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A global metagenomic map of urban microbiomes and antimicrobial resistance

Research output: Contribution to journalArticlepeer-review

The International MetaSUB Consortium

Original languageEnglish
Pages (from-to)3376-3393.e17
JournalCell
Volume184
Issue number13
DOIs
Published24 Jun 2021

Bibliographical note

Funding Information: We thank these organizations, people, and grants for their support: the Tri-I Program in Computational Biology and Medicine (CBM) funded by NIH grant 1T32GM083937; GitHub; Philip Blood and the Extreme Science and Engineering Discovery Environment (XSEDE), supported by NSF grant number ACI-1548562 and NSF award number ACI-1445606; the WCM SCU and Epigenomics and Genomics Core Facilities; the Vallee Foundation; the WorldQuant Foundation; Igor Tulchinsky; The Pershing Square Sohn Cancer Research Alliance; NASA (NNX14AH50G, NNX17AB26G), the NIH (R01AI151059, R25EB020393, R21AI129851, R35GM138152, U01DA053941); STARR Foundation (I13- 0052); LLS (MCL7001-18, LLS 9238-16, LLS-MCL7001-18); the NSF (1840275); the Bill and Melinda Gates Foundation (OPP1151054); the Alfred P. Sloan Foundation (G-2015-13964); Swiss National Science Foundation grant number 407540_167331; NIH award number UL1TR000457; the US Department of Energy Joint Genome Institute under contract number DE-AC02-05CH11231; the National Energy Research Scientific Computing Center, supported by the Office of Science of the US Department of Energy; Stockholm Health Authority grant SLL 20160933; the Institut Pasteur Korea; an NRF Korea grant (NRF-2014K1A4A7A01074645, 2017M3A9G6068246); the CONICYT Fondecyt Iniciaci?n grants 11140666 and 11160905; the Millennium Science Initiative of the Ministry of Economy, Development and Tourism; government of Chile; Keio University Funds for Individual Research; funds from the Yamagata prefectural government and the city of Tsuruoka; JSPS KAKENHI grant number 20K10436; the bilateral AT-UA collaboration fund (WTZ:UA 02/2019; Ministry of Education and Science of Ukraine, UA:M/84-2019, M/126-2020); Kyiv Academic Univeristy; Ministry of Education and Science of Ukraine project numbers 0118U100290 and 0120U101734; the Spanish Ministry of Economy and Competitiveness; Centro de Excelencia Severo Ochoa 2013?2017; the CERCA Programme / Generalitat de Catalunya; the ?la Caixa? Foundation; the CRG-Novartis-Africa mobility program 2016; TMB Director Eladio De Miguel Sainz; research funds from National Cheng Kung University and the Ministry of Science and Technology; Taiwan (MOST grant number 106-2321-B-006-016); the Weill Cornell Clinical and Translational Science Center (CTSC); CUNY Hunter College; Macaulay Honors College at CUNY; City College of the City University of New York; Cornell University; Columbia University; the Icahn School of Medicine at Mt. Sinai; Rockefeller University; and New York University (NYU). We thank all the volunteers who made sampling NYC possible, Minciencias (project no. 639677758300), CNPq (EDN - 309973/2015-5), the Open Research Fund of Key Laboratory of Advanced Theory and Application in Statistics and Data Science ? MOE, ECNU, the Research Grants Council of Hong Kong through project 11215017, National Key RD Project of China (2018YFE0201603), and Shanghai Municipal Science and Technology Major Project (2017SHZDZX01) (L.S.). Sampling was carried out in compliance with regulations and permissions from local authorities (Azienda Napoletana Mobilit? s.p.a. in Naples, Italy; R?gie des Transports M?tropolitains in Marseille, France; Transmilenio and ANLA permit 1484 in Bogot?, Colombia; Nigerian Railway Corporation (NRC) (Ilorin and Offa Branch) and Kwara Express Transport. MetaSUB Ukraine would like to express gratitude to Kyiv Metro and BioLabTech for the organizational support of the sampling days. We wish to thank all transit authorities that helped with this sampling. Conceptualization, D. Danko, D.B. E.E.A. and C.E.M.; methodology, D. Danko, D.B. S.W.T. J.H. B.M. K.I.U. M.D. S.A. E.D.-N. P.P.L. K.M. N.R. D.J.B. L.M.S. H. Shaaban, K.A.R. J.L.S. H. Suzuki, M.A.S. B.Y. and A.K.; software, D. Danko; formal analysis, D. Danko, D.B. K. Kuchin, L.M. C.B. D.M. M.A.S. A.K. and N.C.K.; data curation, D. Danko, D.B. E.E.A. S.A. C.B. D.J.B. K.R.C. D. Donnellan, J.H. K.J. M.K. A.L. H.M. B.M. R.Y.N. A.N. O.N. T.N. E.P. K.A.R. J.L.S. H. Shaaban, M.A.S. D.T. O.O.A. J.A. M.B. R.B. E.C.-N. A.M.C. A.D.C. R.W.C. F.D.F. Y.D. C.D. E.D.-N. M.D. E.E. D.E. A.F. D.G. J.S.G. D.C.G. I.H. M.H. G.I. S.J. A.K. F.J.K. K. Knights, N.C.K. P.P.L. P.K.H.L. M.H.Y.L. P.O.L. G.M.-B. K.M. C.M. E.F.M. M.O.M. N.N. M.N.-C. H.N. M.O. S.O. O.O.O. O.O. D.P.-E. N.R. H.R. G.R. L.M.S. T. Semmler, O.U.S. L.S. T. Shi, L.H.S. H. Suzuki, D.S.C. S.W.T. X.T. K.I.U. J.A.U. B.V. D.I.V. E.M.V. T.P.V. J.W. M.M.Z. J.Z. S.Z. and C.E.M.; writing ? original draft, D. Danko, D.B. and C.E.M.; writing ? review and editing, all authors have reviewed and approved the manuscript; supervision, C.E.M.; project administration, D. Danko, D.B. E.E.A. K.A.R. B.Y. and C.E.M. 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. Funding Information: We thank these organizations, people, and grants for their support: the Tri-I Program in Computational Biology and Medicine (CBM) funded by NIH grant 1T32GM083937 ; GitHub ; Philip Blood and the Extreme Science and Engineering Discovery Environment (XSEDE), supported by NSF grant number ACI-1548562 and NSF award number ACI-1445606 ; the WCM SCU and Epigenomics and Genomics Core Facilities ; the Vallee Foundation ; the WorldQuant Foundation ; Igor Tulchinsky ; The Pershing Square Sohn Cancer Research Alliance ; NASA ( NNX14AH50G , NNX17AB26G ), the NIH ( R01AI151059 , R25EB020393 , R21AI129851 , R35GM138152 , U01DA053941 ); STARR Foundation ( I13- 0052 ); LLS ( MCL7001-18 , LLS 9238-16 , LLS-MCL7001-18 ); the NSF ( 1840275 ); the Bill and Melinda Gates Foundation ( OPP1151054 ); the Alfred P. Sloan Foundation ( G-2015-13964 ); Swiss National Science Foundation grant number 407540_167331 ; NIH award number UL1TR000457 ; the US Department of Energy Joint Genome Institute under contract number DE-AC02-05CH11231 ; the National Energy Research Scientific Computing Center , supported by the Office of Science of the US Department of Energy ; Stockholm Health Authority grant SLL 20160933 ; the Institut Pasteur Korea ; an NRF Korea grant ( NRF-2014K1A4A7A01074645 , 2017M3A9G6068246 ); the CONICYT Fondecyt Iniciación grants 11140666 and 11160905 ; the Millennium Science Initiative of the Ministry of Economy, Development and Tourism ; government of Chile ; Keio University Funds for Individual Research; funds from the Yamagata prefectural government and the city of Tsuruoka ; JSPS KAKENHI grant number 20K10436 ; the bilateral AT-UA collaboration fund ( WTZ:UA 02/2019 ; Ministry of Education and Science of Ukraine , UA:M/84-2019 , M/126-2020 ); Kyiv Academic Univeristy ; Ministry of Education and Science of Ukraine project numbers 0118U100290 and 0120U101734 ; the Spanish Ministry of Economy and Competitiveness ; Centro de Excelencia Severo Ochoa 2013–2017 ; the CERCA Programme / Generalitat de Catalunya ; the “la Caixa” Foundation ; the CRG-Novartis-Africa mobility program 2016; TMB Director Eladio De Miguel Sainz ; research funds from National Cheng Kung University and the Ministry of Science and Technology ; Taiwan (MOST grant number 106-2321-B-006-016 ); the Weill Cornell Clinical and Translational Science Center (CTSC); CUNY Hunter College ; Macaulay Honors College at CUNY ; City College of the City University of New York ; Cornell University ; Columbia University ; the Icahn School of Medicine at Mt. Sinai ; Rockefeller University ; and New York University (NYU). We thank all the volunteers who made sampling NYC possible, Minciencias (project no. 639677758300 ), CNPq ( EDN - 309973/2015-5 ), the Open Research Fund of Key Laboratory of Advanced Theory and Application in Statistics and Data Science – MOE , ECNU , the Research Grants Council of Hong Kong through project 11215017 , National Key RD Project of China ( 2018YFE0201603 ), and Shanghai Municipal Science and Technology Major Project ( 2017SHZDZX01 ) (L.S.). Sampling was carried out in compliance with regulations and permissions from local authorities (Azienda Napoletana Mobilità s.p.a. in Naples, Italy; Régie des Transports Métropolitains in Marseille, France; Transmilenio and ANLA permit 1484 in Bogotá, Colombia; Nigerian Railway Corporation (NRC) (Ilorin and Offa Branch) and Kwara Express Transport. MetaSUB Ukraine would like to express gratitude to Kyiv Metro and BioLabTech for the organizational support of the sampling days. We wish to thank all transit authorities that helped with this sampling. Publisher Copyright: © 2021 The Author(s) Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

King's Authors

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.

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