Skip to main content

The Listeria monocytogenes Triad for Success: Food Matrix, Stress Response and Virulence

  • Chapter
  • First Online:
Foodborne Pathogens

Part of the book series: Food Microbiology and Food Safety ((PRACT))

Abstract

As with most foodborne pathogens, Listeria monocytogenes, during its life cycle, encounters many environmental stresses, beginning with its residence in soil, through the food production chain until it encounters host challenges to accomplish a successful infection process. Exposure to a single stress or a combination of stresses can compromise the integrity of the bacterial cell, and to circumvent those injuries the pathogen is equipped with mechanisms that can sense sublethal stress and trigger its gene expressing arsenal to reprogram its mode of survival by expressing stress tolerance factors. Such tolerance factors were initially identified using laboratory media. However, these approaches did not reliably translate those tolerance responses in real food matrices that the pathogen requires, and the molecular elements associated with those responses. Using different omics approaches, recent studies are revealing the tolerance responses associated with different food matrices and their possible impact in enabling the pathogen to better survive in vivo stress challenges. This knowledge is useful for developing new and more efficient control strategies and improving food safety, especially for minimally processed foods.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abdullah, D., & Calicioglu, M. (2013). Survival of Listeria monocytogenes during production and ripening of traditional Turkish Savak Tulum cheese and in synthetic gastric fluid. Journal of Food Protection, 76, 1801–1805.

    Article  CAS  Google Scholar 

  • Abram, F., Starr, E., Karatzas, K. A. G., Matlawska-Wasowska, K., Boyd, A., Wiedmann, M., Boor, K. J., Connally, D., & O’Byrne, C. P. (2008). Identification of components of the SigB regulon in Listeria monocytogenes that contribute to acid and salt tolerance. Applied and Environmental Microbiology, 74, 6848–6858.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Adrião, A., Vieira, M., Fernandes, I., Barbosa, M., Sol, M., Tenreiro, R. P., Chambel, L., Barata, B., Zilhao, I., Shama, G., Perni, S., Jordan, S. J., Andrew, P. J., & Faleiro, M. L. (2008). Marked intra-strain variation in response of Listeria monocytogenes dairy isolates to acid or salt stress and the effect of acid or salt adaptation on adherence to abiotic surfaces. International Journal of Food Microbiology, 123, 142–150.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Archambauld, C., Nahori, M. A., Pizarro-Cerda, J., Cossart, P., & Dussurget, O. (2006). Control of Listeria superoxide dismutase by phosphorylation. The Journal of Biological Chemistry, 281, 31812–31822.

    Article  CAS  Google Scholar 

  • Arguedas-Villa, C., Stephan, R., & Tasara, T. (2010). Evaluation of cold growth and related gene transcription responses associated with Listeria monocytogenes strains of different origins. Food Microbiology, 27, 653–660.

    Article  CAS  PubMed  Google Scholar 

  • Al-Nabulsi, A. A., Osaili, T. M., Shaker, R. R., Olaimat, A. N., Jaradat, Z. W., Elabedeen, N. A. Z., & Holley, R. A. (2015). Effects of osmotic pressure, acid, or cold stresses on antibiotic susceptibility of Listeria monocytogenes. Food Microbiology, 46, 154–160.

    Article  CAS  PubMed  Google Scholar 

  • Alessandria, V., Rantsiou, K., Dolci, P., Zeppa, G., & Cocolin, L. (2013). A comparison of gene expression of Listeria monocytogenes in vitro and in the soft cheese Crescenza. International Journal of Dairy Technology, 66, 83–89.

    Article  CAS  Google Scholar 

  • Allen, K. J., Watecka-Zacharska, E., Chen, J. C., Kosek-Paszkowska, K., Devlieghere, F., Meervenne, E. V., Osek, J., Wieczorek, K., & Bania, J. (2015). Listeria monocytogenes – An examination of food chain factors potentially contributing to antimicrobial resistance. Food Microbiology. doi:10.1016/j.fm.2014.08.006.

    Google Scholar 

  • Allerberger, F., & Wagner, M. (2010). Listeriosis: A resurgent foodborne infection. Clinical Microbiology and Infection, 16, 16–23.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Alonso-Hernando, A., Alonso-Calleja, C., & Capita, R. (2010). Effects of exposure to poultry chemical decontaminants on the membrane fluidity of Listeria monocytogenes and Salmonella enterica strains. International Journal of Food Microbiology, 137, 130–136.

    Article  CAS  PubMed  Google Scholar 

  • Antunes, P., Réu, C., Sousa, J. C., Pestana, N., & Peixe, L. (2002). Incidence and susceptibility to antimicrobial agents of Listeria spp. and Listeria monocytogenes isolated from poultry carcasses in Porto, Portugal. Journal of Food Protection, 65, 1888–1893.

    Article  CAS  PubMed  Google Scholar 

  • Barbosa, J., Borges, S., Magalhães, R., Ferreira, V., Santos, I., Silva, J., Almeida, G., Gibbs, P., & Teixeira, P. (2012). Behaviour of Listeria monocytogenes isolates through gastro-intestinal tract passage simulation, before and after two sub-lethal stresses. Food Microbiology, 30, 24–28.

    Article  CAS  PubMed  Google Scholar 

  • Barbosa, J., Magalhães, R., Santos, I., Ferreira, V., Brandão, T. R. S., Silva, J., Almeida, G., & Teixeira, P. (2013). Evaluation of antibiotic resistance patterns of food and clinical Listeria monocytogenes isolates in Portugal. Foodborne Pathogens and Disease, 10, 861–866.

    Article  CAS  PubMed  Google Scholar 

  • Barmpalia-Davis, I. M., Geornaras, I., Kendall, P. A., & Sofos, J. N. (2008). Differences in survival among thirteen Listeria monocytogenes strains in a dynamic model of the stomach and small intestine. Applied and Environmental Microbiology, 74, 5563–5567.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barmpalia-Davis, I. M., Geornaras, I., Kendall, P. A., & Sofos, J. N. (2009). Effect of fat content on survival of Listeria monocytogenes during simulated digestion of inoculated beef frankfurters stored at 7°C. Food Microbiology, 26, 483–490.

    Article  CAS  PubMed  Google Scholar 

  • Begley, M., Gahan, C. G. M., & Hill, C. (2002). Bile stress response in Listeria monocytogenes LO28: Adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Applied and Environmental Microbiology, 68, 6005–6012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begley, M., Sleator, R. D., Gahan, C. G. M., & Hill, C. (2005). Contribution of three bile associated loci, bsh, pva, and btlB, to gastrointestinal persistence and bile tolerance of Listeria monocytogenes. Infection and Immunity, 73, 894–904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begley, M., Kerr, C., & Hill, C. (2009). Exposure to bile influences biofilm formation by Listeria monocytogenes. Gut Pathogens, 1, 1–4.

    Article  CAS  Google Scholar 

  • Bergholz, T. M., den Bakker, H. C., Fortes, E. D., Boor, K. J., & Wiedmann, M. (2010). Salt stress phenotypes in Listeria monocytogenes vary by genetic lineage and temperature. Foodborne Pathogens and Disease, 7, 1537–1549.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bergholz, T. M., Bowen, B., Wiedmann, M., & Boor, K. J. (2012). 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, 2602–2612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bergholz, T. M., Tang, S., Wiedmann, M., & Boor, K. J. (2013). Nisin resistance of Listeria monocytogenes is increased by exposure to salt stress and is mediated via LiaR. Applied and Environmental Microbiology, 79, 5682–5688.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bertsch, D., Muelli, M., Weller, M., Uruty, A., Lacroix, C., & Meile, L. (2014). Antimicrobial susceptibility and antibiotic resistance gene transfer analysis of foodborne, clinical, and environmental Listeria spp. isolates including Listeria monocytogenes. Microbiology, 3, 118–127.

    CAS  Google Scholar 

  • Bonnet, M., & Montville, T. J. (2005). Acid-tolerant Listeria monocytogenes persist in a model food system fermented with nisin-producing bacteria. Letters in Applied Microbiology, 40, 237–242.

    Article  CAS  PubMed  Google Scholar 

  • Booth, I., Cash, P., & O’Byrne, C. (2002). Sensing and adapting to acid stress. Antonie Van Leeuwenhoek, 81, 33–42.

    Article  CAS  Google Scholar 

  • Bowman, J. P., Bittencourt, C. R., & Ross, T. (2008). Differential gene expression of Listeria monocytogenes during high hydrostatic pressure processing. Microbiology, 154, 462–475.

    Article  CAS  PubMed  Google Scholar 

  • Bowman, J. P., Chang, L., Pinfold, K. J., & Ross, T. (2010). Transcriptomic and phenotypic responses of Listeria monocytogenes strains possessing different growth efficiencies under acidic conditions. Applied and Environmental Microbiology, 76, 4836–4850.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brigulla, M., Hoffman, T., Krisp, A., Volker, A., Bremer, A., & Volker, U. (2003). Chill induction of SigB-dependent general stress response in Bacillus subtilis and its contribution to low-temperature adaptation. Journal of Bacteriology, 185, 4305–4314.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bubert, A., Kuhn, M., Goebel, W., & Kohler, S. (1992). Structural and functional properties of the p60 proteins from different Listeria species. Journal of Bacteriology, 174, 8166–8171.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burall, L. S., Laksanalamai, P., & Datta, A. R. (2012). Listeria monocytogenes mutants with altered growth phenotypes at refrigeration temperature and high salt concentrations. Applied and Environmental Microbiology, 78, 1265–1272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burall, L. S., Simpson, A. C., Chou, L., Laksanalamai, P., & Datta, A. R. (2015). A novel gene, lstC, of Listeria monocytogenes is implicated in high salt tolerance. Food Microbiology, 48, 72–82.

    Article  CAS  PubMed  Google Scholar 

  • CAC. Guidelines on the application of general principles of food hygiene to the control of Listeria monocytogenes in ready-to-eat foods – CAC/GL 61-2007. http://www.codexalimentarius.org/standards/list-of-standards/CAC/GL61-2007

  • Cacace, G., Mazzeo, M. F., Sorrentino, A., Spada, V., Malorni, A., & Siciçiano, R. A. (2010). Proteomics for the elucidation of cold adaptation mechanisms in Listeria monocytogenes. Journal of Proteomics, 73, 2021–2030.

    Article  CAS  PubMed  Google Scholar 

  • CDC. (1999). Update: Multistate outbreak of listeriosis, 1998-1999. MMWR, 47, 1117–1118.

    Google Scholar 

  • CDC. (2014). Incidence and trends of infection with pathogens transmitted commonly through food-foodborne diseases active surveillance network, 10 U.S. sites, 2006-2013. MMWR. Morbidity and Mortality Weekly Report, 63, 328–332.

    Google Scholar 

  • CDC. (2015). Incidence and trends of infection with pathogens transmitted commonly through food-foodborne diseases active surveillance network, 10 U.S. sites, 2006-2014. MMWR. Morbidity and Mortality Weekly Report, 64, 495–499.

    Google Scholar 

  • Callejón, R. M., Rodríguez-Naranjo, M. I., Ubeda, C., Hornedo-Ortega, R., Garcia-Parrilla, M. C., & Troncoso, A. M. (2015). Reported foodborne outbreaks due to fresh produce in the United States and European Union: Trends and causes. Foodborne Pathogens and Disease, 12, 32–38.

    Article  PubMed  Google Scholar 

  • Camargo, A. C., de Castilho, N. P. A., da Silva, D. A. L., Vallim, D. C., Hofer, E., & Nero, L. A. (2015). Antibiotic resistance of Listeria monocytogenes isolated from meat-processing environments, beef products, and clinical cases in Brazil. Microbial Drug Resistance, 21, 458–462.

    Article  CAS  PubMed  Google Scholar 

  • Camejo, A., Buchrieser, C., Couvé, E., Carvalho, F., Reis, O., Ferreira, P., Sousa, S., Cossart, P., & Cabanes, D. (2009). In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathogens, 5, e1000449.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carpentier, B., & Cerf, O. (2011). Persistence of Listeria monocytogenes in food industry equipments and premises. International Journal of Food Microbiology, 145, 1–8.

    Article  PubMed  Google Scholar 

  • Castanie-Cornet, M., Penfound, T. A., Smith, D., Elliott, J. F., & Foster, J. W. (1999). Control of acid resistance in Escherichia coli. Journal of Bacteriology, 181, 3525–3535.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cataldo, G., Conte, M. P., Chiarini, F., Seganti, L., Ammendolia, M. G., Superti, F., & Longhi, C. (2007). Acid adaptation and survival of Listeria monocytogenes in Italian-style soft cheeses. Journal of Applied Microbiology, 103, 185–193.

    Article  CAS  PubMed  Google Scholar 

  • Chan, P. F., Foster, S. J., Ingham, E., & Clements, M. O. (1998). Staphylococcus aureus alternative sigma factor sigma B controls the environmental stress response but not starvation survival or pathogenicity in a mouse abscess model. Journal of Bacteriology, 180, 6082–6089.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chan, Y. C., & Wiedmann, M. (2009). Physiology and genetics of Listeria monocytogenes survival and growth at cold temperatures. Critical Reviews in Food Science and Nutrition, 49, 237–253.

    Article  CAS  PubMed  Google Scholar 

  • Chen, J., Cheng, C., Xia, Y., Zhao, H., Fang, C., Shan, Y., Wu, B., & Fang, W. (2011). Lmo0036, an ornithine and putrescine carbamoyltransferase in Listeria monocytogenes, participates in arginine deiminase and agmatine deiminase pathways and mediates acid tolerance. Microbiology, 157, 3150–3161.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, C., Chen, J., Shan, Y., Fang, C., Liu, Y., Xia, Y., Song, H., & Wheihuan, F. (2013). Listeria monocytogenes ArcA contributes to acid tolerance. Journal of Medical Microbiology, 62, 813–821.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, C., Yang, Y., Dong, Z., Wang, X., Fang, C., Yang, M., Sun, J., Xiao, L., Wheihuan, F., & Song, H. (2015). Listeria monocytogenes varies among strains to maintain intracellular pH homeostasis under stresses by different acids as analyzed by a high-through microplate-based fluorometry. Frontiers in Microbiology, 6, 15.

    PubMed  PubMed Central  Google Scholar 

  • Cossart, P., & Lebreton, A. (2014). A trip in the “new microbiology” with the bacterial pathogen Listeria monocytogenes. FEBS Letters, 588, 2437–2445.

    Article  CAS  PubMed  Google Scholar 

  • Cotter, P. D., Emerson, N., Gahan, C. G. M., & Hill, C. (1999). Identification and disruption of lisRK, a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes. Journal of Bacteriology, 181, 6840–6843.

    CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cotter, P. D., Gahan, C. G., & Hill, C. A. (2001a). Glutamate decarboxylase system protects Listeria monocytogenes in gastric fluid. Molecular Microbiology, 40, 465–475.

    Article  CAS  PubMed  Google Scholar 

  • Cotter, P. D., O’Reilly, K., & Hill, C. (2001b). Role of the glutamate decarboxylase acid resistance system in the survival of Listeria monocytogenes LO28 in low pH foods. Journal of Food Protection, 64, 1362–1368.

    Article  CAS  PubMed  Google Scholar 

  • Cotter, P. D., & Hill, C. (2003). Surviving the acid test: Responses of Gram-positive bacteria to low pH. Microbiology and Molecular Biology Reviews, 67, 429–453.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cotter, P. D., Ryan, S., Gahan, C. G., & Hill, C. A. (2005). Presence of GadD1 glutamate decarboxylase in selected Listeria monocytogenes strains is associated with an ability to grow at low pH. Applied and Environmental Microbiology, 71, 2832–2839.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davis, M. J., Coote, P. J., & O’Byrne, C. P. (1996). Acid tolerance in Listeria monocytogenes: The adaptive acid tolerance response (ATR) and growth-phase-dependent acid resistance. Microbiology, 142, 2975–2982.

    Article  CAS  PubMed  Google Scholar 

  • Dowd, G., Hill, C., & Gahan, C. G. M. (2012). Responses of Listeria monocytogenes to different stresses. In H.-C. Wong (Ed.), Stress response of foodborne pathogens (pp. 405–444). New York: Nova Press.

    Google Scholar 

  • Duché, O., Trémoulet, F., Glaser, P., & Labadie, J. (2002a). Salt stress proteins induced in Listeria monocytogenes. Applied and Environmental Microbiology, 68, 1491–1498.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Duché, O., Trémoulet, F., Namane, A., The European Listeria genome Consortium, Labadie, J. (2002b). A proteomic analysis of the salt stress response of Listeria monocytogenes. FEMS Microbiology Letters, 215 183–8.

    Google Scholar 

  • Dussurget, O., Cabanes, D., Dehoux, P., Lecuit, M., Buchrieser, C., Glaser, P., & Cossart, P. (2002). Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis. Molecular Microbiology, 45, 1095–1106.

    Article  CAS  PubMed  Google Scholar 

  • EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). (2015a). The European Union summary report on trends and sources of Zoonoses, Zoonotic agents and food-borne outbreaks in 2013. EFSA Journal, 13(1), 3991.

    Article  Google Scholar 

  • EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). (2015b). The European Union summary report on trends and sources of Zoonoses, Zoonotic agents and food-borne outbreaks in 2014. EFSA Journal, 13(12), 4329.

    Google Scholar 

  • Francis, G. A., Scollard, J., Meally, A., Bolton, D. J., Gahan, C. G. M., Cotter, P. D., Hill, C., & O’Beirne, D. (2007). The glutamate decarboxylase acid resistance mechanism affects survival of Listeria monocytogenes LO28 in modified atmosphere-packaged foods. Journal of Applied Microbiology, 103, 2316–2324.

    Article  CAS  PubMed  Google Scholar 

  • Faleiro, M. L., Andrew, P. W., & Power, D. (2003). Stress response of Listeria monocytogenes isolated from cheese and other foods. International Journal of Food Microbiology, 84, 207–221.

    Article  CAS  PubMed  Google Scholar 

  • Faleiro, M. L. (2012). Response of foodborne bacteria to acid shock. In H.-C. Wong (Ed.), Stress response of foodborne pathogens (pp. 35–70). New York: Nova Press.

    Google Scholar 

  • Felicio, M. T., Hogg, T., Gibbs, P., Teixeira, P., & Wiedmann, M. (2007). Recurrent and sporadic Listeria monocytogenes contamination in alheiras represents considerable diversity, including virulence-attenuated isolates. Applied and Environmental Microbiology, 73, 3887–3895.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fraser, K. R., Sue, D., Wiedmann, M., Boor, K., & O’Byrne, C. P. (2003). Role of sigma B in regulating the compatible solute uptake systems of Listeria monocytogenes: Osmotic induction of opuC is sigma B dependent. Applied and Environmental Microbiology, 69, 2015–2022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira, A., O’Byrne, C. P., & Boor, K. J. (2001). Role of σB in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation. Applied and Environmental Microbiology, 67, 4454–4457.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira, A., Sue, D., O’Byrne, C. P., & Boor, K. J. (2003a). Role of Listeria monocytogenes σB in survival of lethal acidic conditions and in acquired acid tolerance response. Applied and Environmental Microbiology, 69, 2692–2698.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferreira, A., O’Byrne, C., & Boor, K. J. (2003b). Role of σB in heat, etanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Applied and Environmental Microbiology, 67, 4454–4457.

    Article  Google Scholar 

  • Freitag, N., Port, G. C., & Miner, M. D. (2009). Listeria monocytogenes – from saprophyte to intracellular pathogen. Nature Reviews. Microbiology, 7, 1–15.

    Article  CAS  Google Scholar 

  • Fritsch, F., Mauder, N., Williams, T., Weiser, J., Oberle, M., & Beier, D. (2011). The cell envelope stress response mediated by the LiaFSR three component system of Listeria monocytogenes is controlled via the phosphatase activity of the bifunctional histidine kinase LiaS. Microbiology, 157, 373–386.

    Article  CAS  PubMed  Google Scholar 

  • Gaillot, O., Pellegrini, E., Bregenholt, S., Nair, S., & Berche, P. (2000). The ClpP serine protease is essential for the intracellular parasitism and virulence of Listeria monocytogenes. Molecular Microbiology, 35, 1286–1294.

    Article  CAS  PubMed  Google Scholar 

  • Gaillot, O., Bregenholt, S., Jaubert, F., Di Santo, J. P., & Berche, P. (2001). Stress-induced ClpP serine protease of Listeria monocytogenes is essential for induction of listeriolysin O-dependent protective immunity. Infection and Immunity, 69, 4938–4943.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardan, R., Cossart, P., & Labadie, J. (2003a). Identification of Listeria monocytogenes genes involved in salt and alkaline-pH tolerance. Applied and Environmental Microbiology, 69, 3137–3143.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gardan, R., Duché, O., Leroy-Sétrin, S., The European Genome Consortium, & Labadie, J. (2003b). Role of ctc from Listeria monocytogenes in osmotolerance. Applied and Environmental Microbiology, 69, 154–161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghandi, M., & Chikindas, M. L. (2007). Listeria: A foodborne pathogen that knows how to survive. International Journal of Food Microbiology, 113, 1–15.

    Article  Google Scholar 

  • Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., Berche, P., Bloecker, H., Brandt, P., Chakraborty, T., Charbit, A., Chetouani, F., Couvé, E., de Daruvar, A., Dehoux, P., Domann, E., Dominguéz-Bernal, G., Duchaud, E., Durant, L., Dussurget, O., Entian, K.-D., Fsihi, H., Garcia-del Portillo, F., Garrido, P., Gautier, L., Goebel, W., Gómez-López, N., Hain, T., Hauf, J., Jackson, D., Jones, L. M., Kaerst, U., Kreft, J., Kuhn, M., Kunst, F., Kurapkat, G., Madueño, E., Maitournam, A., Mata Vicente, J., Ng, E., Nedjari, H., Nordsiek, G., Novella, S., de Pablos, B., Pérez-Diaz, J.-C., Purcell, R., Remmel, B., Rose, M., Schlueter, T., Simões, N., Tierrez, A., Vázquez-Boland, J.-A., Voss, H., Wehland, J., & Cossart, P. (2001). Comparative genomics of Listeria species. Science, 294, 849–852.

    CAS  PubMed  Google Scholar 

  • Gómez, D., Azón, E., Marco, N., Carramiñana, J. J., Rota, C., Ariño, A., & Yangüela. (2014). Antimicrobial resistance of Listeria monocytogenes and Listeria innocua from meat products and meat-processing environment. Food Microbiology, 42, 61–65.

    Article  PubMed  CAS  Google Scholar 

  • Hain, T., Hossain, H., Chatterjee, S. S., Machata, S., Volk, U., Wagner, S., Benedikt, B., Haas, S., Kuenne, C. T., Billion, A., Otten, S., Pane-Farre, J., Engelmann, S., & Chakraborty, T. (2008). Temporal transcriptomic analysis of the Listeria monocytogenes EGD-e σB regulon. BMC Microbiology, 8, 20.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Harakeh, S., Saleh, I., Zouhairi, O., Baydoun, E., Barbour, E., & Alwan, N. (2009). Antimicrobial resistance of Listeria monocytogenes isolated from dairy-based food products. The Science of the Total Environment, 407, 4022–4027.

    Article  CAS  PubMed  Google Scholar 

  • Hill, C., Cotter, P. D., Sleator, R. D., & Gahan, C. G. M. (2002). Bacterial stress response in Listeria monocytogenes: Jumping the hurdles imposed by minimal processing. International Dairy Journal, 12, 273–283.

    Article  Google Scholar 

  • He, L., Deng, Q.-L., M-t, C., Wu, Q.-p., & Lu, Y.-J. (2015). Proteomics analysis of Listeria monocytogenes ATCC 19115 in response to simultaneous triple stresses. Archives of Microbiology, 197, 883–841.

    Article  CAS  Google Scholar 

  • Heavin, S. B., Brennan, O. M., Morrissey, J. P., & O’Byrne, C. P. (2009). Inhibition of Listeria monocytogenes by acetate, benzoate and sorbate: Weak acid tolerance is not influenced by the glutamate decarboxylase system. Letters in Applied Microbiology, 49, 179–185.

    Article  CAS  PubMed  Google Scholar 

  • Hu, Y., Oliver, H. F., Raengpradub, S., Palmer, M. E., Orsi, R. H., Wiedmann, M., & Boor, K. J. (2007a). Transcriptomic and phenotypic analyses suggest a network between the transcriptional regulators HrcA and sigma B in Listeria monocytogenes. Applied and Environmental Microbiology, 73, 7981–7991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu, Y., Raengpradub, S., Schwab, U., Loss, C., Orsi, R. H., Wiedmann, M., & Boor, K. J. (2007b). Phenotypic and transcriptomic analyses demonstrate interactions between the transcriptional regulators CtsR and sigma B in Listeria monocytogenes. Applied and Environmental Microbiology, 73, 7967–7980.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ilhak, O. I., Oksuztepe, G., Calicioglu, M., & Patir, B. (2011). Effect of acid adaptation and different salt concentrations on survival of Listeria monocytogenes in Turkish white cheese. Journal of Food Quality, 34, 379–385.

    Article  CAS  Google Scholar 

  • Imlay, J. (2002). How oxygen damages microbes: Oxygen tolerance and obligate anaerobiosis. Advances in Microbial Physiology, 46, 111–153.

    Article  CAS  PubMed  Google Scholar 

  • Ivy, R. A., Wiedmann, M., & Boor, K. J. (2012). Listeria monocytogenes grown at 7°C shows reduced acid survival and an altered transcriptional response to acid shock compared to L. monocytogenes grown at 37°C. Applied and Environmental Microbiology, 78, 3824–3836.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang, L., Olesen, I., Andersen, T., Fang, W., & Jespersen, L. (2010). Survival of Listeria monocytogenes in simulated gastrointestinal system and transcriptional profiling of stress-and adhesion-related genes. Foodborne Pathogens and Disease, 7, 267–274.

    Article  CAS  PubMed  Google Scholar 

  • Joyce, S. A., & Gahan, C. G. M. (2010). Molecular pathogenesis of Listeria monocytogenes in the alternative model host Galleria mellonella. Microbiology, 156, 3456–3468.

    Article  CAS  PubMed  Google Scholar 

  • Kastbjerg, V. G., & Gram, L. (2012). Industrial disinfectants do not select for resistance in Listeria monocytogenes following long term exposure. International Journal of Food Microbiology, 160, 11–15.

    Article  CAS  PubMed  Google Scholar 

  • Karatzas, K.-A. G., Suur, L., & O’Byrne, C. P. (2012). 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, 3571–3579.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kazmierczak, M. J., Mithoe, S. C., Boor, K. J., & Wiedmann, M. (2003). Listeria monocytogenes sigma B regulates stress response and virulence functions. Journal of Bacteriology, 185, 5722–5734.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khen, B. K., Lynch, O. A., Carroll, J., McDowell, D. A., & Duffy, G. (2015). Occurrence, antibiotic resistance and molecular characterization of Listeria monocytogenes in the beef chain in the republic of Ireland. Zoonoses and Public Health, 62, 11–17.

    CAS  PubMed  Google Scholar 

  • Kovacevic, J., Arguedas-Villa, C., Wozniak, A., Tasara, T., & Allen, K. J. (2013). Examination of food chain-derived Listeria monocytogenes strains of different serotypes reveals considerable diversity in inlA genotypes, mutability, and adaptation to cold temperatures. Applied and Environmental Microbiology, 79, 1915–1922.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koutsoumanis, K. P., Kendall, P. A., & Sofos, J. N. (2003). Effect of food processing – related stresses on acid tolerance of Listeria monocytogenes. Applied and Environmental Microbiology, 69, 7514–7516.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lado, B. H., & Yousef, A. E. (2007). Characteristics of Listeria monocytogenes important to food processors. In E. T. Ryser & E. H. Marth (Eds.), Listeria, listeriosis and food safety (pp. 157–214). Boca Raton (FL): CRC Press.

    Google Scholar 

  • Larsen, N., & Jespersen, L. (2015). Expression of virulence-related genes in Listeria monocytogenes grown on Danish hard cheese as affected by NaCl content. Foodborne Pathogens and Disease, 12, 536–544.

    Article  CAS  PubMed  Google Scholar 

  • Laursen, M. F., Bahl, M. I., Licht, T. R., Gram, L., & Knudsen, G. M. (2015). A single exposure to a sublethal pediocin concentration initiates a resistance-associated temporal cell envelope and general stress response in Listeria monocytogenes. Environmental Microbiology, 17, 1134–1151.

    Article  CAS  PubMed  Google Scholar 

  • Lin, J., Smith, M. P., Chapin, K. C., Baik, H. S., Bennett, G. N., & Foster, J. W. (1996). Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Applied and Environmental Microbiology, 62, 3094–3100.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Linnan, M. J., Mascola, L., Lou, X. D., Goulet, V., May, S., Salminen, C., Hird, D. W., Yonekura, M. L., Hayes, P., Weaver, R., Audurier, A., Plikaytis, B. D., Fannin, S. L., Kleks, A., & Broome, C. V. (1988). Epidemic listeriosis associated with Mexican-style cheese. The New England Journal of Medicine, 319, 823–828.

    Article  CAS  PubMed  Google Scholar 

  • Loepfe, C., Raimann, E., Stephan, R., & Tasara, T. (2010). Reduced host cell invasiveness and oxidative stress tolerance in double and triple csp gene family deletion mutants of Listeria monocytogenes. Foodborne Pathogens and Disease, 7, 775–783.

    Article  CAS  PubMed  Google Scholar 

  • Lou, Y., & Yousef, A. E. (1997). Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Applied and Environmental Microbiology, 63, 1252–1255.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lungu, B., Ricke, S. C., & Johnson, M. G. (2009). Growth, survival, proliferation and pathogenesis of Listeria monocytogenes under low oxygen or anaerobic conditions: A review. Food Microbiology, 15, 7–17.

    CAS  Google Scholar 

  • MacGowan, A. P., Bowker, K., McLauchlin, J., Bennet, P. M., & Reeves, D. S. (1994). The occurrence and seasonal changes in the isolation of Listeria spp. in shop bought food stuffs, human faeces, sewage and soil from urban sources. International Journal of Food Microbiology, 21, 325–334.

    Article  CAS  PubMed  Google Scholar 

  • Madeo, M., O’Riordan, N., Fuchs, T. M., Utratna, M., Karatzas, K. A., & O’Byrne, C. P. (2012). Thiamine plays a critical role in the acid tolerance of Listeria monocytogenes. FEMS Microbiology Letters, 326, 137–143.

    Article  CAS  PubMed  Google Scholar 

  • Makariti, I. P., Printezi, A., Kapetanakou, A. E., Zeaki, N., & Skandamis, P. N. (2015). Investigating boundaries of survival, growth and expression of genes associated with stress and virulence of Listeria monocytogenes in response to acid and osmotic stress. Food Microbiology, 45, 231–244.

    Article  CAS  PubMed  Google Scholar 

  • Matilla, M., Somervuo, P., Rattei, T., Korkeala, H., Staphan, R., & Tasara, T. (2012). Phenotypic and transcriptomic analyses of sigma L-dependent characteristics in Listeria monocytogenes EGD-e. Food Microbiology, 32, 152–164.

    Article  CAS  Google Scholar 

  • Melo, J., Andrew, P. W., & Faleiro, M. L. (2013a). Different assembly of acid and salt tolerance response in two dairy Listeria monocytogenes wild strains. Archives of Microbiology, 195, 339–348.

    Article  CAS  PubMed  Google Scholar 

  • Melo, J., Schrama, D., Andrew, P. W., & Faleiro, M. L. (2013b). Proteomic analysis shows that individual Listeria monocytogenes strains use different strategies in response to gastric stress. Foodborne Pathogens and Disease, 10, 107–119.

    Article  CAS  PubMed  Google Scholar 

  • Melo, J., Schrama, D., Hussey, S., Andrew, P. W., & Faleiro, M. L. (2013c). Listeria monocytogenes dairy isolates show a different proteome response to sequential exposure to gastric and intestinal fluids. International Journal of Food Microbiology, 163, 51–63.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Morvan, A., Moubareck, C., Leclercq, A., Herve-Bazin, M., Bremont, S., Lecuit, M., Courvalin, P., & Le Monnier, A. (2010). Antimicrobial resistance of Listeria monocytogenes strains isolated from humans in France. Antimicrobial Agents and Chemotherapy, 54, 2728–2731.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mujahid, S., Pechan, T., & Wang, C. (2008). Protein expression by Listeria monocytogenes grown on a RTE-meat matrix. International Journal Food Microbiology, 128, 203–211.

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nair, S., Milohanic, E., & Berche, P. (2000b). ClpC ATPase is required for cell adhesion and invasion of Listeria monocytogenes. Infection and Immunity, 68, 7061–7068.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nelson, K. E., Fouts, D. E., Mongodin, E. F., Ravel, J., TR, D. B., Kolonay, J. F., Rasko, D. A., Angiouli, S. V., Gill, S. R., Paulsen, I. T., Peterson, J., White, O., Nelson, W. C., Nierman, W., Beanan, M. J., Brinkac, L. M., Daugherty, S. C., Dodson, R. J., Durkin, A. S., Madupu, R., Haft, D. H., Selengut, J., Van Aken, S., Khouri, H., Fedorova, N., Forberger, H., Tran, B., Kathariou, S., Wonderling, L. D., Uhlich, G. A., Bayles, D. O., Luchanski, J. B., & Fraser, C. M. (2004). Whole genome comparisons of serotype 4b and 1/2a strains of the food-borne pathogen Listeria monocytogenes reveal new insights into the core genome components of this species. Nucleic Acids Research, 32, 2386–2395.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newell, D. G., Koopmans, M., Verhoef, L., Duizer, E., Aidara-Kane, A., Sprong, H., et al. (2010). Food-borne diseases—the challenges of 20 years ago still persist while new ones continue to emerge. International Journal of Food Microbiology, 139, S3–15.

    Article  PubMed  Google Scholar 

  • Nightingale, K. K., Ivy, R. A., Ho, A. J., Fortes, E. D., Njaa, B. L., Peters, R. M., & Wiedmann, M. (2008). inlA premature stop codons are common among Listeria monocytogenes isolates from foods and yield virulence-attenuated strains that confer protection against fully virulent strains. Applied and Environmental Microbiology, 74, 6570–6583.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nilsson, R. E., Latham, R., Mellefont, L., Ross, T., & Bowman, J. P. (2012). MudPIT analysis of alkaline tolerance by Listeria monocytogenes strains recovered as persistent food factory contaminants. Food Microbiology, 30, 187–196.

    Article  CAS  PubMed  Google Scholar 

  • Obaidat, M. M., Bani Salman, A. E., Lafi, S. Q., & Al-Abboodi, A. R. (2015). Characterization of Listeria monocytogenes from three countries and antibiotic resistance differences among countries and Listeria monocytogenes serogroups. Letters in Applied Microbiology, 60, 609–614.

    Article  CAS  PubMed  Google Scholar 

  • O’Driscoll, B., Gahan, C. G., & Hill, C. (1996). Adaptative acid tolerance response in Listeria monocytogenes: Isolation of an acid-tolerant mutant which demonstrates increased virulence. Applied and Environmental Microbiology, 62, 1693–1698.

    PubMed  PubMed Central  Google Scholar 

  • Okada, Y., Okada, N., S-i, M., Asakura, H., Yamamoto, S., & Igimi, S. (2006). The sigma factor RpoN (σ54) is involved in osmotolerance in Listeria monocytogenes. FEMS Microbiology Letters, 263, 54–60.

    Article  CAS  PubMed  Google Scholar 

  • Okada, Y., Makinob, S., Okada, N., Asakura, H., Yamamoto, S., & Igimi, S. (2008). Identification and analysis of the osmotolerance associated genes in Listeria monocytogenes. Food Additives and Contaminants, 25, 1089–1094.

    Article  CAS  PubMed  Google Scholar 

  • Olesen, I., Vogensen, F. K., & Jespersen, L. (2009). Gene transcription and virulence potential of Listeria monocytogenes strains after exposure to acidic and NaCl stress. Foodborne Pathogens and Disease, 6, 669–680.

    Article  CAS  PubMed  Google Scholar 

  • Olesen, I., Thorsen, L., & Jespersen, L. (2010). Relative transcription of Listeria monocytogenes virulence genes in liver pâtés with varying NaCl content. International Journal of Food Microbiology, 141, S60–S68.

    Article  CAS  PubMed  Google Scholar 

  • Olier, M., Rousseaux, S., Piveteau, P., Lemaitre, J.-P., Rousset, A., & Guzzo, J. (2004). Screening of glutamate decarboxylase activity and bile salt resistance of human asymptomatic carriage, clinical, food, and environmental isolates of Listeria monocytogenes. International Journal of Food Microbiology, 93, 87–99.

    Article  CAS  PubMed  Google Scholar 

  • Oliver, H. F., Orsi, R. H., Wiedmann, M., & Boor, K. J. (2013). Sigma (B) plays a limited role in the ability of Listeria monocytogenes strain F2365 to survive oxidative and acid stress and in its virulence characteristics. Journal of Food Protection, 76, 2079–2086.

    Article  CAS  PubMed  Google Scholar 

  • Panfill-Kuncewicz, H., Laniewska-Trokenheim, L., & Kuncewicz, A. (2009). Survival of Listeria monocytogenes in Tvorog packaged with the use of different methods. Milchwissenschaft, 64, 64–67.

    Google Scholar 

  • Peterson, L. D., Faith, N. G., & Czuprynski, C. J. (2007). Resistance of Listeria monocytogenes F2365 cells to synthetic gastric fluid is greater following growth on ready-to-eat deli turkey meat than in brain heart infusion broth. Journal of Food Protection, 70, 2589–2595.

    Article  PubMed  Google Scholar 

  • Phan-Thanh, L., Mahouin, F., & Alige, S. (2000). Acid responses of Listeria monocytogenes. International Journal of Food Microbiology, 55, 121–126.

    Article  CAS  PubMed  Google Scholar 

  • Pilgrim, S., Kolb-Mäurer, A., Gentschev, I., Goebel, W., & Kuhn, M. (2003). Deletion of the gene encoding p60 in Listeria monocytogenes leads to abnormal cell division and loss of actin-based motility. Infection and Immunity, 71, 3473–3484.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raengpradub, S., Wiedmann, M., & Boor, K. J. (2008). Comparative analysis of the σB-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Applied and Environmental Microbiology, 74, 158–171.

    Article  CAS  PubMed  Google Scholar 

  • Ramalheira, R., Almeida, M., Azeredo, J., Brandão, T. R. S., Almeida, G., Silva, J., & Teixeira, P. (2010). Survival of food isolates of Listeria monocytogenes through simulated gastrointestinal tract conditions. Foodborne Pathogens and Disease, 7, 121–128.

    Article  CAS  PubMed  Google Scholar 

  • Rantsiou, K., Mataragas, M., Alessandria, V., & Cocolin, L. (2012). Expression of virulence genes of Listeria monocytogenes in food. Journal of Food Safety, 32, 161–168.

    Article  CAS  Google Scholar 

  • Rea, R., Hill, C., & Gahan, C. G. M. (2005). Listeria monocytogenes PerR mutants display a small-colony phenotype, increased sensitivity to hydrogen peroxide, and significantly reduced murine virulence. Applied and Environmental Microbiology, 71, 8314–8322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro, M. H., Manha, S., & Brito, L. (2006). The effects of salt and pH stress on the growth rates of persistent strains of Listeria monocytogenes collected from specific ecological niches. Food Research International, 39, 816–822.

    Article  CAS  Google Scholar 

  • Roldgaard, B. B., Andersen, J. B., Hansen, T. B., Christensen, B. B., & Licht, T. R. (2009). Comparison of three Listeria monocytogenes strains in a guinea pig model simulating food-borne exposure. FEMS Microbiology Letters, 291, 88–94.

    Article  CAS  PubMed  Google Scholar 

  • Rouquette, C., Ripio, M. T., Pellegrini, E., Bolla, J. M., Tascon, R. I., Vazquez-Boland, J. A., & Berche, P. (1996). Identification of a ClpC ATPase required for stress tolerance and in vivo survival of Listeria monocytogenes. Molecular Microbiology, 21, 977–987.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Schrama, D., Helliwell, N., Neto, L., & Faleiro, M. L. (2013). Adaptation of Listeria monocytogenes in a simulated cheese medium: Effects on virulence using the Galleria mellonella infection model. Letters in Applied Microbiology, 51, 421–427.

    Article  CAS  Google Scholar 

  • Schärer, K., Stephan, R., & Tasara, T. (2013). Cold shock proteins contribute to the regulation of Listeriolysin O production in Listeria monocytogenes. Foodborne Pathogens and Disease, 10, 1023–1029.

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sewell, D., Allen, S. C. H., & Phillips, C. A. (2015). Oxygen limitation induces acid tolerance and impacts simulated gastro-intestinal transit in Listeria monocytogenes J0161. Gut Pathogens, 7, 11.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shen, Q., Soni, K. A., & Nannapaneni, R. (2015). Stability of sublethal acid stress adaptation and induced cross protection against lauric arginate in Listeria monocytogenes. International Journal of Food Microbiology, 203, 49–54.

    Article  CAS  PubMed  Google Scholar 

  • Silk, B. J., Date, K. A., Jackson, K. A., Pouillot, R., Holt, K. G., Graves, L. M., Ong, K. L., Hurd, S., Meyer, R., Marcus, R., Shiferaw, B., Norton, D. M., Medus, C., Zansky, S. M., Cronquist, A. B., Henao, O. L., Jones, T. F., Vugia, D. J., Farley, M. M., & Mahon, B. E. (2012). Invasive listeriosis in the foodborne diseases active surveillance network (FoodNet), 2004-2009: Further targeted prevention needed for higher-risk groups. Clinical Infectious Diseases, 54, S396–S404.

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sleator, R. D., Francis, G. A., Beirne, D. O., Gahan, C. G., & Hill, C. (2003). Betaine and carnitine uptake systems in Listeria monocytogenes affect growth and survival in foods and during infection. Journal of Applied Microbiology, 95, 839–846.

    Article  CAS  PubMed  Google Scholar 

  • Sleator, R. D., & Hill, C. (2005). A novel role for the LisRK two-component regulatory system in listerial osmotolerance. Clinical Microbiology and Infection, 11, 599–601.

    Article  CAS  PubMed  Google Scholar 

  • Sue, D., Fink, D., Wiedmann, M., & Boor, K. J. (2004). σB-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology, 150, 3843–3855.

    Article  CAS  PubMed  Google Scholar 

  • Suo, Y., Huang, Y., Liu, Y., Shi, C., & Shi, X. (2012). The expression of superoxide dismutase (SOD) and a putative ABC transporter permease is inversely correlated during biofilm formation in Listeria monocytogenes 4b G. PloS One, 7, e48467.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suo, Y., Liu, Y., Zhou, X., Huang, Y., Shi, C., Matthews, K., & Shi, X. (2014). Impact of sod on the expression of stress-related genes in Listeria monocytogenes 4b G with/without paraquat treatment. Journal of Food Science, 79, M1745–M1749.

    Article  CAS  PubMed  Google Scholar 

  • Swaminathan, B., & Gerner-Smidt, P. (2007). The epidemiology of human listeriosis. Microbes and Infection, 9, 1236–1243.

    Article  PubMed  Google Scholar 

  • Tamburro, M., Ripabelli, G., Vitullo, M., Dallman, T. J., Pontello, M., Amar, C. F. L., & Sammarco, M. L. (2015). Gene expression in Listeria monocytogenes exposed to sublethal concentration of benzalkonium chloride. Comparative Immunology, Microbiology and Infectious Diseases, 40, 31–39.

    Article  PubMed  Google Scholar 

  • Tang, S., Orsi, R. H., den Bakker, H. C., Wiedmann, M., Boor, K. J., & Bergholz, T. M. (2015). Transcriptome analysis of Listeria monocytogenes adaptation to growth on vacuum-packed cold smoked salmon. Applied and Environmental Microbiology. doi:10.1128/AEM.01752-15.

    Google Scholar 

  • Tasara, T., & Stephan, R. (2006). Cold stress tolerance of Listeria monocytogenes: A review of molecular adaptive mechanisms and food safety implications. Journal of Food Protection, 69, 1473–1484.

    Article  CAS  PubMed  Google Scholar 

  • Todd, E. (2007). Listeria: Risk assessment, regulatory control and economic impact. In E. T. Ryser & E. H. Marth (Eds.), Listeria listeriosis, and food safety (pp. 767–812). Marcel Dekker: New York.

    Chapter  Google Scholar 

  • Tompkin, R. (2002). Control of Listeria monocytogenes in the food-processing environment. Journal of Food Protection, 65, 709–725.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Van der Veen, S., Moezelaar, R., Abee, T., & Wells-Bennik, M. H. J. (2008). The growth limits of a large number of Listeria monocytogenes strains at combinations of stresses show serotype- and niche-specific traits. Journal of Applied Microbiology, 105, 1246–1258.

    Article  PubMed  Google Scholar 

  • Van der Veen, S., Abee, T., de Vos, W. M., & Wells-Bennik, M. H. J. (2009). Genome-wide screen for Listeria monocytogenes genes important for growth at high temperatures. FEMS Microbiology Letters, 295, 195–203.

    Article  PubMed  CAS  Google Scholar 

  • Van der Veen, S., van Scalkwijik, S., Molenaar, D., de Vos, W. M., Abee, T., & Wells-Bennik, M. H. (2010). The SOS response of Listeria monocytogenes is involved in stress resistance and mutagenesis. Microbiology, 156, 374–384.

    Article  PubMed  CAS  Google Scholar 

  • Van Stelten, A., Simpson, J. M., Ward, T. J., & Nightingale, K. K. (2010). Revelation by single-nucleotide polymorphism genotyping that mutations leading to a premature stop codon in inlA are common among Listeria monocytogenes isolates from ready-to-eat foods but not human listeriosis cases. Applied and Environmental Microbiology, 76, 2783–2790.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Stelten, A., Simpson, J. M., Chen, Y., Scott, V. N., Whiting, R. C., Ross, W. H., & Nightingale, K. K. (2011). Significant shift in median guinea pig infectious dose shown by an outbreak-associated Listeria monocytogenes epidemic clone strain and a strain carrying a premature stop codon mutation in inlA. Applied and Environmental Microbiology, 77, 2479–2487.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waldor, M. K., & Friedman, D. I. (2005). Phage regulatory circuits and virulence gene expression. Current Opinion in Microbiology, 8, 459–465.

    Article  CAS  PubMed  Google Scholar 

  • Wang, G., Qian, W., Zhang, X., Wang, H., Ye, K., Bai, Y., & Zhou, G. (2015). Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from ready-to-eat meat products in Nanjing, China. Food Control, 50, 202–208.

    Article  CAS  Google Scholar 

  • Walsh, D., Duffy, G., Sheridan, J. J., Blair, I. S., & McDowell, D. A. (2001). Antibiotic resistance among Listeria, including Listeria monocytogenes, in retail foods. Journal of Applied Microbiology, 90, 517–522.

    Article  CAS  PubMed  Google Scholar 

  • Watson, D., Sleator, R. D., Casey, P. G., Hill, C., & Gahan, G. M. C. (2009). Specific osmolyte transporters mediate bile tolerance in Listeria monocytogenes. Infection and Immunity, 77, 4895–4904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werbrouck, H., Vermeulen, A., Van Coillie, E., Messens, W., Herman, L., & Devlieghere, F. (2009). Influence of acid stress on survival, expression of virulence genes and invasion capacity into Caco-2 cells of Listeria monocytogenes strains of different origins. International Journal of Food Microbiology, 134, 140–146.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Q., Feng, Y., Deng, L., Feng, F., Wang, L., Zhou, Q., & Luo, Q. (2011). SigB plays a major role in Listeria monocytogenes tolerance to bile stress. International Journal of Food Microbiology, 145, 238–243.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Y., Carpenter, C. E., Broadbent, J. R., & Luo, X. (2015). Influence of habituation to inorganic and organic acid conditions on the cytoplasmic membrane composition of Listeria monocytogenes. Food Control, 55, 49–53.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maria Leonor Faleiro .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Faleiro, M.L. (2017). The Listeria monocytogenes Triad for Success: Food Matrix, Stress Response and Virulence. In: Gurtler, J., Doyle, M., Kornacki, J. (eds) Foodborne Pathogens. Food Microbiology and Food Safety(). Springer, Cham. https://doi.org/10.1007/978-3-319-56836-2_4

Download citation

Publish with us

Policies and ethics