Cartography of opportunistic pathogens and antibiotic resistance genes in a tertiary hospital environment
Kern Rei Chng, Chenhao Li, Denis Bertrand, Amanda Hui Qi Ng, Junmei Samantha Kwah, Hwee Meng Low, Chengxuan Tong, Maanasa Natrajan, Michael Hongjie Zhang, Licheng Xu, Karrie Kwan Ki Ko, Eliza Xin Pei Ho, Tamar V. Av‐Shalom, Jeanette Teo, Chiea Chuen Khor, David Danko, Daniela Bezdan, Ebrahim Afshinnekoo, Sofia Ahsanuddin, Chandrima Bhattacharya, Daniel Butler, Kern Rei Chng, Francesca De Filippis, Jochen Hecht, André Kahles, Mikhail Karasikov, Nikos C. Kyrpides, Marcus H. Y. Leung, Dmitry Meleshko, Harun Mustafa, Beth Mutai, Russell Y. Neches, Amanda Hui Qi Ng, Marina Nieto‐Caballero, Olga Nikolayeva, Tatyana Nikolayeva, Eileen Png, Jorge L. Sánchez, Heba Shaaban, Maria A. Sierra, Xinzhao Tong, Ben Young, Josue Alicea, Malay Bhattacharyya, Ran Blekhman, Eduardo Castro‐Nallar, A Cañas, Aspassia D. Chatziefthimiou, Robert W. Crawford, Youping Deng, Christelle Desnues, Emmanuel Dias‐Neto, Daisy Donnellan, Marius Dybwad, Eran Elhaik, Danilo Ercolini, Alina Frolova, Alexandra B. Graf, David C. Green, Iman Hajirasouliha, Mark Hernandez, Gregorio Iraola, Soojin Jang, Angela Jones, Frank J. Kelly, Kaymisha Knights, Paweł P. Łabaj, Patrick K. H. Lee, Levy Shawn, Per O. Ljungdahl, Abigail Lyons, Gabriella Mason-Buck, Ken McGrath, Emmanuel F. Mongodin, Milton Ozório Moraes, Niranjan Nagarajan, Houtan Noushmehr, Manuela Oliveira, Stephan Ossowski, Olayinka Osuolale, Orhan Özcan, David Páez-Espino, Nicolás Rascovan, Hugues Richard, Gunnar Rätsch, Lynn M. Schriml, Torsten Semmler, Osman Uğur Sezerman, Leming Shi, Le Huu Song, Haruo Suzuki, Denise Syndercombe Court, Dominique Thomas, Scott Tighe, Klas I. Udekwu, Juan A. Ugalde, Brandon Valentine, Dimitar Vassilev, Elena Vayndorf, Thirumalaisamy P. Velavan
Abstract
Although disinfection is key to infection control, the colonization patterns and resistomes of hospital-environment microbes remain underexplored. We report the first extensive genomic characterization of microbiomes, pathogens and antibiotic resistance cassettes in a tertiary-care hospital, from repeated sampling (up to 1.5 years apart) of 179 sites associated with 45 beds. Deep shotgun metagenomics unveiled distinct ecological niches of microbes and antibiotic resistance genes characterized by biofilm-forming and human-microbiome-influenced environments with corresponding patterns of spatiotemporal divergence. Quasi-metagenomics with nanopore sequencing provided thousands of high-contiguity genomes, phage and plasmid sequences (>60% novel), enabling characterization of resistome and mobilome diversity and dynamic architectures in hospital environments. Phylogenetics identified multidrug-resistant strains as being widely distributed and stably colonizing across sites. Comparisons with clinical isolates indicated that such microbes can persist in hospitals for extended periods (>8 years), to opportunistically infect patients. These findings highlight the importance of characterizing antibiotic resistance reservoirs in hospitals and establish the feasibility of systematic surveys to target resources for preventing infections.