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Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of turkey-processing plants.

ABSTRACT: The resistance of Listeria monocytogenes to cadmium and arsenic has been used extensively for strain subtyping. However, limited information is available on the prevalence of such resistance among isolates from the environment of food-processing plants. In addition, it is not known whether the resistance of such isolates to heavy metals may correlate with resistance to quaternary ammonium compounds extensively used as disinfectants in the food-processing industry. In this study, we characterized 192 L. monocytogenes isolates (123 putative strains) from the environment of turkey-processing plants in the United States for resistance to cadmium and arsenic and to the quaternary ammonium disinfectant benzalkonium chloride (BC). Resistance to cadmium was significantly more prevalent among strains of serotypes 1/2a (or 3a) and 1/2b (or 3b) (83% and 74%, respectively) than among strains of the serotype 4b complex (19%). Resistance to BC was encountered among 60% and 51% of the serotype 1/2a (or 3a) and 1/2b (or 3b) strains, respectively, and among 7% of the strains of the serotype 4b complex. All BC-resistant strains were also resistant to cadmium, although the reverse was not always the case. In contrast, no correlation was found between BC resistance and resistance to arsenic, which overall was low (6%). Our findings suggest that the processing environment of turkey-processing plants may constitute a reservoir for L. monocytogenes harboring resistance to cadmium and to BC and raise the possibility of common genetic elements or mechanisms mediating resistance to quaternary ammonium disinfectants and to cadmium in L. monocytogenes.

SUBMITTER: Mullapudi S

PROVIDER: S-EPMC2258618 | biostudies-literature | 2008 Mar

REPOSITORIES: biostudies-literature

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Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of turkey-processing plants.

Mullapudi S S Siletzky R M RM Kathariou S S

Applied and environmental microbiology 20080111 5

The resistance of Listeria monocytogenes to cadmium and arsenic has been used extensively for strain subtyping. However, limited information is available on the prevalence of such resistance among isolates from the environment of food-processing plants. In addition, it is not known whether the resistance of such isolates to heavy metals may correlate with resistance to quaternary ammonium compounds extensively used as disinfectants in the food-processing industry. In this study, we characterized ...[more]

PMID: 18192428

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Project description:For decades, quaternary ammonium compounds (QAC)-based sanitizers have been broadly used in food processing environments to control foodborne pathogens such as Listeria monocytogenes. Still, there is a lack of consensus on the likelihood and implication of reduced Listeria susceptibility to benzalkonium chloride (BC) that may emerge due to sublethal exposure to the sanitizers in food processing environments. With a focus on fresh produce processing, we attempted to fill multiple data and evidence gaps surrounding the debate. We determined a strong correlation between tolerance phenotypes and known genetic determinants of BC tolerance with an extensive set of fresh produce isolates. We assessed BC selection on L. monocytogenes through a large-scale and source-structured genomic survey of 25,083 publicly available L. monocytogenes genomes from diverse sources in the United States. With the consideration of processing environment constraints, we monitored the temporal onset and duration of adaptive BC tolerance in both tolerant and sensitive isolates. Finally, we examined residual BC concentrations throughout a fresh produce processing facility at different time points during daily operation. While genomic evidence supports elevated BC selection and the recommendation for sanitizer rotation in the general context of food processing environments, it also suggests a marked variation in the occurrence and potential impact of the selection among different commodities and sectors. For the processing of fresh fruits and vegetables, we conclude that properly sanitized and cleaned facilities are less affected by BC selection and unlikely to provide conditions that are conducive for the emergence of adaptive BC tolerance in L. monocytogenes. IMPORTANCE Our study demonstrates an integrative approach to improve food safety assessment and control strategies in food processing environments through the collective leveraging of genomic surveys, laboratory assays, and processing facility sampling. In the example of assessing reduced Listeria susceptibility to a widely used sanitizer, this approach yielded multifaceted evidence that incorporates population genetic signals, experimental findings, and real-world constraints to help address a lasting debate of policy and practical importance.

Project description:Controlling the food-borne pathogen Listeria (L.) monocytogenes is of great importance from a food safety perspective, and thus for human health. The consequences of failures in this regard have been exemplified by recent large listeriosis outbreaks in the USA and Europe. It is thus particularly notable that tolerance to quaternary ammonium compounds such as benzalkonium chloride (BC) has been observed in many L. monocytogenes strains. However, the molecular determinants and mechanisms of BC tolerance of L. monocytogenes are still largely unknown. Here we describe Tn6188, a novel transposon in L. monocytogenes conferring tolerance to BC. Tn6188 is related to Tn554 from Staphylococcus (S.) aureus and other Tn554-like transposons such as Tn558, Tn559 and Tn5406 found in various Firmicutes. Tn6188 comprises 5117 bp, is integrated chromosomally within the radC gene and consists of three transposase genes (tnpABC) as well as genes encoding a putative transcriptional regulator and QacH, a small multidrug resistance protein family (SMR) transporter putatively associated with export of BC that shows high amino acid identity to Smr/QacC from S. aureus and to EmrE from Escherichia coli. We screened 91 L. monocytogenes strains for the presence of Tn6188 by PCR and found Tn6188 in 10 of the analyzed strains. These isolates were from food and food processing environments and predominantly from serovar 1/2a. L. monocytogenes strains harboring Tn6188 had significantly higher BC minimum inhibitory concentrations (MICs) (28.5 ± 4.7 mg/l) than strains without Tn6188 (14 ± 3.2 mg/l). Using quantitative reverse transcriptase PCR we could show a significant increase in qacH expression in the presence of BC. QacH deletion mutants were generated in two L. monocytogenes strains and growth analysis revealed that ?qacH strains had lower BC MICs than wildtype strains. In conclusion, our results provide evidence that Tn6188 is responsible for BC tolerance in various L. monocytogenes strains.

Project description:Selection for Listeria monocytogenes strains that are tolerant to quaternary ammonium compounds (such as benzalkonium chloride [BC]) is a concern across the food industry, including in fresh produce processing environments. This study evaluated the ability of 67 strains of produce-associated L. monocytogenes and other Listeria spp. ("parent strains") to show enhanced BC tolerance after serial passaging in increasing BC concentrations and to maintain this tolerance after substreaking in the absence of BC. After serial passaging in BC, 62/67 "BC passaged cultures" showed higher MICs (4 to 20 mg/L) than parent strains (2 to 6 mg/L). After the substreaking of two isolates from BC passaged cultures for each parent strain, 105/134 "adapted isolates" maintained MICs (4 to 6 mg/L) higher than parent strain MICs. These results suggested that adapted isolates acquired heritable adaptations that confer BC tolerance. Whole-genome sequencing and Sanger sequencing of fepR, a local repressor of the MATE family efflux pump FepA, identified nonsynonymous fepR mutations in 48/67 adapted isolates. The mean inactivation of adapted isolates after exposure to use-level concentrations of BC (300 mg/L) was 4.48 log, which was not significantly different from inactivation observed in parent strains. Serial passaging of cocultures of L. monocytogenes strains containing bcrABC or qacH did not yield adapted isolates that showed enhanced BC tolerance in comparison to that of monocultures. These results suggest that horizontal gene transfer either did not occur or did not yield isolates with enhanced BC tolerance. Overall, this study provides new insights into selection of BC tolerance among L. monocytogenes and other Listeria spp. IMPORTANCE Listeria monocytogenes tolerance to quaternary ammonium compounds has been raised as a concern with regard to L. monocytogenes persistence in food processing environments, including in fresh produce packing and processing environments. Persistence of L. monocytogenes can increase the risk of product contamination, food recalls, and foodborne illness outbreaks. Our study shows that strains of L. monocytogenes and other Listeria spp. can acquire heritable adaptations that confer enhanced tolerance to low concentrations of benzalkonium chloride, but these adaptations do not increase survival of L. monocytogenes and other Listeria spp. when exposed to concentrations of benzalkonium chloride used for food contact surface sanitation (300 mg/L). Overall, these findings suggest that the emergence of benzalkonium chloride-tolerant Listeria strains in food processing environments is of limited concern, as even strains adapted to gain higher MICs in vitro maintain full sensitivity to the concentrations of benzalkonium chloride used for food contact surface sanitation.

Dataset Information

Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of turkey-processing plants.

Publications

Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of turkey-processing plants.

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