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

ABSTRACT: BACKGROUND:Listeria monocytogenes Clonal Complexes (CCs) have been epidemiologically associated with foods, especially ready-to-eat (RTE) products for which the most likely source of contamination depends on the occurrence of persisting clones in food-processing environments (FPEs). As the ability of L. monocytogenes to adapt to environmental stressors met in the food chain challenges the efforts to its eradication from FPEs, the threat of persistent strains to the food industry and public health authorities continues to rise. In this study, 94 food and FPEs L. monocytogenes isolates, representing persistent subtypes contaminating three French seafood facilities over 2-6?years, were whole-genome sequenced to characterize their genetic diversity and determine the biomarkers associated with long-term survival in FPEs. RESULTS:Food and FPEs isolates belonged to five CCs, comprising long-term intra- and inter-plant persisting clones. Mobile genetic elements (MGEs) such as plasmids, prophages and transposons were highly conserved within CCs, some of which harboured genes for resistance to chemical compounds and biocides used in the processing plants. Some of these genes were found in a 90.8 kbp plasmid, predicted to be" mobilizable", identical in isolates from CC204 and CC155, and highly similar to an 81.6 kbp plasmid from isolates belonging to CC7. These similarities suggest horizontal transfer between isolates, accompanied by deletion and homologous recombination in isolates from CC7. Prophage profiles characterized persistent clonal strains and several prophage-loci were plant-associated. Notably, a persistent clone from CC101 harboured a novel 31.5 kbp genomic island that we named Listeria genomic island 3 (LGI3), composed by plant-associated loci and chromosomally integrating cadmium-resistance determinants cadA1C. CONCLUSIONS:Genome-wide analysis indicated that inter- and intra-plant persisting clones harbour conserved MGEs, likely acquired in FPEs and maintained by selective pressures. The presence of closely related plasmids in L. monocytogenes CCs supports the hypothesis of horizontal gene transfer conferring enhanced survival to FPE-associated stressors, especially in hard-to-clean harbourage sites. Investigating the MGEs evolutionary and transmission dynamics provides additional resolution to trace-back potentially persistent clones. The biomarkers herein discovered provide new tools for better designing effective strategies for the removal or reduction of resident L. monocytogenes in FPEs to prevent contamination of RTE seafood.

SUBMITTER: Palma F

PROVIDER: S-EPMC7006209 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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

Palma Federica F Brauge Thomas T Radomski Nicolas N Mallet Ludovic L Felten Arnaud A Mistou Michel-Yves MY Brisabois Anne A Guillier Laurent L Midelet-Bourdin Graziella G

BMC genomics 20200206 1

<h4>Background</h4>Listeria monocytogenes Clonal Complexes (CCs) have been epidemiologically associated with foods, especially ready-to-eat (RTE) products for which the most likely source of contamination depends on the occurrence of persisting clones in food-processing environments (FPEs). As the ability of L. monocytogenes to adapt to environmental stressors met in the food chain challenges the efforts to its eradication from FPEs, the threat of persistent strains to the food industry and publ ...[more]

PMID: 32028892

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Project description:Listeria monocytogenes is a foodborne pathogen and a resilient environmental saprophyte. Dairy farms are a reservoir of L. monocytogenes, and strains can persist on farms for years. Here, we sequenced the genomes of 250 L. monocytogenes isolates to investigate the persistence and mobile genetic elements (MGEs) of Listeria strains inhabiting dairy farms. We performed a single-nucleotide polymorphism (SNP)-based phylogenomic analysis to identify 14 monophyletic clades of L. monocytogenes persistent on the farms for ≥6 months. We found that prophages and other mobile genetic elements were, on average, more numerous among isolates in persistent than nonpersistent clades, and we demonstrated that resistance genes against bacitracin, arsenic, and cadmium were significantly more prevalent among isolates in persistent than nonpersistent clades. We identified a diversity of mobile elements among the 250 farm isolates, including three novel plasmids, three novel transposons, and a novel prophage harboring cadmium resistance genes. Several of the mobile elements we identified in Listeria were identical to the mobile elements of enterococci, which is indicative of recent transfer between these genera. Through a genome-wide association study, we discovered that three putative defense systems against invading prophages and plasmids were negatively associated with persistence on farms. Our findings suggest that mobile elements support the persistence of L. monocytogenes on dairy farms and that L. monocytogenes inhabiting the agroecosystem is a potential reservoir of mobile elements that may spread to the food industry. IMPORTANCE Animal-derived raw materials are an important source of L. monocytogenes in the food industry. Knowledge of the factors contributing to the pathogen's transmission and persistence on farms is essential for designing effective strategies against the spread of the pathogen from farm to fork. An increasing body of evidence suggests that mobile genetic elements support the adaptation and persistence of L. monocytogenes in the food industry, as these elements contribute to the dissemination of genes encoding favorable phenotypes, such as resilience against biocides. Understanding of the role of farms as a potential reservoir of these elements is needed for managing the transmission of mobile elements across the food chain. Because L. monocytogenes coinhabits the farm ecosystem with a diversity of other bacterial species, it is important to assess the degree to which genetic elements are exchanged between Listeria and other species, as such exchanges may contribute to the rise of novel resistance phenotypes.

Project description:Antimicrobial resistance is an existential threat to the health sector, with far-reaching consequences in managing microbial infections. In this study, one hundred and ninety-four Listeria monocytogenes isolates were profiled for susceptibility using disc diffusion techniques. Possible foodborne listeriosis risk associated with ready-to-eat (RTE) foods (RTEF) and the risk of empirical treatment (EMPT) of L. monocytogenes infections, using multiple antimicrobial resistance indices (MARI) and antimicrobial resistance indices (ARI), respectively, were investigated. Twelve European Committee on Antimicrobial Susceptibility Testing (EUCAST) prescribed/recommended antimicrobials (EPAS) for the treatment of listeriosis and ten non-prescribed antimicrobials (non-PAS)] were evaluated. Antimicrobial resistance > 50% against PAs including sulfamethoxazole (61.86%), trimethoprim (56.19%), amoxicillin (42.27%), penicillin (41.24%), and erythromycin (40.21%) was observed. Resistance > 50% against non-PAS, including oxytetracycline (60.89%), cefotetan (59.28%), ceftriaxone (53.09%), and streptomycin (40.21%) was also observed. About 55.67% and 65.46% of the isolates had MARI scores ranging from 0.25-0.92 and 0.30-0.70 for EPAs and non-PAs, respectively. There was a significant difference (p < 0.01) between the MARI scores of the isolates for EPAs and non-PAs (means of 0.27 ± 0.21 and 0.31 ± 0.14, respectively). MARI/ARI scores above the Krumperman permissible threshold (>0.2) suggested a high risk/level of antimicrobial-resistant L. monocytogenes. The MARI risks of the non-success of empirical treatment (EMPT) attributed to EPAs and non-PAs were generally high (55.67% and 65.463%, respectively) due to the antimicrobial resistance of the isolates. MARI-based estimated success and non-success of EMPT if EUCAST-prescribed antimicrobials were administered for the treatment of listeriosis were 44.329% and 55.67%, respectively. The EMPT if non-prescribed antimicrobials were administered for the treatment of listeriosis was 34.53% and 65.46%, respectively. This indicates a potentially high risk with PAs and non-PAs for the treatment of L. monocytogenes infection. Furthermore, ARI scores ≤ 0.2 for EPAs were observed in polony, potato chips, muffins, and assorted sandwiches, whereas ARI scores for non-PAs were >0.2 across all the RTE food types. The ARI-based estimate identified potential risks associated with some RTE foods, including fried fish, red Vienna sausage, Russian sausage, fruit salad, bread, meat pies, fried chicken, cupcakes, and vetkoek. This investigation identified a high risk of EMPT due to the presence of antimicrobial-resistant L. monocytogenes in RTE foods, which could result in severe health consequences.

Dataset Information

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

Publications

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

Similar Datasets

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