Genomic evolution of antimicrobial resistance in Escherichia coli

Pimlapas Leekitcharoenphon; Markus Hans Kristofer Johansson; Patrick Munk; Burkhard Malorny; Magdalena Skarżyńska; Katharina Wadepohl; Gabriel Moyano; Ayla Hesp; Kees T. Veldman; Alex Bossers; Haitske Graveland; Alieda van Essen; Antonio Battisti; Andrea Caprioli; Thomas Blaha; Tine Hald; Hristo Daskalov; Helmut W. Saatkamp; Katharina D.C. Stärk; Roosmarijn E.C. Luiken; Liese Van Gompel; Rasmus Borup Hansen; Jeroen Dewulf; Ana Sofia Ribeiro Duarte; Magdalena Zając; Dariusz Wasyl; Pascal Sanders; Bruno Gonzalez-Zorn; Michael S.M. Brouwer; Jaap A. Wagenaar; Dick J.J. Heederik; Dik Mevius; Frank M. Aarestrup; EFFORT consortium

doi:10.1038/s41598-021-93970-7

Genomic evolution of antimicrobial resistance in Escherichia coli

Pimlapas Leekitcharoenphon^*, Markus Hans Kristofer Johansson, Patrick Munk, Burkhard Malorny, Magdalena Skarżyńska, Katharina Wadepohl, Gabriel Moyano, Ayla Hesp, Kees T. Veldman, Alex Bossers, Haitske Graveland (Member of author collaboration), Alieda van Essen (Member of author collaboration), Antonio Battisti (Member of author collaboration), Andrea Caprioli (Member of author collaboration), Thomas Blaha (Member of author collaboration), Tine Hald (Member of author collaboration), Hristo Daskalov (Member of author collaboration), Helmut W. Saatkamp (Member of author collaboration), Katharina D.C. Stärk (Member of author collaboration), Roosmarijn E.C. Luiken (Member of author collaboration)Liese Van Gompel (Member of author collaboration), Rasmus Borup Hansen (Member of author collaboration), Jeroen Dewulf (Member of author collaboration), Ana Sofia Ribeiro Duarte (Member of author collaboration), Magdalena Zając, Dariusz Wasyl, Pascal Sanders, Bruno Gonzalez-Zorn, Michael S.M. Brouwer, Jaap A. Wagenaar, Dick J.J. Heederik, Dik Mevius, Frank M. Aarestrup, EFFORT consortium

^*Corresponding author for this work

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Abstract

The emergence of antimicrobial resistance (AMR) is one of the biggest health threats globally. In addition, the use of antimicrobial drugs in humans and livestock is considered an important driver of antimicrobial resistance. The commensal microbiota, and especially the intestinal microbiota, has been shown to have an important role in the emergence of AMR. Mobile genetic elements (MGEs) also play a central role in facilitating the acquisition and spread of AMR genes. We isolated Escherichia coli (n = 627) from fecal samples in respectively 25 poultry, 28 swine, and 15 veal calf herds from 6 European countries to investigate the phylogeny of E. coli at country, animal host and farm levels. Furthermore, we examine the evolution of AMR in E. coli genomes including an association with virulence genes, plasmids and MGEs. We compared the abundance metrics retrieved from metagenomic sequencing and whole genome sequenced of E. coli isolates from the same fecal samples and farms. The E. coli isolates in this study indicated no clonality or clustering based on country of origin and genetic markers; AMR, and MGEs. Nonetheless, mobile genetic elements play a role in the acquisition of AMR and virulence genes. Additionally, an abundance of AMR was agreeable between metagenomic and whole genome sequencing analysis for several AMR classes in poultry fecal samples suggesting that metagenomics could be used as an indicator for surveillance of AMR in E. coli isolates and vice versa.

Original language	English
Article number	15108
Journal	Scientific Reports
Volume	11
Number of pages	12
ISSN	2045-2322
DOIs	https://doi.org/10.1038/s41598-021-93970-7
Publication status	Published - 2021

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Leekitcharoenphon, P., Johansson, M. H. K., Munk, P., Malorny, B., Skarżyńska, M., Wadepohl, K., Moyano, G., Hesp, A., Veldman, K. T., Bossers, A., Graveland, H., van Essen, A., Battisti, A., Caprioli, A., Blaha, T., Hald, T., Daskalov, H., Saatkamp, H. W., Stärk, K. D. C., ... consortium, EFFORT. (2021). Genomic evolution of antimicrobial resistance in Escherichia coli. Scientific Reports, 11, Article 15108. https://doi.org/10.1038/s41598-021-93970-7

@article{86aad207901d4913800a0f206516d62f,

title = "Genomic evolution of antimicrobial resistance in Escherichia coli",

abstract = "The emergence of antimicrobial resistance (AMR) is one of the biggest health threats globally. In addition, the use of antimicrobial drugs in humans and livestock is considered an important driver of antimicrobial resistance. The commensal microbiota, and especially the intestinal microbiota, has been shown to have an important role in the emergence of AMR. Mobile genetic elements (MGEs) also play a central role in facilitating the acquisition and spread of AMR genes. We isolated Escherichia coli (n = 627) from fecal samples in respectively 25 poultry, 28 swine, and 15 veal calf herds from 6 European countries to investigate the phylogeny of E. coli at country, animal host and farm levels. Furthermore, we examine the evolution of AMR in E. coli genomes including an association with virulence genes, plasmids and MGEs. We compared the abundance metrics retrieved from metagenomic sequencing and whole genome sequenced of E. coli isolates from the same fecal samples and farms. The E. coli isolates in this study indicated no clonality or clustering based on country of origin and genetic markers; AMR, and MGEs. Nonetheless, mobile genetic elements play a role in the acquisition of AMR and virulence genes. Additionally, an abundance of AMR was agreeable between metagenomic and whole genome sequencing analysis for several AMR classes in poultry fecal samples suggesting that metagenomics could be used as an indicator for surveillance of AMR in E. coli isolates and vice versa.",

author = "Pimlapas Leekitcharoenphon and Johansson, {Markus Hans Kristofer} and Patrick Munk and Burkhard Malorny and Magdalena Skar{\.z}y{\'n}ska and Katharina Wadepohl and Gabriel Moyano and Ayla Hesp and Veldman, {Kees T.} and Alex Bossers and Haitske Graveland and {van Essen}, Alieda and Antonio Battisti and Andrea Caprioli and Thomas Blaha and Tine Hald and Hristo Daskalov and Saatkamp, {Helmut W.} and St{\"a}rk, {Katharina D.C.} and Luiken, {Roosmarijn E.C.} and {Van Gompel}, Liese and Hansen, {Rasmus Borup} and Jeroen Dewulf and Duarte, {Ana Sofia Ribeiro} and Magdalena Zaj{\c a}c and Dariusz Wasyl and Pascal Sanders and Bruno Gonzalez-Zorn and Brouwer, {Michael S.M.} and Wagenaar, {Jaap A.} and Heederik, {Dick J.J.} and Dik Mevius and Aarestrup, {Frank M.} and EFFORT consortium",

year = "2021",

doi = "10.1038/s41598-021-93970-7",

language = "English",

volume = "11",

journal = "Scientific Reports",

issn = "2045-2322",

publisher = "Nature Publishing Group",

}

Leekitcharoenphon, P, Johansson, MHK, Munk, P, Malorny, B, Skarżyńska, M, Wadepohl, K, Moyano, G, Hesp, A, Veldman, KT, Bossers, A, Graveland, H, van Essen, A, Battisti, A, Caprioli, A, Blaha, T, Hald, T, Daskalov, H, Saatkamp, HW, Stärk, KDC, Luiken, REC, Van Gompel, L, Hansen, RB, Dewulf, J, Duarte, ASR, Zając, M, Wasyl, D, Sanders, P, Gonzalez-Zorn, B, Brouwer, MSM, Wagenaar, JA, Heederik, DJJ, Mevius, D, Aarestrup, FM & consortium, EFFORT 2021, 'Genomic evolution of antimicrobial resistance in Escherichia coli', Scientific Reports, vol. 11, 15108. https://doi.org/10.1038/s41598-021-93970-7

TY - JOUR

T1 - Genomic evolution of antimicrobial resistance in Escherichia coli

AU - Leekitcharoenphon, Pimlapas

AU - Johansson, Markus Hans Kristofer

AU - Munk, Patrick

AU - Malorny, Burkhard

AU - Skarżyńska, Magdalena

AU - Wadepohl, Katharina

AU - Moyano, Gabriel

AU - Hesp, Ayla

AU - Veldman, Kees T.

AU - Bossers, Alex

AU - Zając, Magdalena

AU - Wasyl, Dariusz

AU - Sanders, Pascal

AU - Gonzalez-Zorn, Bruno

AU - Brouwer, Michael S.M.

AU - Wagenaar, Jaap A.

AU - Heederik, Dick J.J.

AU - Mevius, Dik

AU - Aarestrup, Frank M.

AU - consortium, EFFORT

A2 - Graveland, Haitske

A2 - van Essen, Alieda

A2 - Battisti, Antonio

A2 - Caprioli, Andrea

A2 - Blaha, Thomas

A2 - Hald, Tine

A2 - Daskalov, Hristo

A2 - Saatkamp, Helmut W.

A2 - Stärk, Katharina D.C.

A2 - Luiken, Roosmarijn E.C.

A2 - Van Gompel, Liese

A2 - Hansen, Rasmus Borup

A2 - Dewulf, Jeroen

A2 - Duarte, Ana Sofia Ribeiro

PY - 2021

Y1 - 2021

N2 - The emergence of antimicrobial resistance (AMR) is one of the biggest health threats globally. In addition, the use of antimicrobial drugs in humans and livestock is considered an important driver of antimicrobial resistance. The commensal microbiota, and especially the intestinal microbiota, has been shown to have an important role in the emergence of AMR. Mobile genetic elements (MGEs) also play a central role in facilitating the acquisition and spread of AMR genes. We isolated Escherichia coli (n = 627) from fecal samples in respectively 25 poultry, 28 swine, and 15 veal calf herds from 6 European countries to investigate the phylogeny of E. coli at country, animal host and farm levels. Furthermore, we examine the evolution of AMR in E. coli genomes including an association with virulence genes, plasmids and MGEs. We compared the abundance metrics retrieved from metagenomic sequencing and whole genome sequenced of E. coli isolates from the same fecal samples and farms. The E. coli isolates in this study indicated no clonality or clustering based on country of origin and genetic markers; AMR, and MGEs. Nonetheless, mobile genetic elements play a role in the acquisition of AMR and virulence genes. Additionally, an abundance of AMR was agreeable between metagenomic and whole genome sequencing analysis for several AMR classes in poultry fecal samples suggesting that metagenomics could be used as an indicator for surveillance of AMR in E. coli isolates and vice versa.

AB - The emergence of antimicrobial resistance (AMR) is one of the biggest health threats globally. In addition, the use of antimicrobial drugs in humans and livestock is considered an important driver of antimicrobial resistance. The commensal microbiota, and especially the intestinal microbiota, has been shown to have an important role in the emergence of AMR. Mobile genetic elements (MGEs) also play a central role in facilitating the acquisition and spread of AMR genes. We isolated Escherichia coli (n = 627) from fecal samples in respectively 25 poultry, 28 swine, and 15 veal calf herds from 6 European countries to investigate the phylogeny of E. coli at country, animal host and farm levels. Furthermore, we examine the evolution of AMR in E. coli genomes including an association with virulence genes, plasmids and MGEs. We compared the abundance metrics retrieved from metagenomic sequencing and whole genome sequenced of E. coli isolates from the same fecal samples and farms. The E. coli isolates in this study indicated no clonality or clustering based on country of origin and genetic markers; AMR, and MGEs. Nonetheless, mobile genetic elements play a role in the acquisition of AMR and virulence genes. Additionally, an abundance of AMR was agreeable between metagenomic and whole genome sequencing analysis for several AMR classes in poultry fecal samples suggesting that metagenomics could be used as an indicator for surveillance of AMR in E. coli isolates and vice versa.

U2 - 10.1038/s41598-021-93970-7

DO - 10.1038/s41598-021-93970-7

M3 - Journal article

C2 - 34301966

SN - 2045-2322

VL - 11

JO - Scientific Reports

JF - Scientific Reports

M1 - 15108

ER -

Genomic evolution of antimicrobial resistance in Escherichia coli

Abstract

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