Nonsynonymous Mutations in
 fepR
 Are Associated with Adaptation of Listeria monocytogenes and Other
 Listeria
 spp. to Low Concentrations of Benzalkonium Chloride but Do Not Increase Survival of L. monocytogenes and Other
 Listeria
 spp. after Exposure to Benzalkonium Chloride Concentrations Recommended for Use in Food Processing Environments

Bolten, Samantha; Harrand, Anna Sophia; Skeens, Jordan; Wiedmann, Martin

doi:10.1128/aem.00486-22

Cited by 10 publications

(9 citation statements)

References 50 publications

(73 reference statements)

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“…Strains that carried a mutation in fepR, as well as strains that artificially overexpress the efflux pump FepA exhibited increased tolerance not only towards BAC, but also towards CTAB, ciprofloxacin and gentamycin, indicating that extrusion by the transporter is rather unspecific. This observation further supports the previous hypothesis that de-repression of fepA is the reason for the observed QAC tolerance (Guérin et al 2014;Bland et al 2022;Bolten et al 2022;Douarre et al 2022). We further substantiated this hypothesis by showing that a mutation in the DNA binding domain of FepR resulted in decreased binding to the promoter of the fepRA operon in comparison to the wildtype FepR protein.…”

Section: Discussionsupporting

confidence: 90%

“…These findings are in accordance with previous studies, which focussed on serial adapted isolated L. monocytogenes and Listeria spp. strains that were exposed to BAC or ciprofloxacin stress and likewise found that the majority of strains acquired mutations in fepR (Bland et al 2022;Bolten et al 2022;Douarre et al 2022). FepR is a TetR-like transcriptional regulator that negatively regulates the fepRA operon, which encodes the regulator itself as well as the MATE family efflux pump FepA (Guérin et al 2014).…”

Section: Discussionmentioning

confidence: 97%

“…In contrast, the chromosomally encoded multidrug and toxic compound (MATE) efflux pump FepA was recently identified as the dominant, stable mode of tolerance for BAC in a screen of over 60 serial adapted produce-associated L. monocytogenes and other Listeria spp. strains (Bolten et al 2022). An independent study of biocide-adapted strains further supported these findings by showing that 94% of the adapted strains possessed mutations in the gene coding for the TetR-like transcriptional regulator FepR that was previously shown to repress its own expression and the expression of the efflux pump encoding gene fepA (Douarre et al 2022).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Adaptation mechanisms ofListeria monocytogenesto quaternary ammonium compounds

Schulz

Dreier

Miranda

et al. 2023

Preprint

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Listeria monocytogenes is ubiquitously found in nature and can easily enter food-processing facilities due to contaminations of raw materials. Several countermeasures are used to combat contamination of food products, for instance the use of disinfectants that contain quaternary ammonium compounds, such as benzalkonium chloride (BAC) and cetyltrimethylammonium bromide (CTAB). In this study, we assessed the potential of the commonly used wildtype strain EGD-e to adapt to BAC and CTAB under laboratory growth conditions. All BAC-tolerant suppressors exclusively carried mutations in fepR or its promoter region likely resulting in the overproduction of the efflux pump FepA. In contrast, CTAB-tolerance was associated with mutations in sugR, which regulates the expression of the efflux pumps SugE1 and SugE2. L. monocytogenes strains lacking either FepA or SugE1/2 could still acquire tolerance towards BAC and CTAB. Genomic analysis revealed that the overproduction of the remaining efflux system could compensate for the deleted one. Even in the absence of both efflux systems, tolerant strains could be isolated, which all carried mutations in the diacylglycerol kinase encoding gene lmo1753 (dgkB). DgkB converts diacylglycerol to phosphatidic acid, which is subsequently re-used for the synthesis of phospholipids suggesting that alterations in membrane composition could be the third adaptation mechanism.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Adaptation mechanisms ofListeria monocytogenesto quaternary ammonium compounds

Schulz

Dreier

Miranda

et al. 2023

Preprint

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“…In addition, we identified bcrABC , a plasmid-borne gene cassette which can confer tolerance of Listeria to low-levels of quats (Bolten et al, 2022), in 67/303 (22%) Listeria isolates. Previous studies surveying meat and vegetable processing plants (Hurley et al, 2019) and meat and salmon processing plants (Fagerlund et al, 2022) showed similar prevalence of bcrABC among Listeria populations.…”

Section: Discussionmentioning

confidence: 99%

Intensive environmental sampling and whole genome sequence-based characterization ofListeriain small and medium sized dairy plants reveal opportunities for simplified and size-appropriate environmental monitoring strategies

Bolten,

Lott,

Ralyea

et al. 2024

Preprint

Self Cite

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Small and medium sized dairy processing plants (SMDPs) may face unique challenges with respect to controlling Listeria in their processing environments, e.g., due to limited resources. The aim of this study was to implement and evaluate environmental monitoring programs (EMPs) for Listeria control in eight SMDPs in a ~1-year longitudinal study; this included a comparison of pre-operation (i.e., after cleaning and sanitation and prior to production) and mid-operation (i.e., at least 4 h into production) sampling strategies. Among 2,072 environmental sponge samples collected across all plants, 272 (13%) were positive for Listeria. Listeria prevalence among pre- and mid-operation samples (15 and 17%, respectively), was not significantly different. Whole genome sequencing (WGS) performed on select isolates to characterize Listeria persistence patterns revealed repeated isolation of closely related Listeria isolates (i.e., ≤20 high quality single nucleotide polymorphism [hqSNP] differences) in 5/8 plants over >6 months, suggesting Listeria persistence and/or re-introduction was relatively common among the SMDPs evaluated here. WGS furthermore showed that for 41 sites where samples collected pre- and mid-operation were positive for Listeria, Listeria isolates obtained were highly related (i.e., ≤10 hqSNP differences), suggesting that pre-operation sampling alone may be sufficient and more effective for detecting sites of Listeria persistence. Importantly, our data also showed that only 1/8 plants showed a significant decrease in Listeria prevalence over 1 year, indicating continued challenges with Listeria control in at least some SMDPs. We conclude that options for simplified Listeria EMP programs (e.g., with a focus on pre-operation sampling, which allows for more rapid identification of likely persistence sites) may be valuable for improved Listeria control in SMDPs.

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“…In another study it was observed that two L. ivanovii strains isolated from postharvest sources in fresh produce processing could adapt to levels of benzalkonium chloride 3-fold higher than non-adapted wild types for the arising of nonsense mutations in the fepR regulator gene of the fepRA operon, which encodes the efflux pump FepA [35].…”

Section: Ivanovii Persistence and Tolerance To Harsh Conditionsmentioning

confidence: 99%

Virulence Characteristics and Distribution of the Pathogen Listeria ivanovii in the Environment and in Food

et al. 2022

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Listeria ivanovii and L. monocytogenes, are the only pathogenic species of the genus Listeria and share many virulence factors and mechanisms of pathogenicity. L. ivanovii shows host tropism towards small ruminants and rodents and much lower virulence for humans compared to L. monocytogenes. However, severe infections caused by L. ivanovii, resulting in bacteremia, abortion and stillbirth, occasionally occurred in immunocompromised persons and in pregnant women, while in immunocompetent hosts L. ivanovii can cause gastroenteritis. In this review, the updated knowledge on virulence aspects and distribution of L. ivanovii in the environment and in food is summarized. Recent research on its virulence characters at genome level gave indications on how pathogenicity evolved in this bacterial species. As for L. monocytogenes, L. ivanovii infections occurred after the ingestion of contaminated food, so an overview of reports regarding its distribution in food products was carried out to obtain indications on the categories of foods exposed to contamination by L. ivanovii. It was found that a wide variety of food products can be a source of this microorganism and that, like L. monocytogenes, L. ivanovii is able to persist in the food production environment. Studies on its ability to grow in enrichment and isolation media suggested that its occurrence in nature might be underestimated. Moreover, virulence varies among strains for differences in virulence character regulation, presence/absence of genetic regions and the possible instability of a Listeria pathogenicity genomic island, LIPI-2, which is unique to L. ivanovii. We can conclude that L. ivanovii, as a possible pathogen for animals and humans, requires more focused investigations regarding its occurrence in the environment and in food and on intra-species variability of pathogenic potential.

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Cited by 10 publications

References 50 publications

Adaptation mechanisms ofListeria monocytogenesto quaternary ammonium compounds

Adaptation mechanisms ofListeria monocytogenesto quaternary ammonium compounds

Intensive environmental sampling and whole genome sequence-based characterization ofListeriain small and medium sized dairy plants reveal opportunities for simplified and size-appropriate environmental monitoring strategies

Virulence Characteristics and Distribution of the Pathogen Listeria ivanovii in the Environment and in Food

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