Cell Envelope Modifications Generating Resistance to Hop Beta Acids and Collateral Sensitivity to Cationic Antimicrobials in <i>Listeria monocytogenes</i>

Hop beta acids (HBAs) are characteristic compounds from the hop plant that are of interest for their strong antimicrobial activity. In this work, we report a resistance mechanism against HBA in the foodborne pathogen <i>Listeria monocytogenes</i>. Using an evolution experiment, we isolat...

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Main Authors: Maarten Goedseels, Chris W. Michiels
Format: Article
Language:English
Published: MDPI AG 2023-08-01
Series:Microorganisms
Subjects:
Online Access:https://www.mdpi.com/2076-2607/11/8/2024
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author Maarten Goedseels
Chris W. Michiels
author_facet Maarten Goedseels
Chris W. Michiels
author_sort Maarten Goedseels
collection DOAJ
description Hop beta acids (HBAs) are characteristic compounds from the hop plant that are of interest for their strong antimicrobial activity. In this work, we report a resistance mechanism against HBA in the foodborne pathogen <i>Listeria monocytogenes</i>. Using an evolution experiment, we isolated two HBA-resistant mutants with mutations in the <i>mprF</i> gene, which codes for the Multiple Peptide Resistance Factor, an enzyme that confers resistance to cationic peptides and antibiotics in several Gram-positive bacteria by lysinylating membrane phospholipids. Besides the deletion of <i>mprF</i>, the deletion of <i>dltA</i>, which mediates the alanylation of teichoic acids, resulted in increased HBA resistance, suggesting that resistance may be caused by a reduction in positive charges on the cell surface. Additionally, we found that this resistance is maintained at low pH, indicating that the resistance mechanism is not solely based on electrostatic interactions of HBA with the cell surface. Finally, we showed that the HBA-resistant mutants display collateral sensitivity to the cationic antimicrobials polymyxin B and nisin, which may open perspectives for combining antimicrobials to prevent resistance development.
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spelling doaj.art-42d50f0520354e6a8330c6abf403a0292023-11-19T02:17:54ZengMDPI AGMicroorganisms2076-26072023-08-01118202410.3390/microorganisms11082024Cell Envelope Modifications Generating Resistance to Hop Beta Acids and Collateral Sensitivity to Cationic Antimicrobials in <i>Listeria monocytogenes</i>Maarten Goedseels0Chris W. Michiels1Department of Microbial and Molecular Systems, KU Leuven, B-3000 Leuven, BelgiumDepartment of Microbial and Molecular Systems, KU Leuven, B-3000 Leuven, BelgiumHop beta acids (HBAs) are characteristic compounds from the hop plant that are of interest for their strong antimicrobial activity. In this work, we report a resistance mechanism against HBA in the foodborne pathogen <i>Listeria monocytogenes</i>. Using an evolution experiment, we isolated two HBA-resistant mutants with mutations in the <i>mprF</i> gene, which codes for the Multiple Peptide Resistance Factor, an enzyme that confers resistance to cationic peptides and antibiotics in several Gram-positive bacteria by lysinylating membrane phospholipids. Besides the deletion of <i>mprF</i>, the deletion of <i>dltA</i>, which mediates the alanylation of teichoic acids, resulted in increased HBA resistance, suggesting that resistance may be caused by a reduction in positive charges on the cell surface. Additionally, we found that this resistance is maintained at low pH, indicating that the resistance mechanism is not solely based on electrostatic interactions of HBA with the cell surface. Finally, we showed that the HBA-resistant mutants display collateral sensitivity to the cationic antimicrobials polymyxin B and nisin, which may open perspectives for combining antimicrobials to prevent resistance development.https://www.mdpi.com/2076-2607/11/8/2024<i>Listeria monocytogenes</i>hop beta acidsnatural antimicrobialcollateral sensitivitycell envelopeMprF
spellingShingle Maarten Goedseels
Chris W. Michiels
Cell Envelope Modifications Generating Resistance to Hop Beta Acids and Collateral Sensitivity to Cationic Antimicrobials in <i>Listeria monocytogenes</i>
Microorganisms
<i>Listeria monocytogenes</i>
hop beta acids
natural antimicrobial
collateral sensitivity
cell envelope
MprF
title Cell Envelope Modifications Generating Resistance to Hop Beta Acids and Collateral Sensitivity to Cationic Antimicrobials in <i>Listeria monocytogenes</i>
title_full Cell Envelope Modifications Generating Resistance to Hop Beta Acids and Collateral Sensitivity to Cationic Antimicrobials in <i>Listeria monocytogenes</i>
title_fullStr Cell Envelope Modifications Generating Resistance to Hop Beta Acids and Collateral Sensitivity to Cationic Antimicrobials in <i>Listeria monocytogenes</i>
title_full_unstemmed Cell Envelope Modifications Generating Resistance to Hop Beta Acids and Collateral Sensitivity to Cationic Antimicrobials in <i>Listeria monocytogenes</i>
title_short Cell Envelope Modifications Generating Resistance to Hop Beta Acids and Collateral Sensitivity to Cationic Antimicrobials in <i>Listeria monocytogenes</i>
title_sort cell envelope modifications generating resistance to hop beta acids and collateral sensitivity to cationic antimicrobials in i listeria monocytogenes i
topic <i>Listeria monocytogenes</i>
hop beta acids
natural antimicrobial
collateral sensitivity
cell envelope
MprF
url https://www.mdpi.com/2076-2607/11/8/2024
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