Bacterial Resistance Toward Antimicrobial Ionic Liquids Mediated by Multidrug Efflux Pumps

The effective elimination of foodborne pathogens through cleaning and disinfection measures is of great importance to the food processing industry. As food producers rely heavily on disinfectants to control pathogenic bacteria in their facilities, the increasing spread of tolerant, often even multid...

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Main Authors: Tobias Gundolf, Roland Kalb, Peter Rossmanith, Patrick Mester
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2022.883931/full
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author Tobias Gundolf
Roland Kalb
Roland Kalb
Peter Rossmanith
Peter Rossmanith
Patrick Mester
author_facet Tobias Gundolf
Roland Kalb
Roland Kalb
Peter Rossmanith
Peter Rossmanith
Patrick Mester
author_sort Tobias Gundolf
collection DOAJ
description The effective elimination of foodborne pathogens through cleaning and disinfection measures is of great importance to the food processing industry. As food producers rely heavily on disinfectants to control pathogenic bacteria in their facilities, the increasing spread of tolerant, often even multidrug resistant, strains is of particular concern. In addition to efforts to prevent or at least reduce development and spread of strains resistant to disinfectants and sanitizers, there is an urgent need for new and effective antimicrobials. One new class of promising antimicrobials is ionic liquids (ILs), which have been reported to be effective against resistant strains as they interact with bacterial cells in multiple ways, but investigations of their effectivity against MDR bacteria or specific defense mechanisms are still limited. This study investigates the role of multidrug efflux pumps of the Resistance Nodulation-Division family (RND) on the resistance of bacterial pathogens Escherichia coli and Salmonella enterica serovar Typhimurium toward 10 antimicrobial active ILs. Results reveal that, while known structure–activity relationships (SARs), such as the side-chain effect, were found for all strains, antimicrobial ILs with one elongated alkyl side chain were significantly affected by the RND efflux pump, highlighting the importance of efflux pumps for future IL toxicity studies. In case of antimicrobial ILs with multiple side chains and different cationic head groups, two ILs were identified that were highly active against all investigated strains with little to no effect of the efflux pump. The results obtained in this study for RND efflux pumps can serve as a starting point for identifying and designing antimicrobial ILs as effective biocides against MDR bacteria.
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spelling doaj.art-ebbd3c79e25743d2829d2af16a8a65162022-12-22T03:35:41ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-05-011310.3389/fmicb.2022.883931883931Bacterial Resistance Toward Antimicrobial Ionic Liquids Mediated by Multidrug Efflux PumpsTobias Gundolf0Roland Kalb1Roland Kalb2Peter Rossmanith3Peter Rossmanith4Patrick Mester5Christian Doppler Laboratory for Monitoring of Microbial Contaminants, Unit for Food Microbiology, Department of Veterinary Public Health and Food Science, University of Veterinary Medicine, Vienna, AustriaProionic Production of Ionic Substances GmbH, Grambach, AustriaJoint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesJoint BioEnergy Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United StatesUnit for Food Microbiology, Department of Veterinary Public Health and Food Science, University of Veterinary Medicine, Vienna, AustriaUnit for Food Microbiology, Department of Veterinary Public Health and Food Science, University of Veterinary Medicine, Vienna, AustriaThe effective elimination of foodborne pathogens through cleaning and disinfection measures is of great importance to the food processing industry. As food producers rely heavily on disinfectants to control pathogenic bacteria in their facilities, the increasing spread of tolerant, often even multidrug resistant, strains is of particular concern. In addition to efforts to prevent or at least reduce development and spread of strains resistant to disinfectants and sanitizers, there is an urgent need for new and effective antimicrobials. One new class of promising antimicrobials is ionic liquids (ILs), which have been reported to be effective against resistant strains as they interact with bacterial cells in multiple ways, but investigations of their effectivity against MDR bacteria or specific defense mechanisms are still limited. This study investigates the role of multidrug efflux pumps of the Resistance Nodulation-Division family (RND) on the resistance of bacterial pathogens Escherichia coli and Salmonella enterica serovar Typhimurium toward 10 antimicrobial active ILs. Results reveal that, while known structure–activity relationships (SARs), such as the side-chain effect, were found for all strains, antimicrobial ILs with one elongated alkyl side chain were significantly affected by the RND efflux pump, highlighting the importance of efflux pumps for future IL toxicity studies. In case of antimicrobial ILs with multiple side chains and different cationic head groups, two ILs were identified that were highly active against all investigated strains with little to no effect of the efflux pump. The results obtained in this study for RND efflux pumps can serve as a starting point for identifying and designing antimicrobial ILs as effective biocides against MDR bacteria.https://www.frontiersin.org/articles/10.3389/fmicb.2022.883931/fullionic liquidsantimicrobialmultidrug resistanceefflux pumpResistance Nodulation Divisionstructure–activity relationship
spellingShingle Tobias Gundolf
Roland Kalb
Roland Kalb
Peter Rossmanith
Peter Rossmanith
Patrick Mester
Bacterial Resistance Toward Antimicrobial Ionic Liquids Mediated by Multidrug Efflux Pumps
Frontiers in Microbiology
ionic liquids
antimicrobial
multidrug resistance
efflux pump
Resistance Nodulation Division
structure–activity relationship
title Bacterial Resistance Toward Antimicrobial Ionic Liquids Mediated by Multidrug Efflux Pumps
title_full Bacterial Resistance Toward Antimicrobial Ionic Liquids Mediated by Multidrug Efflux Pumps
title_fullStr Bacterial Resistance Toward Antimicrobial Ionic Liquids Mediated by Multidrug Efflux Pumps
title_full_unstemmed Bacterial Resistance Toward Antimicrobial Ionic Liquids Mediated by Multidrug Efflux Pumps
title_short Bacterial Resistance Toward Antimicrobial Ionic Liquids Mediated by Multidrug Efflux Pumps
title_sort bacterial resistance toward antimicrobial ionic liquids mediated by multidrug efflux pumps
topic ionic liquids
antimicrobial
multidrug resistance
efflux pump
Resistance Nodulation Division
structure–activity relationship
url https://www.frontiersin.org/articles/10.3389/fmicb.2022.883931/full
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