Large-scale phenotypic and genomic analysis of Listeria monocytogenes reveals diversity in the sensitivity to quaternary ammonium compounds but not to peracetic acid.

Mirena Ivanova; Martin Laage Kragh; Judit Szarvas; Elif Seyda Tosun; Natacha Friis Holmud; Alexander Gmeiner; Corinne Amar; Claudia Guldimann; Tu Anh N. Huynh; Renáta Karpíšková; Carmen Rota; Diego Gomez; Eurydice Aboagye; Andrea Etter; Patrizia Centorame; Marina Torresi; Maria Elisabetta De Angelis; Francesco Pomilio; Anders Hauge Okholm; Yinghua Xiao; Sylvia Kleta; Stefanie Lüth; Ariane Pietzka; Jovana Kovacevic; Franco Pagotto; Kathrin Rychli; Irena Zdovc; Bojan Papic; Even Heir; Solveig Langsrud; Trond Møretrø; Phillip Brown; Sophia Kathariou; Roger Stephan; Taurai Tasara; Paw Dalgaard; Patrick Murigu Kamau Njage; Annette Fagerlund; Frank Aarestrup; Lisbeth Truelstrup Hansen; Pimlapas Leekitcharoenphon

doi:10.1128/aem.01829-24

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Title (eng)

Large-scale phenotypic and genomic analysis of Listeria monocytogenes reveals diversity in the sensitivity to quaternary ammonium compounds but not to peracetic acid.

Author

Mirena Ivanova

Martin Laage Kragh

Judit Szarvas

Elif Seyda Tosun

Natacha Friis Holmud

Alexander Gmeiner

Corinne Amar

Claudia Guldimann

Tu Anh N. Huynh

Renáta Karpíšková

Carmen Rota

Diego Gomez

Eurydice Aboagye

Andrea Etter

Patrizia Centorame

Marina Torresi

Maria Elisabetta De Angelis

Francesco Pomilio

Anders Hauge Okholm

Yinghua Xiao

Sylvia Kleta

Stefanie Lüth

University of Veterinary Medicine Vienna

Irena Zdovc

Bojan Papic

Even Heir

Solveig Langsrud

Trond Møretrø

Phillip Brown

Sophia Kathariou

Roger Stephan

Taurai Tasara

Paw Dalgaard

Patrick Murigu Kamau Njage

Annette Fagerlund

Frank Aarestrup

Lisbeth Truelstrup Hansen

Pimlapas Leekitcharoenphon

Abstract (eng)

Listeria monocytogenes presents a significant concern for the food industry due to its ability to persist in the food processing environment. One of the factors contributing to its persistence is decreased sensitivity to disinfectants. Our objective was to assess the diversity of L. monocytogenes sensitivity to food industry disinfectants by testing the response of 1,671 L. monocytogenes isolates to quaternary ammonium compounds (QACs) and 414 isolates to peracetic acid (PAA) using broth microdilution and growth curve analysis assays, respectively, and to categorize the isolates into sensitive and tolerant. A high phenotype-genotype concordance (95%) regarding tolerance to QACs was obtained by screening the genomes for the presence of QAC tolerance-associated genes bcrABC, emrE, emrC, and qacH. Based on this high concordance, we assessed the QAC genes' dissemination among publicly available L. monocytogenes genomes (n = 39,196). Overall, QAC genes were found in 23% and 28% of the L. monocytogenes collection in this study and in the global data set, respectively. bcrABC and qacH were the most prevalent genes, with bcrABC being the most detected QAC gene in the USA, while qacH dominated in Europe. No significant differences (P> 0.05) in the PAA tolerance were detected among isolates belonging to different lineages, serogroups, clonal complexes, or isolation sources, highlighting limited variation in the L. monocytogenes sensitivity to this disinfectant. The present work represents the largest testing of L. monocytogenes sensitivity to important food industry disinfectants at the phenotypic and genomic level, revealing diversity in the tolerance to QACs while all isolates showed similar sensitivity to PAA.Contamination of Listeria monocytogenes within food processing environments is of great concern to the food industry due to challenges in eradicating the isolates once they become established and persistent in the environment. Genetic markers associated with increased tolerance to certain disinfectants have been identified, which alongside other biotic and abiotic factors can favor the persistence of L. monocytogenes in the food production environment. By employing a comprehensive large-scale phenotypic testing and genomic analysis, this study significantly enhances the understanding of the L. monocytogenes tolerance to quaternary ammonium compounds (QACs) and the genetic determinants associated with the increased tolerance. We provide a global overview of the QAC genes prevalence among public L. monocytogenes sequences and their distribution among clonal complexes, isolation sources, and geographical locations. Additionally, our comprehensive screening of the peracetic acid (PAA) sensitivity shows that this disinfectant can be used in the food industry as the lack of variation in sensitivity indicates reliable effect and no apparent possibility for the emergence of tolerance.

Keywords (eng)

Listeria Monocytogenes Drug EffectsListeria Monocytogenes GeneticsPeracetic Acid PharmacologyDisinfectants PharmacologyQuaternary Ammonium Compounds PharmacologyPhenotypeGenome, BacterialMicrobial Sensitivity TestsFood MicrobiologyGenomicsBacterial Proteins GeneticsBacterial Proteins MetabolismDrug Resistance, Bacterial Genetics

Type (eng)

journal article

Language

[eng]

Persistent identifier

https://phaidra.vetmeduni.ac.at/o:4103

DOI

10.1128/aem.01829-24

Is in series

Title (eng)

Applied and Environmental Microbiology

Volume