Geographics and bacterial networks differently shape the acquired and latent global sewage resistomes
Hannah-Marie Martiny, Patrick Munk, Alessandro Fuschi, Ágnes Becsei, Nikiforos Pyrounakis, Christian Brinch, D. G. Joakim Larsson, Marion Koopmans, Nawel Zaatout, Catherine A. Rees, Guangming Jiang, Jiahua Shi, Bernhard Benka, Franz Allerberger, Sandra Koeberl-Jelovcan, Khalil Hasan Abdulla, Ali Bin Thani, Anowara Begum, Carlon Worrell, Tamegnon Victorien Dougnon, Freddy Soria, Nataša Mazalica, Teddie O. Rahube, Andreza Francisco Martins, Carlos Alberto Tagliati, Larissa Camila Ribeiro de Souza, Ariane Nzouankeu, Muhammad Attiq Rehman, Jeff Gauthier, Roger C. Lévesque, Sean D. Workman, Christopher K. Yost, Aiko Adell Nakashima, Andrés Opazo-Capurro, G. Gonzales, Yongjie Yu, Pilar Donado-Godoy, Tadjidine Youssouf, Pablo-César Rivera-Navarro, Matijana Jergović, Jasna Hrenović, Renáta Karpíšková, Julien Kalpy Coulibaly, William Calero‐Cáceres, M. Abouelnaga, Anna-Maria Hokajärvi, Annamari Heikinheimo, Soizick Le Guyader, Andreas Nitsche, Annika Brinkmann, Sara Schubert, Thomas U. Berendonk, Uli Klümper, Ernest Bonah, Solomon Asante-Sefa, Andrew Camilleri, Courage Kosi Setsoafia Saba, Victoria Bernice Sedor, Kassiani Μellou, Theologia Sideroglou, Charalampos Kotzamanidis, Jens-Peter B. Henriksen, Mie Møller, Thorunn R. Thorsteinsdottir, A. A. Mohamed Hatha, Sima Mohammad, Burhan Shamurad, Hiwa Ali Faraj, Dearbháile Morris, Louise O’Connor, Jacob Moran‐Gilad, Roberta Orletti, Giuseppina La Rosa, M. Iaconelli, Antonio Battisti, Lucia Decastelli, Maira Napoleoni, Alessandra De Cesare, Gianluca Corno, Jeļena Avsejenko, Ghassan M. Matar, Christian Penny, Luc Hervé Samison, Daniel L. Banda, Heera Rajandas, Sivachandran Parimannan, Malcolm Vella Haber, Sunita J. Santchurn, Julián Carrillo‐Reyes, Julian Osvaldo Sanchez-Lara, René Arredondo‐Hernández, Aleksandar Vujacic, Dijana Djurović, Pushkar Pal, Carlos Campos, Isabelle Pattis, Stephen T. Chambers, Gert‐Jan Jeunen, Charles John Elikwu, Olayinka Osuolale
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.