka Chmielarczyk & Anna Różańska

  21. Biological Targeting Diagnosis and Therapy Research Center, Guangxi Medical University, Nanning, 530021, China

    Yongxiang Zhao

  22. College of Architecture and Urban Planning, Tongji University, Shanghai, 200092, China

    Lan Wang

  23. Beijing Advanced Innovation Center for Big Data-Based Precision Medicine, Beihang University & Capital Medical University, Beijing, 100083, China

    Tieliu Shi

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  1. Jun Wu
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  2. Yige Hu
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  21. Yongxiang Zhao
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  22. Lan Wang
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  23. Christopher E. Mason
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  24. Tieliu Shi
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Corresponding authors

Correspondence to Yongxiang Zhao, Lan Wang, Christopher E. Mason or Tieliu Shi.

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The authors declare no competing financial interests relevant to the study, although Christopher E Mason is a co-Founder of Biotia.

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Wu, J., Hu, Y., Perlin, M.H. et al. Landscape of global urban environmental resistome and its association with local socioeconomic and medical status. Sci. China Life Sci. (2024). https://doi.org/10.1007/s11427-023-2504-1

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