Genomic characterization of Listeria monocytogenes isolates reveals that their persistence in a pig slaughterhouse is linked to the presence of benzalkonium chloride resistance genes

Abstract

BackgroundThe aim of this study was to characterize the genomes of 30 Listeria monocytogenes isolates collected at a pig slaughterhouse to determine the molecular basis for their persistence.ResultsComparison of the 30 L. monocytogenes genomes showed that successive isolates (i.e., persistent types) recovered from thew sampling site could be linked on the basis of single nucleotide variants confined to prophage regions. In addition, our study revealed the presence among these strains of the bcrABC cassette which is known to produce efflux pump-mediated benzalkonium chloride resistance, and which may account for the persistence of these isolates in the slaughterhouse environment. The presence of the bcrABC cassette was confirmed by WGS and PCR and the resistance phenotype was determined by measuring minimum inhibitory concentrations. Furthermore, the BC-resistant strains were found to produce lower amounts of biofilm in the presence of sublethal concentrations of BC.ConclusionsHigh resolution SNP-based typing and determination of the bcrABC cassette may provide a means of distinguishing between resident and sporadic L. monocytogenes isolates, and this in turn will support better management of this pathogen in the food industry.Electronic supplementary materialThe online version of this article (10.1186/s12866-018-1363-9) contains supplementary material, which is available to authorized users.

Dynamics of mobile genetic elements of Listeria monocytogenes persisting in ready-to-eat seafood processing plants in France

“…Biofilm-forming ability, physiological adaptation and tolerance to environmental stresses such as temperature, osmotic and oxidative stresses as well as resistance to heavy metals and disinfectants have been phenotypically and genotypically investigated in specific serotypes and CCs of L. monocytogenes to elucidate their persistence mechanisms [19,[23][24][25][26][27][28][29] and comprehensively reviewed by Bergholz et al (2018) [30]. Hence, subtype-specific genetic biomarkers contributing to the persistence phenotype have been described.…”

“…A recent study of Hingston et al (2017) associated the presence/absence and variations of genetic biomarkers such as the virulence gene inlA to different levels of cold and desiccation tolerance in specific serotypes of L. monocytogenes [25]. Tolerance to disinfectants based on quaternary ammonium compounds (QACs), such as benzalkonium chloride (BC), and heavy metals, such as cadmium (Cd) and arsenic (As), have been described in persistent and presumably transient L. monocytogenes strains in FPEs [19,23,27,28,34,35], as well as linked to specific molecular mechanisms. For instance, the three-gene cassette bcrABC, located either on the chromosome or transposable units of L. monocytogenes strains, was described as conferring an increased resistance to BC, a widely used QAC disinfectant in the food industry in the past few decades [36].…”

“…As results of these studies, the persistence of certain L. monocytogenes subtypes is more commonly considered to arise from a complex combination of several factors rather than a single genetic or individual trait [3,23,46]. Hence, understanding the genome-wide diversity and dynamics of MGEs in relevant L. monocytogenes CCs for the food industry is crucial to gain useful information to disentangle their persistence in FPEs.…”

Ecogenetics of antibiotic resistance in Listeria monocytogenes

“…The transposon Tn 6188 (related to the Tn 554 family in Staphylococcus ) carrying the qacH gene is frequently found in L. monocytogenes (Horlbog, Kent, Stephan, & Guldimann, ). The presence of the plasmid‐located bcrABC cassette leads to increased BAC and cadmium resistance, favoring persistence in environments such as pig slaughterhouses (Cherifi et al, ; Minarovičová et al, ; Xu, Nie, Wang, Shi, & Yan, ). In fact, Listeria plasmids frequently contain cadmium resistance determinants (Kuenne et al, ).…”

Strain and Growth Conditions may Regulate Resistance of Listeria monocytogenes Biofilms to Benzalkonium Chloride

“…It is acknowledged that strains of L. monocytogenes with a BAC minimum inhibitory concentration (MIC) of ≥10 mg/L harbor genetic determinants, such as bcrABC [8] and qacH [9], that are known to contribute to BAC resistance. Both transferable resistance genes are prevalent in the food industry [10][11][12]. The efflux systems encoded by these genes belong to the small multidrug resistance (SMR) protein family [8,9].…”