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Survival strategies of Listeria monocytogenes to environmental hostile stress: biofilm formation and stress responses

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Abstract

Listeria monocytogenes is a critical foodborne pathogen that causes listeriosis and threatens public health. This pathogenic microorganism forms a transmission cycle in nature, food industry, and humans, expanding the areas of contamination among them and influencing food safety. L. monocytogenes forms biofilms to protect itself and promotes survival through stress responses to the various stresses (e.g., temperature, pH, and antimicrobial agents) that may be inflicted during food processing. Biofilms and mechanisms of resistance to hostile external or general stresses allow L. monocytogenes to survive despite a variety of efforts to ensure food safety. The current review article focuses on biofilm formation, resistance mechanisms through biofilms, and external specific or general stress responses of L. monocytogenes to help understand the unexpected survival rates of this bacterium; it also proposes the use of obstacle technology to effectively cope with it in the food industry.

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References

  • Adzitey, F., Ali, G. R. R., Huda, N., Cogan, T., & Corry, J. Prevalence, antibiotic resistance and genetic diversity of Listeria monocytogenes isolated from ducks, their rearing and processing environments in Penang, Malaysia. Food Control. 32(2): 607-614 (2013)

    Article  CAS  Google Scholar 

  • Agoston, R., Soni, K., Jesudhasan, P. R., Russell, W. K., Mohácsi-Farkas, C., Pillai, S. D. Differential expression of proteins in Listeria monocytogenes under thermotolerance-inducing, heat shock, and prolonged heat shock conditions. Foodborne pathogens and disease. 6(9): 1133-1140 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Ahlstrom, C. A., Manuel, C. S., Den Bakker, H. C., Wiedmann, M., & Nightingale, K. K. Molecular ecology of Listeria spp., Salmonella, Escherichia coli O157: H7 and non‐O157 Shiga toxin‐producing E. coli in pristine natural environments in Northern Colorado. Journal of Applied Microbiology. 124(2): 511-521 (2018)

    Article  CAS  PubMed  Google Scholar 

  • Akkaya, L., Alisarli, M., Cetinkaya, Z., Kara, R., & Telli, R. Occurrence of Escherichia coli O157:H7/O157, Listeria monocytogenes and Salmonella spp. in beef slaughterhouse environments, equipment and workers. Journal of Muscle Foods. 19(3): 261-274 (2008)

    Article  Google Scholar 

  • Alonso-Hernando, A., Capita, R., Prieto, M., Alonso-Calleja, C. Comparison of antibiotic resistance patterns in Listeria monocytogenes and Salmonella enterica strains pre-exposed and exposed to poultry decontaminants. Food Control. 20(12): 1108-1111 (2009)

    Article  CAS  Google Scholar 

  • Amajoud, N., Leclercq, A., Soriano, J. M., Bracq-Dieye, H., El Maadoudi, M., Senhaji, N. S., ... & Abrini, J. Prevalence of Listeria spp. and characterization of Listeria monocytogenes isolated from food products in Tetouan, Morocco. Food Control. 84: 436-441 (2018)

    Article  Google Scholar 

  • Aminov, R. I. Horizontal gene exchange in environmental microbiota. Frontiers in Microbiology. 2: 158 (2011)

    Article  PubMed  PubMed Central  Google Scholar 

  • Andersson, D. I., Hughes, D. Microbiological effects of sublethal levels of antibiotics. Nature Reviews Microbiology. 12(7): 465-478 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Angelidis, A. S., & Smith, G. M. Three transporters mediate uptake of glycine betaine and carnitine by Listeria monocytogenes in response to hyperosmotic stress. Applied and Environmental Microbiology. 69(2): 1013-1022 (2003)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arcari, T., Feger, M. L., Guerreiro, D. N., Wu, J., O’Byrne, C. P. Comparative Review of the Responses of Listeria monocytogenes and Escherichia coli to low pH stress. Genes. 11(11): 1330 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Archer, D. L. The evolution of FDA's policy on Listeria monocytogenes in ready-to-eat foods in the United States. Current Opinion in Food Science. 20: 64-68 (2018)

    Article  Google Scholar 

  • Arvaniti, M., Tsakanikas, P., Papadopoulou, V., Giannakopoulou, A., Skandamis, P. Listeria monocytogenes sublethal injury and viable-but-nonculturable state induced by acidic conditions and disinfectants. Microbiology Spectrum. 9(3): e01377-21 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azevedo, I., Regalo, M., Mena, C., Almeida, G., Carneiro, L., Teixeira, P., ... & Gibbs, P. A. Incidence of Listeria spp. in domestic refrigerators in Portugal. Food control. 16(2): 121-124 (2005)

    Article  Google Scholar 

  • Bae, D., Liu, C., Zhang, T., Jones, M., Peterson, S. N., Wang, C. Global gene expression of Listeria monocytogenes to salt stress. Journal of Food Protection. 75(5): 906-912 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Bai, X., Liu, D., Xu, L., Tenguria, S., Drolia, R., Gallina, N. L., ... Bhunia, A. K. Biofilm-isolated Listeria monocytogenes exhibits reduced systemic dissemination at the early (12–24 h) stage of infection in a mouse model. npj Biofilms and Microbiomes. 7(1): 18 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barbosa, J., Borges, S., Camilo, R., Magalhães, R., Ferreira, V., Santos, I., ... Teixeira, P. Biofilm formation among clinical and food isolates of Listeria monocytogenes. International Journal of Microbiology. 2013: 524975 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  • Begley, M., Hill, C. Stress adaptation in foodborne pathogens. Annual Review of Food Science and Technology. 6: 191-210 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Bergholz, T. M., Bowen, B., Wiedmann, M., Boor, K. J. Listeria monocytogenes shows temperature-dependent and-independent responses to salt stress, including responses that induce cross-protection against other stresses. Applied and Environmental Microbiology. 78(8): 2602-2612 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beumer, R. R., Te Giffel, M. C., Spoorenberg, E., & Rombouts, F. M. Listeria species in domestic environments. Epidemiology & Infection. 117(3): 437-442 (1996)

    Article  CAS  Google Scholar 

  • Bhavaniramya, S., Vishnupriya, S., Al-Aboody, M. S., Vijayakumar, R., Baskaran, D. Role of essential oils in food safety: Antimicrobial and antioxidant applications. Grain & Oil Science and Technology. 2(2): 49-55 (2019)

    Article  Google Scholar 

  • Bjarnsholt, T. The role of bacterial biofilms in chronic infections. Apmis. 121(s136): 1-58 (2013)

    Article  Google Scholar 

  • Borrusso, P. A., Quinlan, J. J. Prevalence of pathogens and indicator organisms in home kitchens and correlation with unsafe food handling practices and conditions. Journal of Food Protection. 80(4): 590-597 (2017)

    Article  PubMed  Google Scholar 

  • Bremer, P. J., Monk, I., Butler, R. Inactivation of Listeria monocytogenes/Flavobacterium spp. biofilms using chlorine: impact of substrate, pH, time and concentration. Letters in Applied Microbiology. 35(4): 321-325 (2002)

    Article  CAS  PubMed  Google Scholar 

  • Bucur, F. I., Grigore-Gurgu, L., Crauwels, P., Riedel, C. U., Nicolau, A. I. Resistance of Listeria monocytogenes to stress conditions encountered in food and food processing environments. Frontiers in Microbiology. 9: 2700 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Burnett, J., Wu, S. T., den Bakker, H. C., Cook, P. W., Veenhuizen, D. R., Hammons, S. R., ... Oliver, H. F. Listeria monocytogenes is prevalent in retail produce environments but Salmonella enterica is rare. Food Control. 113: 107173 (2020)

    Article  CAS  Google Scholar 

  • Byun, K. H., Han, S. H., Choi, M. W., Kim, B. H., Park, S. H., Ha, S. D. Biofilm eradication ability of phage cocktail against Listeria monocytogenes biofilms formed on food contact materials and effect on virulence-related genes and biofilm structure. Food Research International. 157: 111367 (2022a)

    Article  CAS  PubMed  Google Scholar 

  • Byun, K. H., Han, S. H., Choi, M. W., Park, S. H., Ha, S. D. Isolation, characterization, and application of bacteriophages to reduce and inhibit Listeria monocytogenes in celery and enoki mushroom. Food Control. 135: 108826 (2022b)

    Article  CAS  Google Scholar 

  • Carrascosa, C., Raheem, D., Ramos, F., Saraiva, A., Raposo, A. Microbial biofilms in the food industry—A comprehensive review. International Journal of Environmental Research and Public Health. 18(4): 2014 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castrica, M., Andoni, E., Intraina, I., Curone, G., Copelotti, E., Massacci, F. R., ... & Balzaretti, C. M. Prevalence of Listeria monocytogenes and Salmonella spp. in different ready to eat foods from large retailers and canteens over a 2-year period in Northern Italy. International Journal of Environmental Research and Public Health. 18(20): 10568 (2021)

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapin, T. K., Nightingale, K. K., Worobo, R. W., Wiedmann, M., & Strawn, L. K. Geographical and meteorological factors associated with isolation of Listeria species in New York State produce production and natural environments. Journal of Food Protection. 77(11): 1919-1928 (2014)

    Article  PubMed  Google Scholar 

  • Chaturongakul, S., Raengpradub, S., Wiedmann, M., Boor, K. J. Modulation of stress and virulence in Listeria monocytogenes. Trends in Microbiology. 16(8): 388-396 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen, M., Cheng, J., Zhang, J., Chen, Y., Zeng, H., Xue, L., ... Wu, Q. Isolation, potential virulence, and population diversity of Listeria monocytogenes from meat and meat products in China. Frontiers in Microbiology. 10: 946 (2019)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng, C., Dong, Z., Han, X., Sun, J., Wang, H., Jiang, L., ... Song, H. Listeria monocytogenes 10403S arginine repressor ArgR finely tunes arginine metabolism regulation under acidic conditions. Frontiers in Microbiology. 8: 145 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Conficoni, D., Losasso, C., Cortini, E., Di Cesare, A., Cibin, V., Giaccone, V., ... Ricci, A. Resistance to biocides in Listeria monocytogenes collected in meat-processing environments. Frontiers in Microbiology. 7: 1627 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Cordero, N., Maza, F., Navea-Perez, H., Aravena, A., Marquez-Fontt, B., Navarrete, P., ... Reyes-Jara, A. Different transcriptional responses from slow and fast growth rate strains of Listeria monocytogenes adapted to low temperature. Frontiers in Microbiology. 7: 229 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Cotter, P. D., Gahan, C. G., & Hill, C. Analysis of the role of the Listeria monocytogenes F0F1-ATPase operon in the acid tolerance response. International Journal of Food Microbiology. 60(2-3): 137-146 (2000)

    Article  CAS  PubMed  Google Scholar 

  • Cotter, P. D., Gahan, C. G., Hill, C. A glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Molecular Microbiology. 40(2): 465-475 (2001)

    Article  CAS  PubMed  Google Scholar 

  • Curtis, T. D., Gram, L., Knudsen, G. M. The small colony variant of Listeria monocytogenes is more tolerant to antibiotics and has altered survival in RAW 264.7 murine macrophages. Frontiers in Microbiology. 7: 1056 (2016)

    Article  PubMed  PubMed Central  Google Scholar 

  • Davies, D. Understanding biofilm resistance to antibacterial agents. Nature Reviews Drug discovery. 2(2): 114-122 (2003)

    Article  CAS  PubMed  Google Scholar 

  • Dewey-Mattia, D., Manikonda, K., Hall, A. J., Wise, M. E., Crowe, S. J. Surveillance for foodborne disease outbreaks—United States, 2009–2015. MMWR Surveillance Summaries. 67(10): 1−11 (2018)

    Article  PubMed Central  Google Scholar 

  • Donaghy, J. A., Jagadeesan, B., Goodburn, K., Grunwald, L., Jensen, O. N., Jespers, A. D., ... & Quentin, M. C. Relationship of sanitizers, disinfectants, and cleaning agents with antimicrobial resistance. Journal of Food Protection. 82(5): 889-902 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Donlan, R. M. Biofilms: microbial life on surfaces. Emerging infectious diseases. 8(9): 881 (2002)

    Article  PubMed  PubMed Central  Google Scholar 

  • Ells, T. C., Truelstrup Hansen, L. Increased thermal and osmotic stress resistance in Listeria monocytogenes 568 grown in the presence of trehalose due to inactivation of the phosphotrehalase-encoding gene treA. Applied and Environmental Microbiology. 77(19): 6841-6851 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galie, S., García-Gutiérrez, C., Miguélez, E. M., Villar, C. J., Lombó, F. Biofilms in the food industry: health aspects and control methods. Frontiers in Microbiology. 9: 898 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Garmyn, D., Gal, L., Lemaitre, J. P., Hartmann, A., Piveteau, P. Communication and autoinduction in the species Listeria monocytogenes: A central role for the agr system. Communicative & Integrative Biology. 2(4): 371-374 (2009)

    Article  Google Scholar 

  • GelbíčoVá, T., KaRpíšKoVá, R. Outdoor environment as a source of Listeria monocytogenes in food chain. Czech Journal of Food Sciences. 30(1): 83-88 (2012)

    Article  Google Scholar 

  • Gill, C. O., Reichel, M. P. Growth of the cold-tolerant pathogens Yersinia enterocolitica, Aeromonas hydrophila and Listeria monocytogenes on high-pH beef packaged under vacuum or carbon dioxide. Food Microbiology. 6(4): 223-230 (1989)

    Article  Google Scholar 

  • Goh, S. G., Leili, A. H., Kuan, C. H., Loo, Y. Y., Lye, Y. L., San Chang, W., ... Son, R. Transmission of Listeria monocytogenes from raw chicken meat to cooked chicken meat through cutting boards. Food Control. 37: 51-55 (2014)

    Article  Google Scholar 

  • Golden, C. E., Rothrock Jr, M. J., Mishra, A. Comparison between random forest and gradient boosting machine methods for predicting Listeria spp. prevalence in the environment of pastured poultry farms. Food Research International. 122: 47-55 (2019)

    Article  PubMed  Google Scholar 

  • Gómez, D., Iguácel, L. P., Rota, M. C., Carramiñana, J. J., Ariño, A., Yangüela, J. Occurrence of Listeria monocytogenes in ready-to-eat meat products and meat processing plants in Spain. Foods. 4(3): 271-282 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Gorski, L., Cooley, M. B., Oryang, D., Carychao, D., Nguyen, K., Luo, Y., ... & Chen, Y. Prevalence and clonal diversity of over 1,200 Listeria monocytogenes isolates collected from public access waters near produce production areas on the central California coast during 2011 to 2016. Applied and Environmental Microbiology. 88(8): e00357-22 (2022)

    Article  PubMed  PubMed Central  Google Scholar 

  • Govaert, M., Smet, C., Verheyen, D., Walsh, J. L., Van Impe, J. F. Combined effect of cold atmospheric plasma and hydrogen peroxide treatment on mature Listeria monocytogenes and Salmonella Typhimurium biofilms. Frontiers in Microbiology. 10: 2674 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Gray, J. A., Chandry, P. S., Kaur, M., Kocharunchitt, C., Bowman, J. P., Fox, E. M. Novel biocontrol methods for Listeria monocytogenes biofilms in food production facilities. Frontiers in Microbiology. 9: 605 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Guan, N., Liu, L. Microbial response to acid stress: mechanisms and applications. Applied Microbiology and Biotechnology. 104(1): 51-65 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Guerreiro, D. N., Arcari, T., O’Byrne, C. P. The σB-Mediated general stress response of Listeria monocytogenes: life and death decision making in a pathogen. Frontiers in Microbiology. 11: 1505 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Guerreiro, D. N., Boyd, A., O'Byrne, C. P. The stressosome is required to transduce low pH signals leading to increased transcription of the amino acid-based acid tolerance mechanisms in Listeria monocytogenes. Access Microbiology. 4(9): 000455 (2022)

    Article  CAS  Google Scholar 

  • Guldimann, C., Guariglia-Oropeza, V., Harrand, S., Kent, D., Boor, K. J., & Wiedmann, M. Stochastic and differential activation of σB and PrfA in Listeria monocytogenes at the single cell level under different environmental stress conditions. Frontiers in Microbiology. 8: 348 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Hafner, L., Pichon, M., Burucoa, C., Nusser, S. H., Moura, A., Garcia-Garcera, M., & Lecuit, M. Listeria monocytogenes faecal carriage is common and depends on the gut microbiota. Nature Communications. 12(1): 6826 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hellström, S., Kiviniemi, K., Autio, T., & Korkeala, H. Listeria monocytogenes is common in wild birds in Helsinki region and genotypes are frequently similar with those found along the food chain. Journal of Applied Microbiology. 104(3): 883-888 (2008)

    Article  PubMed  Google Scholar 

  • Hill, D., Sugrue, I., Arendt, E., Hill, C., Stanton, C., Ross, R. P. Recent advances in microbial fermentation for dairy and health. F1000Research. 6: 751 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

  • Hingston, P. A., Piercey, M. J., Truelstrup Hansen, L. Genes associated with desiccation and osmotic stress in Listeria monocytogenes as revealed by insertional mutagenesis. Applied and Environmental Microbiology. 81(16): 5350-5362 (2015)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Høiby, N., Bjarnsholt, T., Givskov, M., Molin, S., Ciofu, O. Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents. 35(4): 322-332 (2010)

    Article  PubMed  Google Scholar 

  • Impens, F., Rolhion, N., Radoshevich, L., Bécavin, C., Duval, M., Mellin, J., ... Cossart, P. N-terminomics identifies Prli42 as a membrane miniprotein conserved in Firmicutes and critical for stressosome activation in Listeria monocytogenes. Nature Microbiology. 2(5): 1-12 (2017)

    Article  Google Scholar 

  • Jackson, V., Blair, I. S., McDowell, D. A., Kennedy, J., & Bolton, D. J. The incidence of significant foodborne pathogens in domestic refrigerators. Food control. 18(4): 346-351 (2007)

    Article  Google Scholar 

  • Jeong, D. K., Frank, J. F. Growth of Listeria monocytogenes at 10 °C in biofilms with microorganisms isolated from meat and dairy processing environments. Journal of Food Protection. 57(7): 576-586 (1994)

    Article  PubMed  Google Scholar 

  • Jiang, X., Zhou, L., Gao, D., Wang, Y., Wang, D., Zhang, Z., ... Shi, L. Expression of efflux pump gene lde in ciprofloxacin‐resistant foodborne isolates of Listeria monocytogenes. Microbiology and Immunology. 56(12): 843-846 (2012)

    Article  CAS  PubMed  Google Scholar 

  • Jiang, X., Yu, T., Xu, Y., Wang, H., Korkeala, H., Shi, L. MdrL, a major facilitator superfamily efflux pump of Listeria monocytogenes involved in tolerance to benzalkonium chloride. Applied Microbiology and Biotechnology. 103: 1339-1350 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Kallipolitis, B., Gahan, C. G., & Piveteau, P. Factors contributing to Listeria monocytogenes transmission and impact on food safety. Current Opinion in Food Science. 36: 9-17 (2020)

    Article  Google Scholar 

  • Karatzas, K. A. G., Suur, L., O'Byrne, C. P. Characterization of the intracellular glutamate decarboxylase system: analysis of its function, transcription, and role in the acid resistance of various strains of Listeria monocytogenes. Applied and Environmental Microbiology. 78(10): 3571-3579 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kayode, A. J., Semerjian, L., Osaili, T., Olapade, O., & Okoh, A. I. Occurrence of multidrug-resistant Listeria monocytogenes in environmental waters: a menace of environmental and public health concern. Frontiers in Environmental Science. 9: 737435 (2021)

    Article  Google Scholar 

  • Kazmierczak, M. J., Wiedmann, M., Boor, K. J. Contributions of Listeria monocytogenes σ B and PrfA to expression of virulence and stress response genes during extra-and intracellular growth. Microbiology. 152(6): 1827-1838 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Knudsen, G. M., Ng, Y., Gram, L. Survival of bactericidal antibiotic treatment by a persister subpopulation of Listeria monocytogenes. Applied and Environmental Microbiology. 79(23): 7390-7397 (2013)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korthals, M., Ege, M., Lick, S., von Mutius, E., & Bauer, J. Occurrence of Listeria spp. in mattress dust of farm children in Bavaria. Environmental Research. 107(3): 299-304 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Kovacevic, J., Ziegler, J., Wałecka-Zacharska, E., Reimer, A., Kitts, D. D., Gilmour, M. W. Tolerance of Listeria monocytogenes to quaternary ammonium sanitizers is mediated by a novel efflux pump encoded by emrE. Applied and Environmental Microbiology. 82(3): 939-953 (2016)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kragh, M. L., Muchaamba, F., Tasara, T., Hansen, L. T. Cold-shock proteins affect desiccation tolerance, biofilm formation and motility in Listeria monocytogenes. International Journal of Food Microbiology. 329: 108662 (2020)

    Article  CAS  PubMed  Google Scholar 

  • Kramarenko, T., Roasto, M., Meremäe, K., Kuningas, M., Põltsama, P., Elias, T. Listeria monocytogenes prevalence and serotype diversity in various foods. Food control. 30(1): 24-29 (2013)

    Article  CAS  Google Scholar 

  • Kremer, P. H. C., Lees, J. A., Koopmans, M. M., Ferwerda, B., Arends, A. W. M., Feller, M. M., ... Bentley, S. D. Benzalkonium tolerance genes and outcome in Listeria monocytogenes meningitis. Clinical Microbiology and Infection. 23(4): 265-e1 (2017)

    Article  PubMed  Google Scholar 

  • Kropac, A. C., Eshwar, A. K., Stephan, R., Tasara, T. New insights on the role of the pLMST6 plasmid in Listeria monocytogenes biocide tolerance and virulence. Frontiers in Microbiology. 10: 1538 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Kwon, H. J., Chen, Z., Evans, P., Meng, J., Chen, Y. Characterization of mobile genetic elements using long-read sequencing for tracking Listeria monocytogenes from food processing environments. Pathogens. 9(10): 822 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee, Y. J. Biofilm formation and physiological heterogeneity of Listeria monocytogenes. PhD thesis, Mississippi State University, Oktibbeha, MS, USA (2019)

  • Lee, Y. J., Wang, C. Links between S‐adenosylmethionine and Agr‐based quorum sensing for biofilm development in Listeria monocytogenes EGD‐e. MicrobiologyOpen. 9(5): e1015 (2020) Lemon, K. P., Freitag, N. E., Kolter, R. The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. Journal of Bacteriology. 192(15): 3969-3976 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee, K. W. K., Periasamy, S., Mukherjee, M., Xie, C., Kjelleberg, S., Rice, S. A. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. The ISME journal. 8(4): 894-907 (2014)

    Article  CAS  PubMed  Google Scholar 

  • Lemon, K. P., Freitag, N. E., Kolter, R. The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. Journal of Bacteriology. 192(15): 3969-3976 (2010)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, Y. H., Tian, X. Quorum sensing and bacterial social interactions in biofilms. Sensors. 12(3): 2519-2538 (2012)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, X., Hospital, X. F., Hierro, E., Fernández, M., Sheng, L., Wang, L. Formation of Listeria monocytogenes persister cells in the produce-processing environment. International Journal of Food Microbiology. 390: 110106 (2023)

    Article  CAS  PubMed  Google Scholar 

  • Liao, X., Ma, Y., Daliri, E. B. M., Koseki, S., Wei, S., Liu, D., ... Ding, T. Interplay of antibiotic resistance and food-associated stress tolerance in foodborne pathogens. Trends in Food Science & Technology. 95: 97-106 (2020)

    Article  CAS  Google Scholar 

  • Linton, R. H., Pierson, M. D., Bishop, J. R. Increase in heat resistance of Listeria monocytogenes Scott A by sublethal heat shock. Journal of Food Protection. 53(11): 924-927 (1990)

    Article  CAS  PubMed  Google Scholar 

  • Liu, Y., Orsi, R. H., Gaballa, A., Wiedmann, M., Boor, K. J., Guariglia-Oropeza, V. Systematic review of the Listeria monocytogenes σB regulon supports a role in stress response, virulence and metabolism. Future Microbiology. 14(9): 801-828 (2019)

    Article  CAS  PubMed  Google Scholar 

  • Matereke, L. T., Okoh, A. I. Listeria monocytogenes virulence, antimicrobial resistance and environmental persistence: A review. Pathogens. 9(7): 528 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Melo, J., Andrew, P. W., Faleiro, M. L. Listeria monocytogenes in cheese and the dairy environment remains a food safety challenge: The role of stress responses. Food Research International. 67: 75-90 (2015)

    Article  Google Scholar 

  • Mendum, M. L., Smith, L. T. Gbu glycine betaine porter and carnitine uptake in osmotically stressed Listeria monocytogenes cells. Applied and Environmental Microbiology. 68(11): 5647-5655 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miceli, A., Settanni, L. Influence of agronomic practices and pre-harvest conditions on the attachment and development of Listeria monocytogenes in vegetables. Annals of Microbiology. 69(3): 185-199 (2019)

    Article  CAS  Google Scholar 

  • Miller, M. B., Bassler, B. L. Quorum sensing in bacteria. Annual Reviews in Microbiology. 55(1): 165-199 (2001)

    Article  CAS  Google Scholar 

  • Muchaamba, F., Von Ah, U., Stephan, R., Stevens, M. J., Tasara, T. Deciphering the global roles of cold shock proteins in Listeria monocytogenes nutrient metabolism and stress tolerance. Frontiers in Microbiology. 13: 1057754 (2022)

    Article  PubMed  PubMed Central  Google Scholar 

  • Muhterem-Uyar, M., Dalmasso, M., Bolocan, A. S., Hernandez, M., Kapetanakou, A. E., Kuchta, T., ... Wagner, M. Environmental sampling for Listeria monocytogenes control in food processing facilities reveals three contamination scenarios. Food Control. 51: 94-107 (2015)

    Article  Google Scholar 

  • Nadon, C. A., Bowen, B. M., Wiedmann, M., Boor, K. J. Sigma B contributes to PrfA-mediated virulence in Listeria monocytogenes. Infection and Immunity. 70(7): 3948-3952 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nair, S., Derré, I., Msadek, T., Gaillot, O., Berche, P. CtsR controls class III heat shock gene expression in the human pathogen Listeria monocytogenes. Molecular Microbiology. 35(4): 800-811 (2000)

    Article  CAS  PubMed  Google Scholar 

  • O’Connor, L., O’leary, M., Leonard, N., Godinho, M., O’Reilly, C., Egan, J., & O’Mahony, R. The characterization of Listeria spp. isolated from food products and the food‐processing environment. Letters in Applied Microbiology. 51(5): 490-498 (2010)

    Article  PubMed  Google Scholar 

  • Okada, Y., Ohnuki, I., Suzuki, H., Igimi, S. Growth of Listeria monocytogenes in refrigerated ready-to-eat foods in Japan. Food Additives & Contaminants: Part A. 30(8): 1446-1449 (2013)

    Article  CAS  Google Scholar 

  • Orsi, R. H., Chaturongakul, S., Oliver, H. F., Ponnala, L., Gaballa, A., Wiedmann, M. Alternative σ Factors Regulate Overlapping as Well as Distinct Stress Response and Metabolic Functions in Listeria monocytogenes under Stationary Phase Stress Condition. Pathogens. 10(4): 411 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palma, F., Brauge, T., Radomski, N., Mallet, L., Felten, A., Mistou, M. Y., ... Midelet-Bourdin, G. Dynamics of mobile genetic elements of Listeria monocytogenes persisting in ready-to-eat seafood processing plants in France. BMC Genomics. 21(1): 1-20 (2020)

    Article  Google Scholar 

  • Parsons, C., Niedermeyer, J., Gould, N., Brown, P., Strules, J., Parsons, A. W., ... Kathariou, S. Listeria monocytogenes at the human–wildlife interface: Black bears (Ursus americanus) as potential vehicles for Listeria. Microbial Biotechnology. 13(3): 706-721 (2020)

    Article  PubMed  Google Scholar 

  • Perreten, V., Kollöffel, B., Teuber, M. Conjugal transfer of the Tn916-like transposon TnFO1 from Enterococcus faecalis isolated from cheese to other Gram-positive bacteria. Systematic and Applied Microbiology. 20(1): 27-38 (1997)

    Article  CAS  Google Scholar 

  • Plata, G., Henry, C. S., Vitkup, D. Long-term phenotypic evolution of bacteria. Nature. 517(7534): 369-372 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Poimenidou, S. V., Dalmasso, M., Papadimitriou, K., Fox, E. M., Skandamis, P. N., Jordan, K. Virulence gene sequencing highlights similarities and differences in sequences in Listeria monocytogenes serotype 1/2a and 4b strains of clinical and food origin from 3 different geographic locations. Frontiers in Microbiology. 9: 1103 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Pöntinen, A., Lindström, M., Skurnik, M., Korkeala, H. Screening of the two-component-system histidine kinases of Listeria monocytogenes EGD-e. LiaS is needed for growth under heat, acid, alkali, osmotic, ethanol and oxidative stresses. Food Microbiology. 65: 36-43 (2017)

    Article  PubMed  Google Scholar 

  • Rabin, N., Zheng, Y., Opoku-Temeng, C., Du, Y., Bonsu, E., Sintim, H. O. Biofilm formation mechanisms and targets for developing antibiofilm agents. Future Medicinal Chemistry. 7(4): 493-512 (2015)

    Article  CAS  PubMed  Google Scholar 

  • Raschle, S., Stephan, R., Stevens, M. J., Cernela, N., Zurfluh, K., Muchaamba, F., & Nüesch-Inderbinen, M. Environmental dissemination of pathogenic Listeria monocytogenes in flowing surface waters in Switzerland. Scientific Reports. 11(1): 9066 (2021)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro, V. B., Mujahid, S., Orsi, R. H., Bergholz, T. M., Wiedmann, M., Boor, K. J., Destro, M. T. Contributions of σB and PrfA to Listeria monocytogenes salt stress under food relevant conditions. International Journal of Food Microbiology. 177: 98-108 (2014)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riedel, C. U., Monk, I. R., Casey, P. G., Waidmann, M. S., Gahan, C. G., Hill, C. AgrD‐dependent quorum sensing affects biofilm formation, invasion, virulence and global gene expression profiles in Listeria monocytogenes. Molecular Microbiology. 71(5): 1177-1189 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Roedel, A., Dieckmann, R., Brendebach, H., Hammerl, J. A., Kleta, S., Noll, M., ... Vincze, S. Biocide-tolerant Listeria monocytogenes isolates from German food production plants do not show cross-resistance to clinically relevant antibiotics. Applied and Environmental Microbiology. 85(20): e01253-19 (2019)

    Article  PubMed  PubMed Central  Google Scholar 

  • Romanova, N. A., Wolffs, P. F. G., Brovko, L. Y., Griffiths, M. W. Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Applied and Environmental Microbiology. 72(5): 3498-3503 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutherford, S. T., Bassler, B. L. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor Perspectives in Medicine. 2(11): a012427 (2012)

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryan, S., Hill, C., Gahan, C. G. Acid stress responses in Listeria monocytogenes. Advance in Applied Microbiology. 65: 67-91 (2008)

    Article  CAS  Google Scholar 

  • Ryan, S., Begley, M., Gahan, C. G., Hill, C. Molecular characterization of the arginine deiminase system in Listeria monocytogenes: regulation and role in acid tolerance. Environmental Microbiology. 11(2): 432-445 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Salazar, J. K., Natarajan, V., Stewart, D., Fay, M., Gonsalves, L. J., Mhetras, T., ... Tortorello, M. L. Listeria monocytogenes growth kinetics in refrigerated ready-to-eat dips and dip components. Plos one. 15(6): e0235472 (2020)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sauders, B. D., Durak, M. Z., Fortes, E., Windham, K., Schukken, Y., Lembo Jr, A. J., ... Wiedmann, M. Molecular characterization of Listeria monocytogenes from natural and urban environments. Journal of Food Protection. 69(1): 93-105 (2006)

    Article  CAS  PubMed  Google Scholar 

  • Schmid, B., Klumpp, J., Raimann, E., Loessner, M. J., Stephan, R., Tasara, T. Role of cold shock proteins in growth of Listeria monocytogenes under cold and osmotic stress conditions. Applied and Environmental Microbiology. 75(6): 1621-1627 (2009)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schoder, D., Guldimann, C., Märtlbauer, E. Asymptomatic carriage of Listeria monocytogenes by animals and humans and its impact on the food chain. Foods. 11(21): 3472 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sergelidis, D., Abrahim, A. Adaptive response of Listeria monocytogenes to heat and its impact on food safety. Food Control. 20(1): 1-10 (2009)

    Article  CAS  Google Scholar 

  • Sibanda, T., Buys, E. M. Listeria monocytogenes pathogenesis: The role of stress adaptation. Microorganisms. 10(8): 1522 (2022)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simonsen, A. K. Environmental stress leads to genome streamlining in a widely distributed species of soil bacteria. The ISME Journal. 16(2): 423-434 (2022)

    Article  CAS  PubMed  Google Scholar 

  • Singh, S., Shalini, R. Effect of hurdle technology in food preservation: a review. Critical Reviews in Food Science and Nutrition. 56(4): 641-649 (2016)

    Article  CAS  PubMed  Google Scholar 

  • Singh, S., Singh, S. K., Chowdhury, I., Singh, R. Understanding the mechanism of bacterial biofilms resistance to antimicrobial agents. The Open Microbiology Journal. 11: 53 (2017)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skandamis, P. N., Yoon, Y., Stopforth, J. D., Kendall, P. A., Sofos, J. N. Heat and acid tolerance of Listeria monocytogenes after exposure to single and multiple sublethal stresses. Food Microbiology. 25(2): 294-303 (2008)

    Article  CAS  PubMed  Google Scholar 

  • Sleator, R. D., Wouters, J., Gahan, C. G., Abee, T., & Hill, C. Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes. Applied and Environmental Microbiology. 67(6): 2692-2698 (2001)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith, J. L., Liu, Y., Paoli, G. C. How does Listeria monocytogenes combat acid conditions?. Canadian Journal of Microbiology. 59(3): 141-152 (2013)

    Article  CAS  PubMed  Google Scholar 

  • Stoller, A., Stevens, M. J., Stephan, R., Guldimann, C. Characteristics of Listeria monocytogenes strains persisting in a meat processing facility over a 4-year period. Pathogens. 8(1): 32 (2019)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taherkhani, A., Movahedian Attar, H., Ahmad Moazzam, M. M., Mirzaee, S. A., & Jalali, M. Prevalence of Listeria monocytogenes in the river receiving the effluent of municipal wastewater treatment plant. International Journal of Environmental Health Engineering. 2(November): 1-5 (2013)

    CAS  Google Scholar 

  • Tapia, N. C., Dorey, A. L., Gahan, C. G., den Besten, H. M., O'Byrne, C. P., Abee, T. Different carbon sources result in differential activation of sigma B and stress resistance in Listeria monocytogenes. International Journal of Food Microbiology. 320: 108504 (2020)

    Article  Google Scholar 

  • Utratna, M., Shaw, I., Starr, E., & O'Byrne, C. P. Rapid, transient, and proportional activation of σB in response to osmotic stress in Listeria monocytogenes. Applied and Environmental Microbiology. 77(21): 7841-7845 (2011)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van der Veen, S., Hain, T., Wouters, J. A., Hossain, H., de Vos, W. M., Abee, T., ... Wells-Bennik, M. H. The heat-shock response of Listeria monocytogenes comprises genes involved in heat shock, cell division, cell wall synthesis, and the SOS response. Microbiology. 153(10): 3593-3607 (2007)

    Article  PubMed  Google Scholar 

  • Van Houdt, R., Michiels, C. W. Biofilm formation and the food industry, a focus on the bacterial outer surface. Journal of Applied Microbiology. 109(4): 1117-1131 (2010)

    Article  PubMed  Google Scholar 

  • Wang, Y., Lu, L., Lan, R., Salazar, J. K., Liu, J., Xu, J., & Ye, C. Isolation and characterization of Listeria species from rodents in natural environments in China: Isolation and characterization of Listeria species. Emerging Microbes & Infections. 6(1): 1-6 (2017)

    Google Scholar 

  • Wemekamp-Kamphuis, H. H., Karatzas, A. K., Wouters, J. A., Abee, T. Enhanced levels of cold shock proteins in Listeria monocytogenes LO28 upon exposure to low temperature and high hydrostatic pressure. Applied and Environmental Microbiology. 68(2): 456-463 (2002)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wesche, A. M., Gurtler, J. B., Marks, B. P., Ryser, E. T. Stress, sublethal injury, resuscitation, and virulence of bacterial foodborne pathogens. Journal of Food Protection. 72(5): 1121-1138 (2009)

    Article  CAS  PubMed  Google Scholar 

  • Wiktorczyk-Kapischke, N., Skowron, K., Grudlewska-Buda, K., Wałecka-Zacharska, E., Korkus, J., Gospodarek-Komkowska, E. Adaptive response of Listeria monocytogenes to the stress factors in the food processing environment. Frontiers in Microbiology. 12:710085 (2021)

    Article  PubMed  PubMed Central  Google Scholar 

  • Wrande, M., Roth, J. R., Hughes, D. Accumulation of mutants in “aging” bacterial colonies is due to growth under selection, not stress-induced mutagenesis. Proceedings of the National Academy of Sciences. 105(33): 11863-11868 (2008)

    Article  CAS  Google Scholar 

  • Wu, S., Wu, Q., Zhang, J., Chen, M., Yan, Z. A., Hu, H. Listeria monocytogenes prevalence and characteristics in retail raw foods in China. PLoS One. 10(8): e0136682 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu, S., Yu, P. L., Flint, S. Persister cell formation of Listeria monocytogenes in response to natural antimicrobial agent nisin. Food Control. 77: 243-250 (2017)

    Article  CAS  Google Scholar 

  • Yan, H., Neogi, S. B., Mo, Z., Guan, W., Shen, Z., Zhang, S., ... & Zhong, N. Prevalence and characterization of antimicrobial resistance of foodborne Listeria monocytogenes isolates in Hebei province of Northern China, 2005–2007. International Journal of Food Microbiology. 144(2): 310-316 (2010)

    Article  CAS  PubMed  Google Scholar 

  • Yoon, J. H., Jeong, D. Y., Lee, S. B., Choi, S., Jeong, M. I., Lee, S. Y., Kim, S. R. Decontamination of Listeria monocytogenes in king oyster mushrooms (Pleurotus eryngii) by combined treatments with organic acids, nisin, and ultrasound. LWT. 144: 111207 (2021)

    Article  CAS  Google Scholar 

  • Yu, T., Jiang, X., Zhang, Y., Ji, S., Gao, W., Shi, L. Effect of benzalkonium chloride adaptation on sensitivity to antimicrobial agents and tolerance to environmental stresses in Listeria monocytogenes. Frontiers in Microbiology. 9: 2906 (2018)

    Article  PubMed  PubMed Central  Google Scholar 

  • Yuan, L., Sadiq, F. A., Wang, N., Yang, Z., He, G. Recent advances in understanding the control of disinfectant-resistant biofilms by hurdle technology in the food industry. Critical Reviews in Food Science and Nutrition. 61(22): 3876-3891 (2021)

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Y., Burkhardt, D. H., Rouskin, S., Li, G. W., Weissman, J. S., Gross, C. A. A stress response that monitors and regulates mRNA structure is central to cold shock adaptation. Molecular Cell. 70(2): 274-286: (2018)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, L., Zhang, Y., Ge, Y., Zhu, X., Pan, J. Regulatory mechanisms and promising applications of quorum sensing-inhibiting agents in control of bacterial biofilm formation. Frontiers in Microbiology. 11: 589640 (2020)

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu, Q., Gooneratne, R., Hussain, M. A. Listeria monocytogenes in fresh produce: outbreaks, prevalence and contamination levels. Foods. 6(3): 21 (2017)

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This study was supported by a grant from the Main Research Program of the Korea Food Research Institute (Grant Number: E0210702-03).

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  1. Food Safety and Distribution Research Group, Korea Food Research Institute, Jeollabuk-Do, Wanju, 55365, Republic of Korea

    Kye-Hwan Byun & Hyun Jung Kim

  2. Department of Food Biotechnology, University of Science and Technology, Daejeon, 34113, Republic of Korea

    Hyun Jung Kim

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Byun, KH., Kim, H.J. Survival strategies of Listeria monocytogenes to environmental hostile stress: biofilm formation and stress responses. Food Sci Biotechnol 32, 1631–1651 (2023). https://doi.org/10.1007/s10068-023-01427-6

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