Gene expression in Listeria monocytogenes exposed to sublethal concentration of benzalkonium chloride

Tamburro, Manuela; Ripabelli, Giancarlo; Vitullo, M; Dallman, Timothy J.; Pontello, M.; Amar, Corinne; Sammarco, Michela Lucia

doi:10.1016/j.cimid.2015.03.004

Cited by 46 publications

(26 citation statements)

References 45 publications

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“…In the case of the strain isolated after the C&D procedures, lde gene was expressed only in the presence of high concentration of BC, suggesting an improved tolerance of the strain to the biocide. This is in line with the results of other authors that reported a different expression rate between strains but with a lower extent in the expression of the targeted genes (Romanova et al, 2006 ; Tamburro et al, 2015 ). Nevertheless, Tamburro et al found high transcription levels of both mdrL and lde efflux systems in selected BC-resistant strains of Listeria monocytogenes , where the lde gene presented the highest expression level among the tested strains (Tamburro et al, 2015 ).…”

Section: Discussionsupporting

confidence: 92%

“…This is in line with the results of other authors that reported a different expression rate between strains but with a lower extent in the expression of the targeted genes (Romanova et al, 2006 ; Tamburro et al, 2015 ). Nevertheless, Tamburro et al found high transcription levels of both mdrL and lde efflux systems in selected BC-resistant strains of Listeria monocytogenes , where the lde gene presented the highest expression level among the tested strains (Tamburro et al, 2015 ). However, both in the work of Romanova et al, and Tamburro et al, the gene expression profiles were evaluated after few minutes of exposure to BC.…”

Section: Discussionsupporting

confidence: 92%

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Resistance to Biocides in Listeria monocytogenes Collected in Meat-Processing Environments

et al. 2016

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The emergence of microorganisms exerting resistance to biocides is a challenge to meat-processing environments. Bacteria can be intrinsically resistant to biocides but resistance can also be acquired by adaptation to their sub-lethal concentrations. Moreover, the presence of biocide resistance determinants, which is closely linked to antibiotic resistance determinants, could lead to co-selection during disinfection practices along the food chain, and select cross-resistant foodborne pathogens. The purpose of this work was to test the resistance of wild strains of Listeria monocytogenes, isolated from pork meat processing plants, toward benzalkonium chloride (BC), used as proxy of quaternary ammonium compounds. Furthermore, the expression of two non-specific efflux pumps genes (lde and mdrL) under biocide exposure was evaluated. L. monocytogenes were isolated from five processing plants located in the Veneto region (northeast of Italy) before and after cleaning and disinfection (C&D) procedures. A total of 45 strains were collected: 36 strains before and nine after the C&D procedures. Collected strains were typed according to MLST and ERIC profiles. Strains sampled in the same site, isolated before, and after the C&D procedures and displaying the same MLST and ERIC profiles were tested for their sensitivity to different concentrations of BC, in a time course assay. The expression of non-specific efflux pumps was evaluated at each time point by qPCR using tufA gene as housekeeping. A differential expression of the two investigated genes was observed: lde was found to be more expressed by the strains isolated before C&D procedures while its expression was dose-dependent in the case of the post C&D procedures strain. On the contrary, the expression of mdrL was inhibited under low biocidal stress (10 ppm BC) and enhanced in the presence of high stress (100 ppm BC). These findings suggests a possible role for C&D procedures to select L. monocytogenes persisters, pointing out the importance of dealing with the identification of risk factors in food plants sanification procedures that might select more tolerant strains.

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Section: Discussionsupporting

confidence: 92%

Section: Discussionsupporting

confidence: 92%

Resistance to Biocides in Listeria monocytogenes Collected in Meat-Processing Environments

et al. 2016

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“…Additionally, these periods could have allowed cells in the bulk phase to have enough time to repair possible damaged cellular structures and express chromosome and plasmid-encoded efflux pumps, therefore causing the extrusion of BAC outside of the cell. With this regard, Tamburro et al, (2015) observed an alteration in the gene expression pattern concomitant with a higher tolerance to BAC in L. monocytogenes after exposure to 10 µg/ml BAC, highlighting a significant increase in the expression of mdrL (efflux pump) and sigB (transcription factor) genes. Similar phenomena have also been reported in E. coli after BAC sublethal exposure (Bore et al, 2007).…”

Section: Discussionmentioning

confidence: 87%

Tolerance development in Listeria monocytogenes-Escherichia coli dual-species biofilms after sublethal exposures to pronase-benzalkonium chloride combined treatments

Rodríguez-López

Cabo

2017

Food Microbiology

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This study was designed to assess the effects that sublethal exposures to pronase (PRN) and benzalkonium chloride (BAC) combined treatments have on Listeria monocytogenes-Escherichia coli dual-species biofilms grown on stainless steel in terms of tolerance development (TD) to these compounds. Additionally, fluorescence microscopy was used to observe the changes of the biofilm structure. PRN-BAC exposure was carried out using three different approaches and TD was evaluated treating biofilms with a final 100 μg/ml PRN followed by 50 μg/ml BAC combined treatment. Results showed that exposure to PRN-BAC significantly decreased the number of adhered L. monocytogenes (P < 0.05), while E. coli counts remained generally unaltered. It was also demonstrated that the incorporation of recovery periods during sublethal exposures increased the tolerance of both species of the mixed biofilm to the final PRN-BAC treatment. Moreover, control biofilms became more resistant to PRN-BAC if longer incubation periods were used. Regardless of the treatment used, log reduction values were generally lower in L. monocytogenes compared to E. coli. Additionally, microscopy images showed an altered morphology produced by sublethal PRN-BAC in exposed L. monocytogenes-E. coli dual-species biofilms compared to control samples. Results also demonstrated that L. monocytogenes-E. coli dual-species biofilms are able to develop tolerance to PRN-BAC combined treatments depending on way they have been previously exposed. Moreover, they suggest that the generation of bacterial tolerance should be included as a parameter for sanitation procedures design.

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“…It has been found that active drug efflux in Gram-positive bacteria is mainly associated with MFS-type pumps ( Li and Nikaido, 2004 ; Andersen et al, 2015 ). In L. monocytogenes , another MFS-pump, MdrL, has also been reported most commonly ( Mata et al, 2000 ; Romanova et al, 2006 ; Tamburro et al, 2015 ). But, it is still unclear whether MdrL is involved in the induced resistance to fluoroquinolones in L. monocytogenes .…”

Section: Introductionmentioning

confidence: 99%

Role of Efflux Pumps in the in vitro Development of Ciprofloxacin Resistance in Listeria monocytogenes

Jiang

et al. 2018

Front. Microbiol.

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Efflux is a primary fluoroquinolone resistance mechanism in Listeria monocytogenes. In the present study, ciprofloxacin resistant strains were selected by exposure of sensitive strain to progressively increasing concentrations of ciprofloxacin and then the roles of efflux pumps Lde and MdrL in the development of resistance to ciprofloxacin were also investigated in L. monocytogenes. Ciprofloxacin sensitive strain of L. monocytogenes exhibited reduced susceptibility to this antibiotic after induction. Cross-resistance to ethidium bromide (EtBr) was observed in ciprofloxacin-induced strains. However, cross-resistance to benzalkonium chloride (BC) did not occur in this study. Compared to the wild-type strain HL06, the expression levels of lde were increased in four ciprofloxacin-induced strains. The single-gene deletion mutants of lde and mdrL from the ciprofloxacin-induced resistant strain HL06CIP4 were constructed. However, decreased minimum inhibitory concentration (MIC) of ciprofloxacin was observed only in HL06CIP4Δlde compared to that of the parental strain HL06CIP4. Ciprofloxacin uptake appeared to be obviously increased in HL06CIP4Δlde in relative to HL06CIP4. These evidences suggested that efflux pump Lde is involved in ciprofloxacin resistance in L. monocytogenes HL06CIP4. The deletion of lexA had no effect on the expression levels of lde in HL06CIP4 in the absence or presence of ciprofloxacin, indicating that LexA was not involved in the regulation of efflux pump Lde in L. monocytogenes.

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Gene expression in Listeria monocytogenes exposed to sublethal concentration of benzalkonium chloride

Cited by 46 publications

References 45 publications

Resistance to Biocides in Listeria monocytogenes Collected in Meat-Processing Environments

Resistance to Biocides in Listeria monocytogenes Collected in Meat-Processing Environments

Tolerance development in Listeria monocytogenes-Escherichia coli dual-species biofilms after sublethal exposures to pronase-benzalkonium chloride combined treatments

Role of Efflux Pumps in the in vitro Development of Ciprofloxacin Resistance in Listeria monocytogenes

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