Geographics and bacterial networks differently shape the acquired and latent global sewage resistomes

Antimicrobial resistance genes (ARGs) have rapidly emerged and spread globally, but the pathways driving their spread remain poorly understood. We analyzed 1240 sewage samples from 351 cities across 111 countries, comparing ARGs known to be mobilized with those identified through functional metagenomics (FG). FG ARGs showed stronger associations with bacterial taxa than the acquired ARGs. Network analyses further confirmed this and showed potential for source attribution of both known and novel ARGs. The FG resistome was more evenly dispersed globally, whereas the acquired resistome followed distinct geographical patterns. City-wise distance-decay analyses revealed that the FG ARGs showed significant decay within countries but not across regions or globally. In contrast, acquired ARGs showed decay at both national and regional scales. At the variant level, both ARG groups had significant national and regional distance-decay effects, but only FG ARGs at a global scale. Additionally, we observed stronger distance effects in Sub-Saharan Africa and East Asia compared to North America. Our findings suggest that differential selection and niche competition, rather than dispersal, shape the global resistome patterns. A limited number of bacterial taxa may act as reservoirs of latent FG ARGs, highlighting the need of targeted surveillance to mitigate future resistance threats.

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Publication Details

Journal
Nature Communications
Published
2025-11-21
DOI
https://doi.org/10.1038/s41467-025-66070-7
Citations
5
Primary Topic
Pharmaceutical and Antibiotic Environmental Impacts
Type
article
Field-Weighted Citation Impact
2.52

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article

Geographics and bacterial networks differently shape the acquired and latent global sewage resistomes

Malcolm Vella Haber, Anna-Maria Hokajärvi, Célia M. Manaia, Aleksandar Vujacic et al.
5 citations
Nature Communications
Pharmaceutical and Antibiotic Environmental Impacts
2.52
article

Geographics and bacterial networks differently shape the acquired and latent global sewage resistomes

Malcolm Vella Haber, Anna-Maria Hokajärvi, Célia M. Manaia, Aleksandar Vujacic, Matijana Jergović, G. Gonzales, J. J. Medardus, Patrick Munk, Teddie O. Rahube, Christian Brinch, Giuseppina La Rosa, Anne Frances Clare Leonard, Carlos Campos, Marija Trkov, D. G. Joakim Larsson, Thomas Ulrich Berendonk, Cemil Kürekçi, Andreas Nitsche, Christopher K. Yost, Patrick J. McNamara, Marion Koopmans, Carlon Worrell, Ibrahim Adisa Raufu, Julián Carrillo‐Reyes, Larissa Camila Ribeiro de Souza, Oluwadamilola Abiodun-Adewusi, Pushkar Pal, Sukhwan Yoon, Jeļena Avsejenko, Magdalena Zając, Amen Ekhosuehi, Erica R. Fuhrmeister, Vladimir Radosavljević, Stephen T. Chambers, Nataša Mazalica, Nicola K. Beck, Victorien Tamègnon Dougnon, Freddy Soria, Frank M. Aarestrup, Uli Klümper, Sean D. Workman, Annamari Heikinheimo, Daniel Remondini, Fernando Gónzález‐Candelas, Hiwa Ali Faraj, Maria Jorge Campos, Olayinka Osuolale, Jeff Gauthier, Jasna Hrenović, Solomon Asante-Sefa, Charles John Elikwu, Bernhard Benka, Hor‐Gil Hur, Dariusz Wasyl, Ernest Bonah, Samaila Musa Chiroma, Tanja Van der Heijden, Ayella Maile-Moskowitz, Anowara Begum, Jens Thomsen, Rukayya Hussain Abubakar, Pilar Donado-Godoy, Antonio Battisti, William Calero‐Cáceres, Yongjie Yu, Dearbháile Morris, Mie Møller, Daniel L. Banda, Christian Penny, Heera Rajandas, Kevin Chau, Sandra Koeberl-Jelovcan, Charalampos Kotzamanidis, Jiahua Shi, Mabel Kamweli Aworh, Renáta Karpíšková, Dagmar Gavačová, Ayorinde O. Afolayan, Angel Anisa Cokro, Akeem Olayiwola Ahmed, Luc Hervé Samison, Andrés Opazo-Capurro, Sivachandran Parimannan, Gianluca Corno, Roger C. Lévesque, Lucia Decastelli, Guangming Jiang, István Csabai, Ali Bin Thani, Maira Napoleoni, Alessandro Fuschi, Carlos Alberto Tagliati, Yu-Ping Hong, Khalil Hasan Abdulla, Annika Brinkmann, M. Iaconelli, Gert‐Jan Jeunen, Karen H. Keddy, Kayode Fashae, René Arredondo‐Hernández, Ismail Ayoade Odetokun, Olga Burduniuc, Jacob Moran‐Gilad, Natalie Weiler, Eugénia Cardoso, Isabelle Pattis, Theologia Sideroglou, Isabel Martínez‐Alcalá, Hannah-Marie Martiny, John Scott Meschke, Catherine A. Rees, Joaquín Sánchez-Lara, Ouidiane Obaidi, Sunita J. Santchurn, Nawel Zaatout, Alessandra De Cesare, Franz Allerberger, Thorunn R. Thorsteinsdottir, A. A. Mohamed Hatha, Mwapu Dika Ndahi, Andreza Francisco Martins, Julien Kalpy Coulibaly, Marta Cerdà‐Cuéllar, Courage Kosi Setsoafia Saba, Ágnes Becsei, Rune Holmstad, M. Abouelnaga, Lilly Wong, Sara Schubert, Pei‐Ying Hong, Ghassan M. Matar, Muhammad Attiq Rehman, Kassiani Μellou, Victoria Bernice Sedor, Nikiforos Pyrounakis, Min Song, Claire L. Mitchell, Saeed Mohammad, Louise O’Connor, Dijana Djurović, A Cañas, Soizick Le Guyader, Ariane Nzouankeu, Rajeev Nagassar, Lihong Zhang, Tadjidine Youssouf, Bruce Paterson, Andrew Camilleri, Aiko Adell Nakashima, Pablo-César Rivera-Navarro, Burhan Shamurad, Roberta Orletti, Yahia Ali Sabiel, Jens-Peter B. Henriksen
article en
5 citations

Abstract

Antimicrobial resistance genes (ARGs) have rapidly emerged and spread globally, but the pathways driving their spread remain poorly understood. We analyzed 1240 sewage samples from 351 cities across 111 countries, comparing ARGs known to be mobilized with those identified through functional metagenomics (FG). FG ARGs showed stronger associations with bacterial taxa than the acquired ARGs. Network analyses further confirmed this and showed potential for source attribution of both known and novel ARGs. The FG resistome was more evenly dispersed globally, whereas the acquired resistome followed distinct geographical patterns. City-wise distance-decay analyses revealed that the FG ARGs showed significant decay within countries but not across regions or globally. In contrast, acquired ARGs showed decay at both national and regional scales. At the variant level, both ARG groups had significant national and regional distance-decay effects, but only FG ARGs at a global scale. Additionally, we observed stronger distance effects in Sub-Saharan Africa and East Asia compared to North America. Our findings suggest that differential selection and niche competition, rather than dispersal, shape the global resistome patterns. A limited number of bacterial taxa may act as reservoirs of latent FG ARGs, highlighting the need of targeted surveillance to mitigate future resistance threats.

Nature CommunicationsVol. 16(1)
Marquette University (US), Eötvös Loránd University (HU), University of Bahrain (BH), Universidade Federal de Minas Gerais (BR), Suez Canal University (EG), Tufts University (US), Universidade Federal do Rio Grande do Sul (BR), University of Helsinki (FI), University of Ilorin (NG), University of Antananarivo (MG), Universidad Andrés Bello (CL), Ifremer (FR), Korea Advanced Institute of Science and Technology (KR), University of Malawi (MW), Universitat de València (ES), University of Batna 1 (DZ), University of Iceland (IS), Tampere University (FI), Instituto Politécnico de Leiria (PT), Nanyang Technological University (SG), University of Concepción (CL), Ilisimatusarfik (GL), University of Zagreb (HR), University of Ibadan (NG), Scottish Environment Protection Agency (GB), Ollscoil na Gaillimhe – University of Galway (IE), University of Regina (CA), Nanjing University of Information Science and Technology (CN), University of Washington (US), Melbourne Water (AU), University of Wollongong (AU), Cochin University of Science and Technology (IN), University of Dhaka (BD), Botswana International University of Science and Technology (BW), University of Exeter (GB), Robert Koch Institute (DE), Universidade Católica Portuguesa (PT), Istituto Superiore di Sanità (IT), Instituto de Salud Carlos III (ES), Agriculture and Forestry University (NP), Federal Ministry of Agriculture and Rural Development (NG), Israel Ministry of Health (IL), AIMST University (MY), Babcock University (NG), Elizade University (NG), Universidad de Costa Rica (CR), Gwangju Institute of Science and Technology (KR), University of Oxford (GB), Institute of Food Safety, Animal Health and Environment “BIOR” (LV), Escuela Nacional de Sanidad (ES), African Field Epidemiology Network (NG), Greenland National Museum & Archives (GL), Research and Productivity Council (CA), Abu Dhabi Health Services (AE), Centre de Recerca en Sanitat Animal (ES), Regional Health (US), Public Health Authority of the Slovak Republic (SK), Ambiente Italia (Italy) (IT), Laboratoire National de Référence (MA), Luxembourg Institute of Science and Technology (LU), Centre Pasteur du Cameroun (CM), Water Research Institute (IT), Veterinary Research Institute (CZ), Université d'Abomey-Calavi (BJ), National Veterinary Research Institute (PL), Public Health Institute of the Republic of Srpska (BA), Development Center for Biotechnology (TW), Istituto Zooprofilattico Sperimentale dell'Umbria e delle Marche (IT), Colombian Corporation for Agricultural Research - AGROSAVIA (CO), New Zealand Institute for Public Health and Forensic Science (NZ), National Laboratory of Health, Environment and Food (SI), Bahrain Center for Strategic International and Energy Studies (BH), Ministry for Health (MT), Andrija Stampar Teaching Institute of Public Health (HR), Ministerio de Salud Pública y Bienestar Social (PY), Institut Pasteur de Côte d'Ivoire (CI), Barbados Community College (BB), Ministry of Food and Agriculture (GH), Universidad Técnica de Ambato (EC), National Public Health Organization (GR), Istituto Zooprofilattico Sperimentale delle Regioni Lazio e Toscana (IT), Águas de Portugal (Portugal) (PT), Asiaq Greenland Survey (GL), National Research Council (IT), Ghana Health Service (GH), Austrian Agency for Health and Food Safety (AT), Istituto Zooprofilattico Sperimentale del Piemonte Liguria e Valle d'Aosta (IT), Université Laval (CA), Mustafa Kemal University (TR), Shahid Beheshti University (IR), University of Montenegro (ME), Cawthron Institute (NZ), University of Benin (NG), University of Maiduguri (NG), University of Sulaimani (IQ), Universidad Católica de Murcia (ES), University of Mauritius (MU), University of Pretoria (ZA), King Abdullah University of Science and Technology (SA), Technische Universität Dresden (DE), Universidad de Murcia (ES), University of Otago (NZ), University for Development Studies (GH), Sokoine University of Agriculture (TZ), Virginia Tech (US), University of Gothenburg (SE), Dubai Pharmacy College (AE), Universidad Nacional Autónoma de México (MX), Erasmus University Rotterdam (NL), Universidad Católica Boliviana San Pablo (BO), Sudan University of Science and Technology (SD), University of Bologna (IT), Technical University of Denmark (DK), American University of Beirut (LB)
European Commission, Novo Nordisk, Novo Nordisk Fonden, Horizon 2020 Framework Programme
Openalex Percentile: Top 10%
Pharmaceutical and Antibiotic Environmental Impacts
2.52
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