Benzalkonium chloride forces selective evolution of resistance towards antibiotics in Salmonella enterica serovar Typhimurium.


Journal

Journal of infection and public health
ISSN: 1876-035X
Titre abrégé: J Infect Public Health
Pays: England
ID NLM: 101487384

Informations de publication

Date de publication:
Dec 2023
Historique:
received: 06 06 2023
revised: 05 09 2023
accepted: 22 10 2023
medline: 27 11 2023
pubmed: 8 11 2023
entrez: 7 11 2023
Statut: ppublish

Résumé

Although food-grade disinfectants are extensively used worldwide, it has been reported that the long-term exposure of bacteria to these compounds may represent a selective force inducing evolution including the emergence of antibiotic resistance. However, the mechanism underlying this correlation has not been elucidated. This study aims to investigate the genomic evolution caused by long-term disinfectant exposure in terms of antibiotic resistance in Salmonella enterica Typhimurium. S. Typhimurium isolates were exposed to increasing concentrations of benzalkonium chloride (BAC) and variations of their antibiotic susceptibilities were monitored. Strains that survived BAC exposure were analyzed at whole genome perspective using comparative genomics, and Sanger sequencing-confirmed mutations in ramR gene were identified. Next, the efflux activity in ramR-mutated strains shown as bisbenzimide accumulation and expression of genes involved in AcrAB-TolC efflux pump using quantitative reverse transcriptase PCR were determined. Mutation rates of evolved strains varied from 5.82 × 10 This work demonstrated that disinfectants, specifically BAC forces S. Typhimurium to enter a specific evolutionary trajectory towards antibiotic resistance illustrating the side effects of long-term exposure to BAC and probably also to other disinfectants. Most significantly, this study provides new insights in understanding the emergence of antibiotic resistance in modern society.

Sections du résumé

BACKGROUND BACKGROUND
Although food-grade disinfectants are extensively used worldwide, it has been reported that the long-term exposure of bacteria to these compounds may represent a selective force inducing evolution including the emergence of antibiotic resistance. However, the mechanism underlying this correlation has not been elucidated. This study aims to investigate the genomic evolution caused by long-term disinfectant exposure in terms of antibiotic resistance in Salmonella enterica Typhimurium.
METHODS METHODS
S. Typhimurium isolates were exposed to increasing concentrations of benzalkonium chloride (BAC) and variations of their antibiotic susceptibilities were monitored. Strains that survived BAC exposure were analyzed at whole genome perspective using comparative genomics, and Sanger sequencing-confirmed mutations in ramR gene were identified. Next, the efflux activity in ramR-mutated strains shown as bisbenzimide accumulation and expression of genes involved in AcrAB-TolC efflux pump using quantitative reverse transcriptase PCR were determined.
RESULTS RESULTS
Mutation rates of evolved strains varied from 5.82 × 10
CONCLUSIONS CONCLUSIONS
This work demonstrated that disinfectants, specifically BAC forces S. Typhimurium to enter a specific evolutionary trajectory towards antibiotic resistance illustrating the side effects of long-term exposure to BAC and probably also to other disinfectants. Most significantly, this study provides new insights in understanding the emergence of antibiotic resistance in modern society.

Identifiants

pubmed: 37935604
pii: S1876-0341(23)00360-X
doi: 10.1016/j.jiph.2023.10.022
pii:
doi:

Substances chimiques

Anti-Bacterial Agents 0
Benzalkonium Compounds 0
Disinfectants 0
Bacterial Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

225-235

Informations de copyright

Copyright © 2023 The Authors. Published by Elsevier Ltd.. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of Competing Interest The authors have no interest to declare.

Auteurs

Ricardo A Wu-Chen (RA)

Department of Food Science and Nutrition, College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, China.

Jinsong Feng (J)

Department of Food Science and Nutrition, College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, China.

Mohamed Elhadidy (M)

Biomedical Sciences Program, University of Science and Technology, Zewail City of Science and Technology, Giza, Egypt; Center for Genomics, Helmy Institute for Medical Sciences, Zewail City of Science and Technology, Giza, Egypt; Department of Bacteriology, Mycology and Immunology, Faculty of Veterinary Medicine, Mansoura University, Mansoura, Egypt.

Reshma B Nambiar (RB)

College of Animal Sciences, Zhejiang University, Hangzhou 310058, China.

Xinyu Liao (X)

Department of Food Science and Nutrition, College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, China; Future Food Laboratory, Innovation Center of Yangtze River Delta, Zhejiang University, Jiaxing 314100, China.

Min Yue (M)

College of Animal Sciences, Zhejiang University, Hangzhou 310058, China. Electronic address: myue@zju.edu.cn.

Tian Ding (T)

Department of Food Science and Nutrition, College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, China; Future Food Laboratory, Innovation Center of Yangtze River Delta, Zhejiang University, Jiaxing 314100, China. Electronic address: tding@zju.edu.cn.

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Classifications MeSH