Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance

Patrick Munk; Christian Brinch; Frederik Duus Møller; Thomas N. Petersen; Rene S. Hendriksen; Anne Mette Seyfarth; Jette S. Kjeldgaard; Christina Aaby Svendsen; Bram van Bunnik; Fanny Berglund; Artan Bego; Pablo Power; Catherine Rees; Dionisia Lambrinidis; Elizabeth Heather Jakobsen Neilson; Karen Gibb; Kris Coventry; Peter Collignon; Susan Cassar; Franz Allerberger; Anowara Begum; Zenat Zebin Hossain; Carlon Worrell; Olivier Vandenberg; Ilse Pieters; Dougnon Tamègnon Victorien; Angela Daniela Salazar Gutierrez; Freddy Soria; Vesna Rudić Grujić; Nataša Mazalica; Teddie O. Rahube; Carlos Alberto Tagliati; Dalia Rodrigues; Guilherme Oliveira; Larissa Camila Ribeiro de Souza; Ivan Ivanov; Bonkoungou Isidore Juste; Traoré Oumar; Thet Sopheak; Yith Vuthy; Antoinette Ngandijo; Ariane Nzouankeu; Ziem A.Abah Jacques Olivier; Christopher K. Yost; Lisbeth Truelstrup Hansen; Pernille Erland Jensen; Sivachandran Parimannan; Yaovi Mahuton Gildas Hounmanou; Jens Thomsen; Frank M. Aarestrup; Global Sewage Surveillance Consortium

doi:10.1038/s41467-022-34312-7

Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance

Patrick Munk^*, Christian Brinch, Frederik Duus Møller, Thomas N. Petersen, Rene S. Hendriksen, Anne Mette Seyfarth, Jette S. Kjeldgaard, Christina Aaby Svendsen, Bram van Bunnik, Fanny Berglund, Artan Bego, Pablo Power, Catherine Rees, Dionisia Lambrinidis, Elizabeth Heather Jakobsen Neilson, Karen Gibb, Kris Coventry, Peter Collignon, Susan Cassar, Franz AllerbergerAnowara Begum, Zenat Zebin Hossain, Carlon Worrell, Olivier Vandenberg, Ilse Pieters, Dougnon Tamègnon Victorien, Angela Daniela Salazar Gutierrez, Freddy Soria, Vesna Rudić Grujić, Nataša Mazalica, Teddie O. Rahube, Carlos Alberto Tagliati, Dalia Rodrigues, Guilherme Oliveira, Larissa Camila Ribeiro de Souza, Ivan Ivanov, Bonkoungou Isidore Juste, Traoré Oumar, Thet Sopheak, Yith Vuthy, Antoinette Ngandijo, Ariane Nzouankeu, Ziem A.Abah Jacques Olivier, Christopher K. Yost, Lisbeth Truelstrup Hansen, Pernille Erland Jensen, Sivachandran Parimannan, Yaovi Mahuton Gildas Hounmanou, Jens Thomsen, Frank M. Aarestrup, Global Sewage Surveillance Consortium

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

135 Citationer (Scopus)

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Abstract

Antimicrobial resistance (AMR) is a major threat to global health. Understanding the emergence, evolution, and transmission of individual antibiotic resistance genes (ARGs) is essential to develop sustainable strategies combatting this threat. Here, we use metagenomic sequencing to analyse ARGs in 757 sewage samples from 243 cities in 101 countries, collected from 2016 to 2019. We find regional patterns in resistomes, and these differ between subsets corresponding to drug classes and are partly driven by taxonomic variation. The genetic environments of 49 common ARGs are highly diverse, with most common ARGs carried by multiple distinct genomic contexts globally and sometimes on plasmids. Analysis of flanking sequence revealed ARG-specific patterns of dispersal limitation and global transmission. Our data furthermore suggest certain geographies are more prone to transmission events and should receive additional attention.

Originalsprog	Engelsk
Artikelnummer	7251
Tidsskrift	Nature Communications
Vol/bind	13
Antal sider	16
ISSN	2041-1723
DOI	https://doi.org/10.1038/s41467-022-34312-7
Status	Udgivet - 2022

Bibliografisk note

Correction: 10.1038/s41467-023-35890-w
Publisher Copyright:
© 2022, The Author(s).

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10.1038/s41467-022-34312-7Licens: CC BY

FulltextForlagets udgivne version, 4,13 MBLicens: CC BY

Citationsformater

Munk, P., Brinch, C., Møller, F. D., Petersen, T. N., Hendriksen, R. S., Seyfarth, A. M., Kjeldgaard, J. S., Svendsen, C. A., van Bunnik, B., Berglund, F., Bego, A., Power, P., Rees, C., Lambrinidis, D., Neilson, E. H. J., Gibb, K., Coventry, K., Collignon, P., Cassar, S., ... Global Sewage Surveillance Consortium (2022). Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance. Nature Communications, 13, [7251]. https://doi.org/10.1038/s41467-022-34312-7

Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance. / Munk, Patrick; Brinch, Christian; Møller, Frederik Duus; Petersen, Thomas N.; Hendriksen, Rene S.; Seyfarth, Anne Mette; Kjeldgaard, Jette S.; Svendsen, Christina Aaby; van Bunnik, Bram; Berglund, Fanny; Bego, Artan; Power, Pablo; Rees, Catherine; Lambrinidis, Dionisia; Neilson, Elizabeth Heather Jakobsen; Gibb, Karen; Coventry, Kris; Collignon, Peter; Cassar, Susan; Allerberger, Franz; Begum, Anowara; Hossain, Zenat Zebin; Worrell, Carlon; Vandenberg, Olivier; Pieters, Ilse; Victorien, Dougnon Tamègnon; Gutierrez, Angela Daniela Salazar; Soria, Freddy; Grujić, Vesna Rudić; Mazalica, Nataša; Rahube, Teddie O.; Tagliati, Carlos Alberto; Rodrigues, Dalia; Oliveira, Guilherme; de Souza, Larissa Camila Ribeiro; Ivanov, Ivan; Juste, Bonkoungou Isidore; Oumar, Traoré; Sopheak, Thet; Vuthy, Yith; Ngandijo, Antoinette; Nzouankeu, Ariane; Olivier, Ziem A.Abah Jacques; Yost, Christopher K.; Hansen, Lisbeth Truelstrup; Jensen, Pernille Erland; Parimannan, Sivachandran; Hounmanou, Yaovi Mahuton Gildas; Thomsen, Jens; Aarestrup, Frank M.; Global Sewage Surveillance Consortium.

I: Nature Communications, Bind 13, 7251, 2022.

Publikation: Bidrag til tidsskrift › Tidsskriftartikel › Forskning › peer review

Munk, P, Brinch, C, Møller, FD, Petersen, TN, Hendriksen, RS, Seyfarth, AM, Kjeldgaard, JS, Svendsen, CA, van Bunnik, B, Berglund, F, Bego, A, Power, P, Rees, C, Lambrinidis, D, Neilson, EHJ, Gibb, K, Coventry, K, Collignon, P, Cassar, S, Allerberger, F, Begum, A, Hossain, ZZ, Worrell, C, Vandenberg, O, Pieters, I, Victorien, DT, Gutierrez, ADS, Soria, F, Grujić, VR, Mazalica, N, Rahube, TO, Tagliati, CA, Rodrigues, D, Oliveira, G, de Souza, LCR, Ivanov, I, Juste, BI, Oumar, T, Sopheak, T, Vuthy, Y, Ngandijo, A, Nzouankeu, A, Olivier, ZAAJ, Yost, CK, Hansen, LT, Jensen, PE, Parimannan, S, Hounmanou, YMG, Thomsen, J, Aarestrup, FM & Global Sewage Surveillance Consortium 2022, 'Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance', Nature Communications, bind 13, 7251. https://doi.org/10.1038/s41467-022-34312-7

Munk, Patrick ; Brinch, Christian ; Møller, Frederik Duus ; Petersen, Thomas N. ; Hendriksen, Rene S. ; Seyfarth, Anne Mette ; Kjeldgaard, Jette S. ; Svendsen, Christina Aaby ; van Bunnik, Bram ; Berglund, Fanny ; Bego, Artan ; Power, Pablo ; Rees, Catherine ; Lambrinidis, Dionisia ; Neilson, Elizabeth Heather Jakobsen ; Gibb, Karen ; Coventry, Kris ; Collignon, Peter ; Cassar, Susan ; Allerberger, Franz ; Begum, Anowara ; Hossain, Zenat Zebin ; Worrell, Carlon ; Vandenberg, Olivier ; Pieters, Ilse ; Victorien, Dougnon Tamègnon ; Gutierrez, Angela Daniela Salazar ; Soria, Freddy ; Grujić, Vesna Rudić ; Mazalica, Nataša ; Rahube, Teddie O. ; Tagliati, Carlos Alberto ; Rodrigues, Dalia ; Oliveira, Guilherme ; de Souza, Larissa Camila Ribeiro ; Ivanov, Ivan ; Juste, Bonkoungou Isidore ; Oumar, Traoré ; Sopheak, Thet ; Vuthy, Yith ; Ngandijo, Antoinette ; Nzouankeu, Ariane ; Olivier, Ziem A.Abah Jacques ; Yost, Christopher K. ; Hansen, Lisbeth Truelstrup ; Jensen, Pernille Erland ; Parimannan, Sivachandran ; Hounmanou, Yaovi Mahuton Gildas ; Thomsen, Jens ; Aarestrup, Frank M. ; Global Sewage Surveillance Consortium. / Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance. I: Nature Communications. 2022 ; Bind 13.

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title = "Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance",

abstract = "Antimicrobial resistance (AMR) is a major threat to global health. Understanding the emergence, evolution, and transmission of individual antibiotic resistance genes (ARGs) is essential to develop sustainable strategies combatting this threat. Here, we use metagenomic sequencing to analyse ARGs in 757 sewage samples from 243 cities in 101 countries, collected from 2016 to 2019. We find regional patterns in resistomes, and these differ between subsets corresponding to drug classes and are partly driven by taxonomic variation. The genetic environments of 49 common ARGs are highly diverse, with most common ARGs carried by multiple distinct genomic contexts globally and sometimes on plasmids. Analysis of flanking sequence revealed ARG-specific patterns of dispersal limitation and global transmission. Our data furthermore suggest certain geographies are more prone to transmission events and should receive additional attention.",

author = "Patrick Munk and Christian Brinch and M{\o}ller, {Frederik Duus} and Petersen, {Thomas N.} and Hendriksen, {Rene S.} and Seyfarth, {Anne Mette} and Kjeldgaard, {Jette S.} and Svendsen, {Christina Aaby} and {van Bunnik}, Bram and Fanny Berglund and Artan Bego and Pablo Power and Catherine Rees and Dionisia Lambrinidis and Neilson, {Elizabeth Heather Jakobsen} and Karen Gibb and Kris Coventry and Peter Collignon and Susan Cassar and Franz Allerberger and Anowara Begum and Hossain, {Zenat Zebin} and Carlon Worrell and Olivier Vandenberg and Ilse Pieters and Victorien, {Dougnon Tam{\`e}gnon} and Gutierrez, {Angela Daniela Salazar} and Freddy Soria and Gruji{\'c}, {Vesna Rudi{\'c}} and Nata{\v s}a Mazalica and Rahube, {Teddie O.} and Tagliati, {Carlos Alberto} and Dalia Rodrigues and Guilherme Oliveira and {de Souza}, {Larissa Camila Ribeiro} and Ivan Ivanov and Juste, {Bonkoungou Isidore} and Traor{\'e} Oumar and Thet Sopheak and Yith Vuthy and Antoinette Ngandijo and Ariane Nzouankeu and Olivier, {Ziem A.Abah Jacques} and Yost, {Christopher K.} and Hansen, {Lisbeth Truelstrup} and Jensen, {Pernille Erland} and Sivachandran Parimannan and Hounmanou, {Yaovi Mahuton Gildas} and Jens Thomsen and Aarestrup, {Frank M.} and {Global Sewage Surveillance Consortium}",

note = "Correction: 10.1038/s41467-023-35890-w Funding Information: We would like to thank everyone who has helped with sampling, shipping, and the logistics of transporting sewage to Denmark since the beginning of the pilot project including the Drainage Services Department, The Government of the Hong Kong Special Administrative Region. We also want to thank the system administrators of Computerome, for troubleshooting, guidance, and compute resources. A special thanks to the laboratory technicians at DTU who worked hard to receive and treat the incoming sewage and Elena Lavinia Diaconu (IZSLT). Lastly, we would like to acknowledge the Novo Nordisk Foundation (Grant: NNF16OC0021856: Global Surveillance of Antimicrobial Resistance) and the European Union{\textquoteright}s Horizon 2020 research and innovation programme (Grant: 874735) for funding the work. Funding Information: We would like to thank everyone who has helped with sampling, shipping, and the logistics of transporting sewage to Denmark since the beginning of the pilot project including the Drainage Services Department, The Government of the Hong Kong Special Administrative Region. We also want to thank the system administrators of Computerome, for troubleshooting, guidance, and compute resources. A special thanks to the laboratory technicians at DTU who worked hard to receive and treat the incoming sewage and Elena Lavinia Diaconu (IZSLT). Lastly, we would like to acknowledge the Novo Nordisk Foundation (Grant: NNF16OC0021856: Global Surveillance of Antimicrobial Resistance) and the European Union{\textquoteright}s Horizon 2020 research and innovation programme (Grant: 874735) for funding the work. Publisher Copyright: {\textcopyright} 2022, The Author(s).",

year = "2022",

doi = "10.1038/s41467-022-34312-7",

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journal = "Nature Communications",

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T1 - Genomic analysis of sewage from 101 countries reveals global landscape of antimicrobial resistance

AU - Munk, Patrick

AU - Brinch, Christian

AU - Møller, Frederik Duus

AU - Petersen, Thomas N.

AU - Hendriksen, Rene S.

AU - Seyfarth, Anne Mette

AU - Kjeldgaard, Jette S.

AU - Svendsen, Christina Aaby

AU - van Bunnik, Bram

AU - Berglund, Fanny

AU - Bego, Artan

AU - Power, Pablo

AU - Rees, Catherine

AU - Lambrinidis, Dionisia

AU - Neilson, Elizabeth Heather Jakobsen

AU - Gibb, Karen

AU - Coventry, Kris

AU - Collignon, Peter

AU - Cassar, Susan

AU - Allerberger, Franz

AU - Begum, Anowara

AU - Hossain, Zenat Zebin

AU - Worrell, Carlon

AU - Vandenberg, Olivier

AU - Pieters, Ilse

AU - Victorien, Dougnon Tamègnon

AU - Gutierrez, Angela Daniela Salazar

AU - Soria, Freddy

AU - Grujić, Vesna Rudić

AU - Mazalica, Nataša

AU - Rahube, Teddie O.

AU - Tagliati, Carlos Alberto

AU - Rodrigues, Dalia

AU - Oliveira, Guilherme

AU - de Souza, Larissa Camila Ribeiro

AU - Ivanov, Ivan

AU - Juste, Bonkoungou Isidore

AU - Oumar, Traoré

AU - Sopheak, Thet

AU - Vuthy, Yith

AU - Ngandijo, Antoinette

AU - Nzouankeu, Ariane

AU - Olivier, Ziem A.Abah Jacques

AU - Yost, Christopher K.

AU - Hansen, Lisbeth Truelstrup

AU - Jensen, Pernille Erland

AU - Parimannan, Sivachandran

AU - Hounmanou, Yaovi Mahuton Gildas

AU - Thomsen, Jens

AU - Aarestrup, Frank M.

AU - Global Sewage Surveillance Consortium

N1 - Correction: 10.1038/s41467-023-35890-w Funding Information: We would like to thank everyone who has helped with sampling, shipping, and the logistics of transporting sewage to Denmark since the beginning of the pilot project including the Drainage Services Department, The Government of the Hong Kong Special Administrative Region. We also want to thank the system administrators of Computerome, for troubleshooting, guidance, and compute resources. A special thanks to the laboratory technicians at DTU who worked hard to receive and treat the incoming sewage and Elena Lavinia Diaconu (IZSLT). Lastly, we would like to acknowledge the Novo Nordisk Foundation (Grant: NNF16OC0021856: Global Surveillance of Antimicrobial Resistance) and the European Union’s Horizon 2020 research and innovation programme (Grant: 874735) for funding the work. Funding Information: We would like to thank everyone who has helped with sampling, shipping, and the logistics of transporting sewage to Denmark since the beginning of the pilot project including the Drainage Services Department, The Government of the Hong Kong Special Administrative Region. We also want to thank the system administrators of Computerome, for troubleshooting, guidance, and compute resources. A special thanks to the laboratory technicians at DTU who worked hard to receive and treat the incoming sewage and Elena Lavinia Diaconu (IZSLT). Lastly, we would like to acknowledge the Novo Nordisk Foundation (Grant: NNF16OC0021856: Global Surveillance of Antimicrobial Resistance) and the European Union’s Horizon 2020 research and innovation programme (Grant: 874735) for funding the work. Publisher Copyright: © 2022, The Author(s).

PY - 2022

Y1 - 2022

N2 - Antimicrobial resistance (AMR) is a major threat to global health. Understanding the emergence, evolution, and transmission of individual antibiotic resistance genes (ARGs) is essential to develop sustainable strategies combatting this threat. Here, we use metagenomic sequencing to analyse ARGs in 757 sewage samples from 243 cities in 101 countries, collected from 2016 to 2019. We find regional patterns in resistomes, and these differ between subsets corresponding to drug classes and are partly driven by taxonomic variation. The genetic environments of 49 common ARGs are highly diverse, with most common ARGs carried by multiple distinct genomic contexts globally and sometimes on plasmids. Analysis of flanking sequence revealed ARG-specific patterns of dispersal limitation and global transmission. Our data furthermore suggest certain geographies are more prone to transmission events and should receive additional attention.

AB - Antimicrobial resistance (AMR) is a major threat to global health. Understanding the emergence, evolution, and transmission of individual antibiotic resistance genes (ARGs) is essential to develop sustainable strategies combatting this threat. Here, we use metagenomic sequencing to analyse ARGs in 757 sewage samples from 243 cities in 101 countries, collected from 2016 to 2019. We find regional patterns in resistomes, and these differ between subsets corresponding to drug classes and are partly driven by taxonomic variation. The genetic environments of 49 common ARGs are highly diverse, with most common ARGs carried by multiple distinct genomic contexts globally and sometimes on plasmids. Analysis of flanking sequence revealed ARG-specific patterns of dispersal limitation and global transmission. Our data furthermore suggest certain geographies are more prone to transmission events and should receive additional attention.

U2 - 10.1038/s41467-022-34312-7

DO - 10.1038/s41467-022-34312-7

M3 - Journal article

C2 - 36456547

AN - SCOPUS:85143185703

VL - 13

JO - Nature Communications

JF - Nature Communications

SN - 2041-1723

M1 - 7251

ER -