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1. A global metagenomic map of urban microbiomes and antimicrobial resistance.

Author

Danko D, Bezdan D, Afshin EE, Ahsanuddin S, Bhattacharya C, Butler DJ, Chng KR, Donnellan D, Hecht J, Jackson K, Kuchin K, Karasikov M, Lyons A, Mak L, Meleshko D, Mustafa H, Mutai B, Neches RY, Ng A, Nikolayeva O, Nikolayeva T, Png E, Ryon KA, Sanchez JL, Shaaban H, Sierra MA, Thomas D, Young B, Abudayyeh OO, Alicea J, Bhattacharyya M, Blekhman R, Castro-Nallar E, Cañas AM, Chatziefthimiou AD, Crawford RW, De Filippis F, Deng Y, Desnues C, Dias-Neto E, Dybwad M, Elhaik E, Ercolini D, Frolova A, Gankin D, Gootenberg JS, Graf AB, Green DC, Hajirasouliha I, Hastings JJA, Hernandez M, Iraola G, Jang S, Kahles A, Kelly FJ, Knights K, Kyrpides NC, Łabaj PP, Lee PKH, Leung MHY, Ljungdahl PO, Mason-Buck G, McGrath K, Meydan C, Mongodin EF, Moraes MO, Nagarajan N, Nieto-Caballero M, Noushmehr H, Oliveira M, Ossowski S, Osuolale OO, Özcan O, Paez-Espino D, Rascovan N, Richard H, Rätsch G, Schriml LM, Semmler T, Sezerman OU, Shi L, Shi T, Siam R, Song LH, Suzuki H, Court DS, Tighe SW, Tong X, Udekwu KI, Ugalde JA, Valentine B, Vassilev DI, Vayndorf EM, Velavan TP, Wu J, Zambrano MM, Zhu J, Zhu S, and Mason CE

Subjects
Biodiversity, Databases, Genetic, Humans, Drug Resistance, Bacterial genetics, Metagenomics, Microbiota genetics, Urban Population
Abstract

We present a global atlas of 4,728 metagenomic samples from mass-transit systems in 60 cities over 3 years, representing the first systematic, worldwide catalog of the urban microbial ecosystem. This atlas provides an annotated, geospatial profile of microbial strains, functional characteristics, antimicrobial resistance (AMR) markers, and genetic elements, including 10,928 viruses, 1,302 bacteria, 2 archaea, and 838,532 CRISPR arrays not found in reference databases. We identified 4,246 known species of urban microorganisms and a consistent set of 31 species found in 97% of samples that were distinct from human commensal organisms. Profiles of AMR genes varied widely in type and density across cities. Cities showed distinct microbial taxonomic signatures that were driven by climate and geographic differences. These results constitute a high-resolution global metagenomic atlas that enables discovery of organisms and genes, highlights potential public health and forensic applications, and provides a culture-independent view of AMR burden in cities., Competing Interests: Declaration of interests C.E.M. is co-founder of Biotia and Onegevity Health. D.B. is co-founder and CSO of Poppy Health Inc. The other authors declare they have no competing interests that impacted this study., (Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.)

Published
2021
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2. Cartography of opportunistic pathogens and antibiotic resistance genes in a tertiary hospital environment

Author

Chng K. R., Li C., Bertrand D., Ng A. H. Q., Kwah J. S., Low H. M., Tong C., Natrajan M., Zhang M. H., Xu L., Ko K. K. K., Ho E. X. P., Av-Shalom T. V., Teo J. W. P., Khor C. C., Danko D., Bezdan D., Afshinnekoo E., Ahsanuddin S., Bhattacharya C., Butler D. J., De Filippis F., Hecht J., Kahles A., Karasikov M., Kyrpides N. C., Leung M. H. Y., Meleshko D., Mustafa H., Mutai B., Neches R. Y., Ng A., Nieto-Caballero M., Nikolayeva O., Nikolayeva T., Png E., Sanchez J. L., Shaaban H., Sierra M. A., Tong X., Young B., Alicea J., Bhattacharyya M., Blekhman R., Castro-Nallar E., Canas A. M., Chatziefthimiou A. D., Crawford R. W., Deng Y., Desnues C., Dias-Neto E., Donnellan D., Dybwad M., Elhaik E., Ercolini D., Frolova A., Graf A. B., Green D. C., Hajirasouliha I., Hernandez M., Iraola G., Jang S., Jones A., Kelly F. J., Knights K., Labaj P. P., Lee P. K. H., Shawn L., Ljungdahl P., Lyons A., Mason-Buck G., McGrath K., Mongodin E. F., Moraes M. O., Nagarajan N., Noushmehr H., Oliveira M., Ossowski S., Osuolale O. O., Ozcan O., Paez-Espino D., Rascovan N., Richard H., Ratsch G., Schriml L. M., Semmler T., Sezerman O. U., Shi L., Song L. H., Suzuki H., Court D. S., Thomas D., Tighe S. W., Udekwu K. I., Ugalde J. A., Valentine B., Vassilev D. I., Vayndorf E., Velavan T. P., Zambrano M. M., Zhu J., Zhu S., Mason C. E., Chen S. L., Ng O. T., Marimuthu K., Ang B., Genome Institute of Singapore (GIS), Singapore University of Technology and Design (SUTD), Singapore General Hospital, National University Hospital [Singapore] (NUH), Weill Cornell Medicine [Cornell University], Cornell University [New York], Nanyang Technological University [Singapour], Tan Tock Seng Hospital, Department of Computational and Systems Biology [Singapore], Funding for this work was provided by A*STAR (N.N.), and we are grateful for support from NMRC (NMRC CGAug16C005: O.T.N. and K.M.). C.E.M. acknowledges support from the WorldQuant Foundation, the Bill and Melinda Gates Foundation (OPP1151054) and the Alfred P. Sloan Foundation (G-2015-13964). The funders had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript. We would like to thank J. Gilbert for insightful comments and feedback on this work., MetaSUB Consortium: David Danko, Daniela Bezdan, Ebrahim Afshinnekoo, Sofia Ahsanuddin, Chandrima Bhattacharya, Daniel J. Butler, Kern Rei Chng, Francesca De Filippis, Jochen Hecht, Andre Kahles, Mikhail Karasikov, Nikos C. Kyrpides, Marcus H. Y. Leung, Dmitry Meleshko, Harun Mustafa, Beth Mutai, Russell Y. Neches, Amanda Ng, Marina Nieto-Caballero, Olga Nikolayeva, Tatyana Nikolayeva, Eileen Png, Jorge L. Sanchez, Heba Shaaban, Maria A. Sierra, Xinzhao Tong, Ben Young, Josue Alicea, Malay Bhattacharyya, Ran Blekhman, Eduardo Castro-Nallar, Ana M. 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 Ljungdahl, Abigail Lyons, Gabriella Mason-Buck, Ken McGrath, Emmanuel F. Mongodin, Milton Ozorio Moraes, Niranjan Nagarajan, Houtan Noushmehr, Manuela Oliveira, Stephan Ossowski, Olayinka O. Osuolale, Orhan Özcan, David Paez-Espino, Nicolas Rascovan, Hugues Richard, Gunnar Rätsch, Lynn M. Schriml, Torsten Semmler, Osman U. Sezerman, Leming Shi, Le Huu Song, Haruo Suzuki, Denise Syndercombe Court, Dominique Thomas, Scott W. Tighe, Klas I. Udekwu, Juan A. Ugalde, Brandon Valentine, Dimitar I. Vassilev, Elena Vayndorf, Thirumalaisamy P. Velavan, María M. Zambrano, Jifeng Zhu, Sibo Zhu & Christopher E. Mason, Weill Cornell Medicine [New York], Chng, K. R., Li, C., Bertrand, D., Ng, A. H. Q., Kwah, J. S., Low, H. M., Tong, C., Natrajan, M., Zhang, M. H., Xu, L., Ko, K. K. K., Ho, E. X. P., Av-Shalom, T. V., Teo, J. W. P., Khor, C. C., Danko, D., Bezdan, D., Afshinnekoo, E., Ahsanuddin, S., Bhattacharya, C., Butler, D. J., De Filippis, F., Hecht, J., Kahles, A., Karasikov, M., Kyrpides, N. C., Leung, M. H. Y., Meleshko, D., Mustafa, H., Mutai, B., Neches, R. Y., Ng, A., Nieto-Caballero, M., Nikolayeva, O., Nikolayeva, T., Png, E., Sanchez, J. L., Shaaban, H., Sierra, M. A., Tong, X., Young, B., Alicea, J., Bhattacharyya, M., Blekhman, R., Castro-Nallar, E., Canas, A. M., Chatziefthimiou, A. D., Crawford, R. W., Deng, Y., Desnues, C., Dias-Neto, E., Donnellan, D., Dybwad, M., Elhaik, E., Ercolini, D., Frolova, A., Graf, A. B., Green, D. C., Hajirasouliha, I., Hernandez, M., Iraola, G., Jang, S., Jones, A., Kelly, F. J., Knights, K., Labaj, P. P., Lee, P. K. H., Shawn, L., Ljungdahl, P., Lyons, A., Mason-Buck, G., Mcgrath, K., Mongodin, E. F., Moraes, M. O., Nagarajan, N., Noushmehr, H., Oliveira, M., Ossowski, S., Osuolale, O. O., Ozcan, O., Paez-Espino, D., Rascovan, N., Richard, H., Ratsch, G., Schriml, L. M., Semmler, T., Sezerman, O. U., Shi, L., Song, L. H., Suzuki, H., Court, D. S., Thomas, D., Tighe, S. W., Udekwu, K. I., Ugalde, J. A., Valentine, B., Vassilev, D. I., Vayndorf, E., Velavan, T. P., Zambrano, M. M., Zhu, J., Zhu, S., Mason, C. E., Chen, S. L., Ng, O. T., Marimuthu, K., Ang, B., and Acibadem University Dspace

Subjects
0301 basic medicine, Disease prevention, 030106 microbiology, Geographic Mapping, Drug resistance, Beds, Biology, Opportunistic Infections, Genome, General Biochemistry, Genetics and Molecular Biology, Article, Tertiary Care Centers, 03 medical and health sciences, Plasmid, Antibiotic resistance, Spatio-Temporal Analysis, Drug Resistance, Multiple, Bacterial, Drug Resistance, Bacterial, Patients' Rooms, Humans, Microbiome, Equipment and Supplies, Hospital, Genetics, Cross Infection, Infection Control, Singapore, Microbiota, General Medicine, [SDV.MP.BAC]Life Sciences [q-bio]/Microbiology and Parasitology/Bacteriology, 3. Good health, Resistome, Disinfection, 030104 developmental biology, Metagenomics, Biofilms, Equipment Contamination, Mobilome, Microbial genetics
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., Spatiotemporal characterization of microbial diversity and antibiotic resistance in a tertiary-care hospital reveals broad distribution and persistence of antibiotic-resistant organisms that could cause opportunistic infections in a healthcare setting.

Published
2020

3. A global metagenomic map of urban microbiomes and antimicrobial resistance

Author

Nadine Farhat, Tomoki Takeda, Astred Castro, Ken McGrath, Khaliun Sanchir, Iman Hajirasouliha, Eunice So, Laraib Zafar, Diana N. Nunes, Harun Mustafa, Amy Zhang, Priscilla Lisboa, Christian Schori, Marisano James, Jasna Chalangal, Sebastien Halary, Shahryar Rana, Yunmi Lee, Oli Schacher, Liliana Godoy, David A. Coil, Phanthira Pugdeethosal, Michelle D. Williams, German Marchandon, Angela Cantillo, Naoya Takahashi, Christopher Mozsary, Juana Gonzalez, Patrick K. H. Lee, Gerardo de Lamotte, Alessandro Robertiello, Steven Du, Fabienne Velter, Stefan G. Stark, Miguel Carbajo, Vincent Matthys, David A. Westfall, Julia Boeri, Irène Mauricette Mendy, Jonathan Cedillo, Francesco Oteri, Robert W. Crawford, Takayuki Ito, Tina Wunderlin, Maureen Muscat, David Paez-Espino, Carmen Urgiles, Aida Nesimi, Steffen Schaaf, Adan Ramirez-Rojas, Kunihiko Miyake, Christopher E. Mason, Anais Cardenas, Sharah Islam, Diego Benítez, Melissa Pool Pizzi, Kianna Ciaramella, Ciro Borrelli, Riham Islam, Dorottya Nagy-Szakal, Abd-Manaaf Bakere, Ait-hamlat Adel, Olha Lakhneko, Badamnyambuu Iderzorig, Ana Valeria Castro, Adam Phillips, Robert A. Petit, Flavia Corsi, Romain Conte, Krista Ryon, Soojin Jang, Joseph Benson, Fernanda de Souza Gomes Kehdy, Cindy Wang, Nicole Mathews, Jenn-Wei Chen, Rachel Paras, Paulina Pastuszek, Abigail Lyons, Paul Roldán, Muntaha Munia, Pierre Nicolas, Cassie L. Ettinger, Kyrylo Pyrshev, Katterinne N. Mendez, Eduardo Castro-Nallar, Valeriia Dotsenko, Michelle Tuz, Krizzy Mallari, Eileen Png, Yuya Sonohara, Tanja Miketic, Stéphane Delmas, Shu Zhang, Masaki Sato, Yuanting Zheng, Jifeng Zhu, Roland Häusler, Lucie Bittner, Savlatjon Rahmatulloev, Jonathan Foox, Bruno D'Alessandro, Alketa Plaku, Faisal Alquaddoomi, Yang Zhang, Kern Rei Chng, Juliana Lago, Allaeddine Chettouh, Tamera Henry, Houtan Noushmehr, Tranette Gregory, Sara Abdul Majid, Frank J. Kelly, Benjamin Pulatov, Laurie Casalot, Takema Kajita, Lennard Epping, Thais Fernanda Bartelli, Eftar Moniruzzaman, Renee Vivancos-Koopman, Thirumalaisamy P. Velavan, Tracy W. Liu, Yelyzaveta Tymoshenko, Alma Plaku, Nika Gurianova, Ambar Mendez, Anna Tomaselli, Sonia Dorado, Donato Giovannelli, Hira Choudhry, Synti Ng, Sheelta S. Kumar, Jennifer Q. Lu, Weijun Liang, Ellen Koag, Dennis Gankin, Maria João Amorim, Gwenola Simon, Kiyoshi Suganuma, Mikhail Karasikov, Christos A. Ouzounis, Madelyn May, Eran Elhaik, Stephan Ossowski, Kevin Bolzli, Matthew Arthur, Yuya Oto, Jananan Pathmanathan, Salah Mahmoud, Kou Takahashi, Brunna Marques, Kelly French, Felipe Sepúlveda, Shusei Yoshikawa, Paulo Thiago de Souza Santos, Andrew N. Gray, Juliana S Bernardes, Felipe Segato, Björn Brindefalk, George C. Yeh, Jhovana L. Velasco Flores, Jill Sullivan, Silva Baburyan, Denisse Flores, Russell Y. Neches, Sabrina Persaud, Rasheena Wright, Takumi Togashi, Verónica Antelo, Nao Kato, Skye Felice, Tatjana Mustac, Daisy Donnellan, Katerine Carrillo, Anna Litskevitch, Catalina García, Sota Ito, Naya Eady, Andrew Wan, Irene Meng, Sophie Guasco, Danilo Ercolini, Francesca De Filippis, Vincent Lemaire, Luice Fan, Lothar H. Wieler, Mariia Rybak, Jorge Sanchez, Jonathan S. Gootenberg, Itsuki Tomita, Maritza S Mosella, Laura Garcia, Natalka Makogon, Daisy Cheung, Hitler Francois Vasquez Arevalo, Freddy Asenjo, Gabriela P. Branco, Erika Cifuentes, Chloé Dequeker, Aspassia D. Chatziefthimiou, Alexis Terrero, Roy Meoded, Isabelle de Oliveira Moraes, Shaleni K. Singh, Orgil-Erdene Molomjamts, Karishma Miah, Laurent David, Wolfgang Haehr, Dao Phuong Giang, Romain Lannes, Prashanthi Ratnanandan, Ryota Yamanaka, Riccardo Vicedomini, Sadaf Ayaz, Oluwatosin M. Osuolale, Laura E. Vann, Gregory Chem, Andrea Gonzalez, Aszia Burrell, Ariel Chernomoretz, Sakura Ishizuka, Michelle Rivera, Avigdor Nosrati, Michelle B. Chen, Juliette Auvinet, Nils Ordioni, Tomoro Warashina, Guillaume Blanc, Tomislav Ivankovic, Christina Black, Lauren E. Hittle, David Hess-Homeier, Michael Kozhar, Hamood Suliman, Karobi Moitra, Saher Rahiel, Spyridon Gkotzis, Jenny Arevalo, Shaikh B. Iqbal, Beth Mutai, Mohammed Mohsin, Scott Tighe, Sylvie Collin, Yoshitaka Saito, Wayne Menary, Youping Deng, Lucy Lee, Esmeralda Jiminez, Ayuki Watanabe, Nikos C. Kyrpides, Natasha Mohan, Angelika Pupiec, Dedan Githae, Simone Cawthorne, Jonathan A. Eisen, Tomoki Iwashiro, Chiaki Homma, Thomas Saw Aung, Laura Molina, Marcus H. Y. Leung, Ophélie Da Silva, Yan Ling Wong, Hosna Noorzi, Mario Moreno, Alina Butova, Leming Shi, Brian W. Wong, Sarah S. Jackson, Moses Lin, Annabelle Meagher, Pujita Das, Catherine Burke, Mitsuki Ota, Maria Domenica Moccia, Nicolas Sprinsky, Catherine E. Pugh, David C. Green, Fazlina Fauzi, Erdenetsetseg Batdelger, Annie Geiger, Valeria Ventorino, Tolulope Oluwadare, Delisia Cuebas, Catalina Truong, Leonardo Posada, Michael Angelov, Tathiane M. Malta, Amanda Ng, Francesca Nadalin, Arya Hawkins-Zafarnia, Yuh Shiwa, Athena Mitsios, Milton Ozório Moraes, Manolo Laiola, Kalyn Ali, Jaden J.A. Hastings, Ikuto Saito, Maheen Shakil, Chisato Suzuki, Elena M. Vayndorf, Hubert Rehrauer, Ajay Menon, Kaitlan Russell, Aliyah Shari, Rebecca Smith, Gregorio Iraola, Max Priestman, Alan Briones, Silver A. Wolf, Camila Gonzalez-Poblete, Eleonora De Lazzari, Shirley Chiu, Michelle Ki, Irene Hoxie, Marianne Jaubert, Ayantu Jinfessa, Ryan J. King, Nghiem Xuan Hoan, Jalia Bynoe, Jacob Friedman, Aneisa Ramcharan, Pablo Fresia, Cristina Muñoz, Muhammad Afaq, Anyi Tang, Médine Benchouaia, Isabella Kuniko T. Takenaka, Anastasia Chasapi, Areeg Naeem, Hannah Benisty, Cecilia N. Cossio, Nathalie Hüsser, Mahfuza Sabina, Thais S. Sabedot, JoAnn Jacobs, Camila P. E. de Souza, Manuela Oliveira, Jean-Pierre Bouly, Mariko Usui, Wilson Miranda, Natalia Marciniak, Hiram Caballero, Samuel Weekes, Alexandra B. Graf, Emily Leong, Tatyana Nikolayeva, Dominique Thomas, Charlotte Greselle, Cecilia Salazar, Sreya Ray Chaudhuri, Kevin Becher, Sandra Roth, Ryusei Miura, Kari Oline Bøifot, Dimitri Manoir, Oliver Toth, Chandrima Bhattacharya, Manuel Perez, Isha Lamba, Takafumi Tsurumaki, Timothy D. Read, Anna-Lena M. Schinke, Ryan Sankar, Le Huu Song, Narasimha Rao Nedunuri, Emmanuel Dias-Neto, Ana Flávia Costa, Adiell Melamed, Christelle Desnues, Natalie R. Davidson, Aaron E. Darling, Hyung Jun Kim, Josephine Galipon, Jacqueline Orrego, Dimitar Vassilev, Michael Huber, Nur Hazlin Hazrin-Chong, Gaston H. Gonnet, Kaymisha Knights, Osman U. Sezerman, Dmitry Meleshko, Eunice Thambiraja, Jingcheng Yang, Aubin Fleiss, Gloria Nguyen, Katelyn Jackson, Nuria Aventin, Stephanie L. Hyland, Andrea Hässig, Catharine Aquino, Simona Lysakova, Israel O. Osuolale, Kasia Sluzek, Rania Siam, Alina Frolova, Samuel Hernandez, Yui Him Lo, Bazartseren Boldgiv, Ben Young, Maryna Korshevniuk, Majelia Ampadu, Yuk Man Tang, Amanda L. Muehlbauer, Sade Thomas, Gabriel Figueroa, Alexis Rivera, Lisbeth Pineda, Alexandra Dutan, Jennifer M. Tran, Chris K. Deng, Vedbar S. Khadka, Paola Florez de Sessions, Elizabeth Humphries, Hugues Richard, Hiba Naveed, Nora C. Toussaint, Mahshid Khavari, Maria del Mar Vivanco Ruiz, Antonin Thiébaut, Nicolás Rascovan, Marius Dybwad, Orhan Özcan, Lawrence Kwong, David Danko, Shaira Khan, Andrea Tassinari, Silvia Beurmann, Tsoi Ying Lai, Nanami Kubota, Tieliu Shi, Diana Chicas, Evan E. Afshin, Hirokazu Yano, Jonas Krebs, Mayuko Nakagawa, Hyun Jung Lee, Irene González Navarrete, Rachid Ounit, Lucia E. Alvarado-Arnez, Masaki Nasu, Allison Chan, Harilanto Andrianjakarivony, Jennifer Amachee, Mahdi Taye, Wan Chiew Ng, Kathryn O’Brien, Shino Ishikawa, Tristan Bitard-Feildel, Sora Takagi, Felix Hartkopf, Niamh B. O’Hara, Marcos A. S. Fonseca, Subhamitra Pakrashi, Amrit Kaur, Eva Hell, Patricia Vera-Wolf, Naimah Munim, Luiza Ferreira de Araújo, Mizuki Igarashi, Brianna Pompa-Hogan, Alessandra Carbone, Anne-Sophie Benoiston, Eric Helfrich, Michael A. Suarez-Villamil, Omar O. Abudayyeh, Natasha Abdullah, Jaime J. Fuentes, Juan Carlos Forero, Tetiana Yeskova, Denis Bertrand, Sambhawa Priya, Denisse Maldonado, Agier Nicolas, Ana Valeria B Castro, Starr Chatziefthimiou, André Kahles, Aaishah Francis, Fernanda Arredondo, Emilio Tarcitano, Irvind Buttar, Alex Alexiev, Jennifer Molinet, Sarah Shalaby, Itunu A. Oluwadare, Jason Sperry, Katrin Bakhl, Ana M. Cañas, Sofia Ahsanuddin, Miar Elaskandrany, Elodie Laine, Sven Bönigk, Johannes Werner, Stephen Eduard Boja Ruiz, Gargi Dayama, Paulina Buczansla, Brandon Valentine, Bharath Prithiviraj, Toni Bode, Stas Zubenko, Jake Cohen, Guilllaume Jospin, Zulena Saravi, Per O. Ljungdahl, Inderjit Kaur, Mauricio Moldes, Giuseppe KoLoMonaco, Denise Syndercombe Court, Sonia Bouchard, Sonia Losim, Sookwon Moon, Heba Shaaban, Suraj Patel, Sibo Zhu, Sarh Aly, Arif Asyraf Md Supie, LaShonda Dorsey, Juan Guerra, François Baudon, Rantimi A. Olawoyin, Alexia Bordigoni, Iqra Faiz, Mathilde Garcia, Gabriella Mason-Buck, María Gabriela Portilla, Niranjan Nagarajan, Fumie Takahara, Nancy Merino, Watson Andrew, Gina Kim, Yuma Sato, Hyenah Shim, Marie-Laure Jerier, Affifah Saadah Ahmad Kassim, Katerina Kuchin, Daniel Butler, Paweł P. Łabaj, Nadezhda Kobko-Litskevitch, Emmanuel F. Mongodin, Yuto Togashi, Paula Rodríguez, Pilar Lopez Hernandez, Xiaoqing Chen, Maria A. Sierra, Olga Nikolayeva, Manon Loubens, Colleen Conger, Hikaru Shirahata, Chenhao Li, Timothy Donahoe, Youngja Park, Lucia Elena Alvarado Arnez, Salama Chaker, Francisco Chavez, Alessandra Breschi, Jorge L. Sanchez, Kaung Myat San, Nayra Aguilar Rojas, Marcos Abraao, Kai Sasaki, Bryan Nazario, Olena Yemets, Klas I. Udekwu, Lynn M. Schriml, Anisia Peters, Aliaksei Holik, Mark Hernandez, Emile Faure, Malay Bhattacharyya, Josef W. Moser, Núria Andreu Somavilla, María Mercedes Zambrano, Kannan Rajendran, Gabriela E. Albuquerque, Tao Qing, Kazutoshi Tsuda, Ymke De Jong, Princess Osma, Mayra Arauco Livia, Javier Quilez Oliete, Carl Chrispin, Hyun Woo Joo, Ingrid Lafontaine, Nala An, Seisuke Sato, Felipe Segato Dezem, Andrew Maltez Thomas, Alexandre Desert, Xiao Wen Cai, O. Osuolale, Jun Wu, Coral Pardo-Esté, Courtney Robinson, Yuri Matsuzaki, Marina Nieto-Caballero, Cem Meydan, Ralph Schlapbach, Mark Menor, Sofia Castro, Rachel Kwong, Brittany Blyther, Olexandr Lykhenko, Jason R. Schriml, Christian Brion, Jenessa Orpilla, Juan A. Ugalde, Elsy Mankah Ngwa, Álvaro Aranguren, Lauren Mak, Matías Giménez, Ashanti Narce, Torsten Semmler, Stefan I. Tsonev, Abdollahi Nika, Katherine E. Dahlhausen, Monika Devi, Gunnar Rätsch, Oasima Muner, Carla Bello, Muhammad Al-Fath Amran, Anyelic Rosario, Melissa Ortega, Andrea Patrignani, Ante Peros, Elias McComb, Ryo Sato, Ireen Alam, Clara N. Dias, Soma Tanaka, Dayana Calderon, Ran Blekhman, Mathilde Mignotte, Alicia Boyd, Jochen Hecht, Thomas Neff, Xinzhao Tong, Josue Alicea, Kiara Olmeda, Sonia Marinovic, Carme Arnan, Kohei Ito, Samantha L. Goldman, Marianna S. Serpa, Renee Richer, Kaisei Sato, Jordana M. Silva, Akash Keluth Chavan, Sangwan Kim, Laís Pereira Ferreira, Sophie Vacant, Nowshin Sayara, Haruo Suzuki, Madeline Leahy, Juan C. Severyn, Sierra Vincent, Masaru Tomita, Maliha Mamun, Lucinda B. Davenport, Gabriella Oken, Dagmara Lewandowska, Gustavo Adolfo Malca Salas, Andrii Kuklin, Tyler Wong, Charlie Feigin, Eric Minwei Liu, Sonia L. Ghose, Daniela Bezdan, Antonietta La Storia, Juan P. Escalera-Antezana, Nuno Rufino de Sousa, Samuel M. Gerner, Weill Cornell Medicine [New York], Icahn School of Medicine at Mount Sinai [New York] (MSSM), Genome Institute of Singapore (GIS), Centre for Genomic Regulation [Barcelona] (CRG), Universitat Pompeu Fabra [Barcelona] (UPF)-Centro Nacional de Analisis Genomico [Barcelona] (CNAG), Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology [Zürich] (ETH Zürich), Lawrence Berkeley National Laboratory [Berkeley] (LBNL), AUTRES, Massachusetts Institute of Technology (MIT), Indian Statistical Institute [Kolkata], University of Minnesota System, Universidad Andrés Bello [Santiago] (UNAB), California State University [Sacramento], University of Naples Federico II, University of Hawaii, Institut méditerranéen d'océanologie (MIO), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS)-Université de Toulon (UTLN), Medical Genomics Group, University College of London [London] (UCL)-UCL Cancer Institute, Norwegian Defence Research Establishment (FFI), Lund University [Lund], Institute of Molecular Biology and Genetics of National Academy of Sciences of Ukraine, University of Vienna [Vienna], King‘s College London, University of Colorado [Boulder], Institut Pasteur de Montevideo, Réseau International des Instituts Pasteur (RIIP), Institut Pasteur Korea - Institut Pasteur de Corée, Fudan University [Shanghai], City University of Hong Kong [Hong Kong] (CUHK), Stockholm University, University of Maryland School of Medicine, University of Maryland System, Fundação Oswaldo Cruz (FIOCRUZ), University of São Paulo (USP), Instituto de Patologia e Imunologia Molecular da Universidade do Porto (IPATIMUP), Barcelona Institute of Science and Technology (BIST), Elizade University, Acibadem Mehmet Ali Aydınlar University, Paléogénomique microbienne - Microbial paleogenomics, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Sorbonne Université (SU), Robert Koch Institute [Berlin] (RKI), East China Normal University [Shangaï] (ECNU), Cairo University, Vietnamese-German Center for Medical Research, Keio University, Université du Vermont, Universidad del Desarrollo, University of Sofia, University of Alaska [Fairbanks] (UAF), Universitätsklinikum Tübingen - University Hospital of Tübingen, Eberhard Karls Universität Tübingen = Eberhard Karls University of Tuebingen, Corporación Corpogen-Research Center, Biologie Computationnelle et Quantitative = Laboratory of Computational and Quantitative Biology (LCQB), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Paris Seine (IBPS), Sorbonne Université (SU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Weill Cornell Medicine [Cornell University], Cornell University [New York], University of Naples Federico II = Università degli studi di Napoli Federico II, Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Toulon (UTLN)-Centre National de la Recherche Scientifique (CNRS), Fundação Oswaldo Cruz / Oswaldo Cruz Foundation (FIOCRUZ), Universidade de São Paulo = University of São Paulo (USP), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Софийски университет = Sofia University, Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Universidad Andrés Bello - UNAB (CHILE), Acibadem University Dspace, Danko, D., Bezdan, D., Afshin, E. E., Ahsanuddin, S., Bhattacharya, C., Butler, D. J., Chng, K. R., Donnellan, D., Hecht, J., Jackson, K., Kuchin, K., Karasikov, M., Lyons, A., Mak, L., Meleshko, D., Mustafa, H., Mutai, B., Neches, R. Y., Ng, A., Nikolayeva, O., Nikolayeva, T., Png, E., Ryon, K. A., Sanchez, J. L., Shaaban, H., Sierra, M. A., Thomas, D., Young, B., Abudayyeh, O. O., Alicea, J., Bhattacharyya, M., Blekhman, R., Castro-Nallar, E., Canas, A. M., Chatziefthimiou, A. D., Crawford, R. W., De Filippis, F., Deng, Y., Desnues, C., Dias-Neto, E., Dybwad, M., Elhaik, E., Ercolini, D., Frolova, A., Gankin, D., Gootenberg, J. S., Graf, A. B., Green, D. C., Hajirasouliha, I., Hastings, J. J. A., Hernandez, M., Iraola, G., Jang, S., Kahles, A., Kelly, F. J., Knights, K., Kyrpides, N. C., Labaj, P. P., Lee, P. K. H., Leung, M. H. Y., Ljungdahl, P. O., Mason-Buck, G., Mcgrath, K., Meydan, C., Mongodin, E. F., Moraes, M. O., Nagarajan, N., Nieto-Caballero, M., Noushmehr, H., Oliveira, M., Ossowski, S., Osuolale, O. O., Ozcan, O., Paez-Espino, D., Rascovan, N., Richard, H., Ratsch, G., Schriml, L. M., Semmler, T., Sezerman, O. U., Shi, L., Shi, T., Siam, R., Song, L. H., Suzuki, H., Court, D. S., Tighe, S. W., Tong, X., Udekwu, K. I., Ugalde, J. A., Valentine, B., Vassilev, D. I., Vayndorf, E. M., Velavan, T. P., Wu, J., Zambrano, M. M., Zhu, J., Zhu, S., Mason, C. E., Abdullah, N., Abraao, M., Adel, A. -H., Afaq, M., Al-Quaddoomi, F. S., Alam, I., Albuquerque, G. E., Alexiev, A., Ali, K., Alvarado-Arnez, L. E., Aly, S., Amachee, J., Amorim, M. G., Ampadu, M., Amran, M. A. -F., An, N., Andrew, W., Andrianjakarivony, H., Angelov, M., Antelo, V., Aquino, C., Aranguren, A., Araujo, L. F., Vasquez Arevalo, H. F., Arevalo, J., Arnan, C., Alvarado Arnez, L. E., Arredondo, F., Arthur, M., Asenjo, F., Aung, T. S., Auvinet, J., Aventin, N., Ayaz, S., Baburyan, S., Bakere, A. -M., Bakhl, K., Bartelli, T. F., Batdelger, E., Baudon, F., Becher, K., Bello, C., Benchouaia, M., Benisty, H., Benoiston, A. -S., Benson, J., Benitez, D., Bernardes, J., Bertrand, D., Beurmann, S., Bitard-Feildel, T., Bittner, L., Black, C., Blanc, G., Blyther, B., Bode, T., Boeri, J., Boldgiv, B., Bolzli, K., Bordigoni, A., Borrelli, C., Bouchard, S., Bouly, J. -P., Boyd, A., Branco, G. P., Breschi, A., Brindefalk, B., Brion, C., Briones, A., Buczansla, P., Burke, C. M., Burrell, A., Butova, A., Buttar, I., Bynoe, J., Bonigk, S., Boifot, K. O., Caballero, H., Cai, X. W., Calderon, D., Cantillo, A., Carbajo, M., Carbone, A., Cardenas, A., Carrillo, K., Casalot, L., Castro, S., Castro, A. V., Castro, A., Castro, A. V. B., Cawthorne, S., Cedillo, J., Chaker, S., Chalangal, J., Chan, A., Chasapi, A. I., Chatziefthimiou, S., Chaudhuri, S. R., Chavan, A. K., Chavez, F., Chem, G., Chen, X., Chen, M., Chen, J. -W., Chernomoretz, A., Chettouh, A., Cheung, D., Chicas, D., Chiu, S., Choudhry, H., Chrispin, C., Ciaramella, K., Cifuentes, E., Cohen, J., Coil, D. A., Collin, S., Conger, C., Conte, R., Corsi, F., Cossio, C. N., Costa, A. F., Cuebas, D., D'Alessandro, B., Dahlhausen, K. E., Darling, A. E., Das, P., Davenport, L. B., David, L., Davidson, N. R., Dayama, G., Delmas, S., Deng, C. K., Dequeker, C., Desert, A., Devi, M., Dezem, F. S., Dias, C. N., Donahoe, T. R., Dorado, S., Dorsey, L., Dotsenko, V., Du, S., Dutan, A., Eady, N., Eisen, J. A., Elaskandrany, M., Epping, L., Escalera-Antezana, J. P., Ettinger, C. L., Faiz, I., Fan, L., Farhat, N., Faure, E., Fauzi, F., Feigin, C., Felice, S., Ferreira, L. P., Figueroa, G., Fleiss, A., Flores, D., Velasco Flores, J. L., Fonseca, M. A. S., Foox, J., Forero, J. C., Francis, A., French, K., Fresia, P., Friedman, J., Fuentes, J. J., Galipon, J., Garcia, M., Garcia, L., Garcia, C., Geiger, A., Gerner, S. M., Ghose, S. L., Giang, D. P., Gimenez, M., Giovannelli, D., Githae, D., Gkotzis, S., Godoy, L., Goldman, S., Gonnet, G. H., Gonzalez, J., Gonzalez, A., Gonzalez-Poblete, C., Gray, A., Gregory, T., Greselle, C., Guasco, S., Guerra, J., Gurianova, N., Haehr, W., Halary, S., Hartkopf, F., Hawkins-Zafarnia, A., Hazrin-Chong, N. H., Helfrich, E., Hell, E., Henry, T., Hernandez, S., Hernandez, P. L., Hess-Homeier, D., Hittle, L. E., Hoan, N. X., Holik, A., Homma, C., Hoxie, I., Huber, M., Humphries, E., Hyland, S., Hassig, A., Hausler, R., Husser, N., Petit, R. A., Iderzorig, B., Igarashi, M., Iqbal, S. B., Ishikawa, S., Ishizuka, S., Islam, S., Islam, R., Ito, K., Ito, S., Ito, T., Ivankovic, T., Iwashiro, T., Jackson, S., Jacobs, J., James, M., Jaubert, M., Jerier, M. -L., Jiminez, E., Jinfessa, A., De Jong, Y., Joo, H. W., Jospin, G., Kajita, T., Ahmad Kassim, A. S., Kato, N., Kaur, A., Kaur, I., de Souza Gomes Kehdy, F., Khadka, V. S., Khan, S., Khavari, M., Ki, M., Kim, G., Kim, H. J., Kim, S., King, R. J., Kolomonaco, G., Koag, E., Kobko-Litskevitch, N., Korshevniuk, M., Kozhar, M., Krebs, J., Kubota, N., Kuklin, A., Kumar, S. S., Kwong, R., Kwong, L., Lafontaine, I., Lago, J., Lai, T. Y., Laine, E., Laiola, M., Lakhneko, O., Lamba, I., de Lamotte, G., Lannes, R., De Lazzari, E., Leahy, M., Lee, H., Lee, Y., Lee, L., Lemaire, V., Leong, E., Lewandowska, D., Li, C., Liang, W., Lin, M., Lisboa, P., Litskevitch, A., Liu, E. M., Liu, T., Livia, M. A., Lo, Y. H., Losim, S., Loubens, M., Lu, J., Lykhenko, O., Lysakova, S., Mahmoud, S., Majid, S. A., Makogon, N., Maldonado, D., Mallari, K., Malta, T. M., Mamun, M., Manoir, D., Marchandon, G., Marciniak, N., Marinovic, S., Marques, B., Mathews, N., Matsuzaki, Y., Matthys, V., May, M., Mccomb, E., Meagher, A., Melamed, A., Menary, W., Mendez, K. N., Mendez, A., Mendy, I. M., Meng, I., Menon, A., Menor, M., Meoded, R., Merino, N., Miah, K., Mignotte, M., Miketic, T., Miranda, W., Mitsios, A., Miura, R., Miyake, K., Moccia, M. D., Mohan, N., Mohsin, M., Moitra, K., Moldes, M., Molina, L., Molinet, J., Molomjamts, O. -E., Moniruzzaman, E., Moon, S., de Oliveira Moraes, I., Moreno, M., Mosella, M. S., Moser, J. W., Mozsary, C., Muehlbauer, A. L., Muner, O., Munia, M., Munim, N., Muscat, M., Mustac, T., Munoz, C., Nadalin, F., Naeem, A., Nagy-Szakal, D., Nakagawa, M., Narce, A., Nasu, M., Navarrete, I. G., Naveed, H., Nazario, B., Nedunuri, N. R., Neff, T., Nesimi, A., Ng, W. C., Ng, S., Nguyen, G., Ngwa, E., Nicolas, A., Nicolas, P., Nika, A., Noorzi, H., Nosrati, A., Nunes, D. N., O'Brien, K., O'Hara, N. B., Oken, G., Olawoyin, R. A., Oliete, J. Q., Olmeda, K., Oluwadare, T., Oluwadare, I. A., Ordioni, N., Orpilla, J., Orrego, J., Ortega, M., Osma, P., Osuolale, I. O., Osuolale, O. M., Ota, M., Oteri, F., Oto, Y., Ounit, R., Ouzounis, C. A., Pakrashi, S., Paras, R., Pardo-Este, C., Park, Y. -J., Pastuszek, P., Patel, S., Pathmanathan, J., Patrignani, A., Perez, M., Peros, A., Persaud, S., Peters, A., Phillips, A., Pineda, L., Pizzi, M. P., Plaku, A., Pompa-Hogan, B., Portilla, M. G., Posada, L., Priestman, M., Prithiviraj, B., Priya, S., Pugdeethosal, P., Pugh, C. E., Pulatov, B., Pupiec, A., Pyrshev, K., Qing, T., Rahiel, S., Rahmatulloev, S., Rajendran, K., Ramcharan, A., Ramirez-Rojas, A., Rana, S., Ratnanandan, P., Read, T. D., Rehrauer, H., Richer, R., Rivera, A., Rivera, M., Robertiello, A., Robinson, C., Rodriguez, P., Rojas, N. A., Roldan, P., Rosario, A., Roth, S., Ruiz, M., Boja Ruiz, S. E., Russell, K., Rybak, M., Sabedot, T. S., Sabina, M., Saito, I., Saito, Y., Malca Salas, G. A., Salazar, C., San, K. M., Sanchez, J., Sanchir, K., Sankar, R., de Souza Santos, P. T., Saravi, Z., Sasaki, K., Sato, Y., Sato, M., Sato, S., Sato, R., Sato, K., Sayara, N., Schaaf, S., Schacher, O., Schinke, A. -L. M., Schlapbach, R., Schori, C., Schriml, J. R., Segato, F., Sepulveda, F., Serpa, M. S., De Sessions, P. F., Severyn, J. C., Shakil, M., Shalaby, S., Shari, A., Shim, H., Shirahata, H., Shiwa, Y., Da Silva, O., Silva, J. M., Simon, G., Singh, S. K., Sluzek, K., Smith, R., So, E., Andreu Somavilla, N., Sonohara, Y., Rufino de Sousa, N., Souza, C., Sperry, J., Sprinsky, N., Stark, S. G., La Storia, A., Suganuma, K., Suliman, H., Sullivan, J., Supie, A. A. M., Suzuki, C., Takagi, S., Takahara, F., Takahashi, N., Takahashi, K., Takeda, T., Takenaka, I. K., Tanaka, S., Tang, A., Man Tang, Y., Tarcitano, E., Tassinari, A., Taye, M., Terrero, A., Thambiraja, E., Thiebaut, A., Thomas, S., Thomas, A. M., Togashi, Y., Togashi, T., Tomaselli, A., Tomita, M., Tomita, I., Toth, O., Toussaint, N. C., Tran, J. M., Truong, C., Tsonev, S. I., Tsuda, K., Tsurumaki, T., Tuz, M., Tymoshenko, Y., Urgiles, C., Usui, M., Vacant, S., Vann, L. E., Velter, F., Ventorino, V., Vera-Wolf, P., Vicedomini, R., Suarez-Villamil, M. A., Vincent, S., Vivancos-Koopman, R., Wan, A., Wang, C., Warashina, T., Watanabe, A., Weekes, S., Werner, J., Westfall, D., Wieler, L. H., Williams, M., Wolf, S. A., Wong, B., Wong, Y. L., Wong, T., Wright, R., Wunderlin, T., Yamanaka, R., Yang, J., Yano, H., Yeh, G. C., Yemets, O., Yeskova, T., Yoshikawa, S., Zafar, L., Zhang, Y., Zhang, S., Zhang, A., Zheng, Y., and Zubenko, S.

Subjects
Urban Population, Drug Resistance, Sequence assembly, Microbiologia, microbiome, global health, computer.software_genre, Medical and Health Sciences, shotgun sequencing, BGC, 0302 clinical medicine, Databases, Genetic, 11. Sustainability, Global health, AMR, 11 Medical and Health Sciences, ComputingMilieux_MISCELLANEOUS, 0303 health sciences, built environment, metagenome, antimicrobial resistance, NGS, de novo assembly, biology, Shotgun sequencing, Microbiota, built Environment, Bacterial, Biodiversity, Biological Sciences, 3. Good health, [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology, Infection, Biotechnology, Geospatial analysis, [SDV.BID]Life Sciences [q-bio]/Biodiversity, Article, General Biochemistry, Genetics and Molecular Biology, Databases, 03 medical and health sciences, Antibiotic resistance, Genetic, Drug Resistance, Bacterial, International MetaSUB Consortium, Genetics, Humans, Microbiome, 030304 developmental biology, Human Genome, 06 Biological Sciences, 15. Life on land, biology.organism_classification, Resistènica als medicaments antiinfecciosos, SAÚDE PÚBLICA, Genòmica, 13. Climate action, Evolutionary biology, Metagenomics, Antimicrobial Resistance, [SDE.BE]Environmental Sciences/Biodiversity and Ecology, computer, 030217 neurology & neurosurgery, Archaea, Developmental Biology
Abstract

Summary We present a global atlas of 4,728 metagenomic samples from mass-transit systems in 60 cities over 3 years, representing the first systematic, worldwide catalog of the urban microbial ecosystem. This atlas provides an annotated, geospatial profile of microbial strains, functional characteristics, antimicrobial resistance (AMR) markers, and genetic elements, including 10,928 viruses, 1,302 bacteria, 2 archaea, and 838,532 CRISPR arrays not found in reference databases. We identified 4,246 known species of urban microorganisms and a consistent set of 31 species found in 97% of samples that were distinct from human commensal organisms. Profiles of AMR genes varied widely in type and density across cities. Cities showed distinct microbial taxonomic signatures that were driven by climate and geographic differences. These results constitute a high-resolution global metagenomic atlas that enables discovery of organisms and genes, highlights potential public health and forensic applications, and provides a culture-independent view of AMR burden in cities., Graphical abstract, Highlights • Cities possess a consistent “core” set of non-human microbes • Urban microbiomes echo important features of cities and city-life • Antimicrobial resistance genes are widespread in cities • Cities contain many novel bacterial and viral species, This systematic, worldwide catalog of urban microbiomes represents a metagenomic atlas important for understanding the ecology, virulence, and antibiotic resistance of city-specific microbial communities.

Published
2021

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