Ethanol adaptation in foodborne bacterial pathogens

References

• Álvarez-Ordóñez, A., M. Prieto, A. Bernardo, C. Hill, and M. López. 2012. The acid tolerance response of Salmonella spp.: An adaptive strategy to survive in stressful environments prevailing in foods and the host. Food Research International 45 (2):482–92. doi: 10.1016/j.foodres.2011.04.002.
   Web of Science ®Google Scholar
• Alvarez-Ordóñez, A., V. Broussolle, P. Colin, C. Nguyen-The, and M. Prieto. 2015. The adaptive response of bacterial food-borne pathogens in the environment, host and food: Implications for food safety. International Journal of Food Microbiology 213:99–109. doi: 10.1016/j.ijfoodmicro.2015.06.004.
   PubMed Web of Science ®Google Scholar
• Alzeer, J., and K. A. Hadeed. 2016. Ethanol and its Halal status in food industries. Trends in Food Science & Technology 58:14–20. doi: 10.1016/j.tifs.2016.10.018.
   Web of Science ®Google Scholar
• Andersson, D. I., and D. Hughes. 2014. Microbiological effects of sublethal levels of antibiotics. Nature Reviews Microbiology 12 (7):465–78. doi: 10.1038/nrmicro3270.
   PubMed Web of Science ®Google Scholar
• Bae, Y. M., S. Y. Baek, and S. Y. Lee. 2012. Resistance of pathogenic bacteria on the surface of stainless steel depending on attachment form and efficacy of chemical sanitizers. International Journal of Food Microbiology 153 (3):465–73. doi: 10.1016/j.ijfoodmicro.2011.12.017.
   PubMed Web of Science ®Google Scholar
• Begley, M., and C. Hill. 2015. Stress adaptation in foodborne pathogens. Annual Review of Food Science and Technology 6:191–210. doi: 10.1146/annurev-food-030713-092350.
   PubMed Web of Science ®Google Scholar
• Brissette, J. L., M. Russel, L. Weiner, and P. Model. 1990. Phage shock protein, a stress protein of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 87 (3):862–6. doi: 10.1073/pnas.87.3.862.
   PubMed Web of Science ®Google Scholar
• Browne, N., and B. C. A. Dowds. 2001. Heat and salt stress in the food pathogen Bacillus cereus. Journal of Applied Microbiology 91 (6):1085–94. doi: 10.1046/j.1365-2672.2001.01478.x.
   PubMed Web of Science ®Google Scholar
• Browne, N., and B. C. A. Dowds. 2002. Acid stress in the food pathogen Bacillus cereus. Journal of Applied Microbiology 92 (3):404–14. doi: 10.1046/j.1365-2672.2002.01541.x.
   PubMed Web of Science ®Google Scholar
• Burgess, C. M., A. Gianotti, N. Gruzdev, J. Holah, S. Knøchel, A. Lehner, E. Margas, S. S. Esser, S. S. Sela (Saldinger), and O. Tresse. 2016. The response of foodborne pathogens to osmotic and desiccation stresses in the food chain. International Journal of Food Microbiology 221:37–53. doi: 10.1016/j.ijfoodmicro.2015.12.014.
   PubMed Web of Science ®Google Scholar
• Cao, H., D. Wei, Y. Yang, Y. Shang, G. Li, Y. Zhou, Q. Ma, and Y. Xu. 2017. Systems-level understanding of ethanol-induced stresses and adaptation in E. coli. Scientific Reports 7:1–15.
   Web of Science ®Google Scholar
• Chiang, M. L., W. L. Ho, and C. C. Chou. 2006. Response of Vibrio parahaemolyticus to ethanol shock. Food Microbiology 23 (5):461–7. doi: 10.1016/j.fm.2005.07.001.
   PubMed Web of Science ®Google Scholar
• Chiang, M. L., W. L. Ho, and C. C. Chou. 2008. Ethanol shock changes the fatty acid profile and survival behavior of Vibrio parahaemolyticus in various stress conditions. Food Microbiology 25 (2):359–65. doi: 10.1016/j.fm.2007.10.002.
   PubMed Web of Science ®Google Scholar
• Chiang, M. L., W. L. Ho, R. C. Yu, and C. C. Chou. 2008. Protein expression in Vibrio parahaemolyticus 690 subjected to sublethal heat and ethanol shock treatments. Journal of Food Protection 71 (11):2289–94. doi: 10.4315/0362-028x-71.11.2289.
   PubMed Web of Science ®Google Scholar
• Chiang, M. L., and C. C. Chou. 2008. Expression of superoxide dismutase, catalase and thermostable direct hemolysin by, and growth in the presence of various nitrogen and carbon sources of heat-shocked and ethanol-shocked Vibrio parahaemolyticus. International Journal of Food Microbiology 121 (3):268–74. doi: 10.1016/j.ijfoodmicro.2007.11.001.
   PubMed Web of Science ®Google Scholar
• Chang, C. H., M. L. Chiang, and C. C. Chou. 2009. The effect of temperature and length of heat shock treatment on the thermal tolerance and cell leakage of Cronobacter sakazakii BCRC 13988. International Journal of Food Microbiology 134 (3):184–9. doi: 10.1016/j.ijfoodmicro.2009.06.005.
   PubMed Web of Science ®Google Scholar
• Chiang, M. L., and C. C. Chou. 2009. Survival of Vibrio parahaemolyticus under environmental stresses as influenced by growth phase and pre-adaptation treatment. Food Microbiology 26 (4):391–5. doi: 10.1016/j.fm.2009.01.005.
   PubMed Web of Science ®Google Scholar
• Chiou, R. Y., R. D. Phillips, P. Zhao, M. P. Doyle, and L. R. Beuchat. 2004. Ethanol-mediated variations in cellular fatty acid composition and protein profiles of two genotypically different strains of Escherichia coli O157:H7. Applied and Environmental Microbiology 70 (4):2204–10. doi: 10.1128/aem.70.4.2204-2210.2004.
   PubMed Web of Science ®Google Scholar
• Dao, T., and P. Dantigny. 2011. Control of food spoilage fungi by ethanol. Food Control 22 (3-4):360–8. doi: 10.1016/j.foodcont.2010.09.019.
   Web of Science ®Google Scholar
• De Angelis, M., R. Di Cagno, C. Huet, C. Crecchio, P. F. Fox, and M. Gobbetti. 2004. Heat shock response in Lactobacillus plantarum. Applied and Environmental Microbiology 70 (3):1336–46. doi: 10.1128/aem.70.3.1336-1346.2004.
   PubMed Web of Science ®Google Scholar
• Derman, Y., H. Söderholm, M. Lindström, and H. Korkeala. 2015. Role of csp genes in NaCl, pH, and ethanol stress response and motility in Clostridium botulinum ATCC 3502. Food Microbiology 46:463–70. doi: 10.1016/j.fm.2014.09.004.
   PubMed Web of Science ®Google Scholar
• Doulia, D., G. Katsinis, and B. Mougin. 2000. Prolongation of the microbial shelf life of wrapped part baked baguettes. International Journal of Food Properties 3 (3):447–57. doi: 10.1080/10942910009524648.
   Web of Science ®Google Scholar
• Esbelin, J., T. Santos, and M. Hébraud. 2018. Desiccation: An environmental and food industry stress that bacteria commonly face. Food Microbiology 69:82–8. doi: 10.1016/j.fm.2017.07.017.
   PubMed Web of Science ®Google Scholar
• Ferreira, A., C. P. O'Byrne, and K. J. Boor. 2001. Role of σB in heat, ethanol, acid, and oxidative stress resistance and during carbon starvation in Listeria monocytogenes. Applied and Environmental Microbiology 67 (10):4454–7. doi: 10.1128/AEM.67.10.4454-4457.2001.
   PubMed Web of Science ®Google Scholar
• Finn, S., O. Condell, P. McClure, A. Amézquita, and S. Fanning. 2013. Mechanisms of survival, responses and sources of Salmonella in low-moisture environments. Frontiers in Microbiology 4:331. doi: 10.3389/fmicb.2013.00331.
   PubMed Web of Science ®Google Scholar
• Finn, S., K. Händler, O. Condell, A. Colgan, S. Cooney, P. McClure, A. Amézquita, J. C. D. Hinton, and S. Fanning. 2013. ProP is required for the survival of desiccated Salmonella enterica serovar Typhimurium cells on a stainless steel surface. Applied and Environmental Microbiology 79 (14):4376–84. doi: 10.1128/AEM.00515-13.
   PubMed Web of Science ®Google Scholar
• Flores-Kim, J., and A. J. Darwin. 2016. The phage shock protein response. Annual Review of Microbiology 70:83–101. doi: 10.1146/annurev-micro-102215-095359.
   PubMed Web of Science ®Google Scholar
• Fong, K., and S. Wang. 2016. Heat resistance of Salmonella enterica is increased by pre-adaptation to peanut oil or sub-lethal heat exposure. Food Microbiology 58:139–47. doi: 10.1016/j.fm.2016.04.004.
   PubMed Web of Science ®Google Scholar
• Gorgus, E., M. Hittinger, and D. Schrenk. 2016. Estimates of ethanol exposure in children from food not labeled as alcohol-containing. Journal of Analytical Toxicology 40 (7):537–42. doi: 10.1093/jat/bkw046.
   PubMed Web of Science ®Google Scholar
• Hassani, A. S., F. Malekzadeh, N. Amirmozafari, K. Hamdi, N. Ordouzadeh, and A. Ghaemi. 2009. Phage shock protein G, a novel ethanol-induced stress protein in Salmonella typhimurium. Current Microbiology 58 (3):239–44. doi: 10.1007/s00284-008-9314-6.
   PubMed Web of Science ®Google Scholar
• He, S., X. Zhou, C. Shi, and X. Shi. 2016. Ethanol adaptation induces direct protection and cross-protection against freezing stress in Salmonella enterica serovar Enteritidis. Journal of Applied Microbiology 120 (3):697–704. doi: 10.1111/jam.13042.
   PubMed Web of Science ®Google Scholar
• He, S., Y. Cui, X. Qin, F. Zhang, C. Shi, G. C. Paoli, and X. Shi. 2018. Influence of ethanol adaptation on Salmonella enterica serovar Enteritidis survival in acidic environments and expression of acid tolerance-related genes. Food Microbiology 72:193–8. doi: 10.1016/j.fm.2017.12.005.
   PubMed Web of Science ®Google Scholar
• He, S., X. Qin, C. W. Y. Wong, C. Shi, S. Wang, and X. Shi. 2019. Ethanol adaptation strategies in Salmonella enterica serovar Enteritidis revealed by global proteomic and mutagenic analyses. Applied and Environmental Microbiology 85:e01107–19.
   PubMed Web of Science ®Google Scholar
• Hingston, P., J. Chen, K. Allen, L. T. Hansen, and S. Wang. 2017. Strand specific RNA-sequencing and membrane lipid profiling reveals growth phase-dependent cold stress response mechanisms in Listeria monocytogenes. PloS One 12 (6):e0180123. doi: 10.1371/journal.pone.0180123.
   PubMed Web of Science ®Google Scholar
• Huang, Y. T., K. C. Cheng, R. C. Yu, and C. C. Chou. 2013. Effect of ethanol shock pretreatment on the tolerance of Cronobacter sakazakii BCRC 13988 exposed to subsequent lethal stresses. Foodborne Pathogens and Disease 10 (2):165–70. doi: 10.1089/fpd.2012.1291.
   PubMed Web of Science ®Google Scholar
• Huang, Y., T. C. Ells, and L. T. Hansen. 2015. Role of sigB and osmolytes in desiccation survival of Listeria monocytogenes in simulated food soils on the surface of food grade stainless steel. Food Microbiology 46:443–51. doi: 10.1016/j.fm.2014.09.007.
   PubMed Web of Science ®Google Scholar
• Jiang, X., R. Keto-Timonen, M. Skurnik, and H. Korkeala. 2019. Role of DEAD-box RNA helicase genes in the growth of Yersinia pseudotuberculosis IP32953 under cold, pH, osmotic, ethanol and oxidative stresses. PloS One 14 (7):e0219422. doi: 10.1371/journal.pone.0219422.
   PubMed Web of Science ®Google Scholar
• Jørgensen, F., T. B. Hansen, and S. Knøchel. 1999. Heat shock-induced thermotolerance in Listeria monocytogenes 13-249 is dependent on growth phase, pH and lactic acid. Food Microbiology. 16 (2):185–94. doi: 10.1006/fmic.1998.0222.
   Web of Science ®Google Scholar
• Katsinis, G., F. Rigas, and D. Doulia. 2008. Synergistic effect of chemical preservatives with ethanol on the microbial shelf life of bread by factorial design. International Journal of Food Science & Technology 43 (2):208–15. doi: 10.1111/j.1365-2621.2006.01386.x.
   Web of Science ®Google Scholar
• Korem, M., Y. Gov, and M. Rosenberg. 2010. Global gene expression in Staphylococcus aureus following exposure to alcohol. Microbial Pathogenesis 48 (2):74–84. doi: 10.1016/j.micpath.2009.11.002.
   PubMed Web of Science ®Google Scholar
• Lai, W. B., and H. C. Wong. 2013. Influence of combinations of sublethal stresses on the control of Vibrio parahaemolyticus and its cellular oxidative response. Food Control 33 (1):186–92. doi: 10.1016/j.foodcont.2013.02.036.
   Web of Science ®Google Scholar
• Leistner, L. 2000. Basic aspects of food preservation by hurdle technology. International Journal of Food Microbiology 55 (1-3):181–6. doi: 10.1016/s0168-1605(00)00161-6.
   PubMed Web of Science ®Google Scholar
• Lianou, A., and K. P. Koutsoumanis. 2013a. Strain variability of the behavior of foodborne bacterial pathogens: A review. International Journal of Food Microbiology 167 (3):310–21. doi: 10.1016/j.ijfoodmicro.2013.09.016.
   PubMed Web of Science ®Google Scholar
• Lianou, A., and K. P. Koutsoumanis. 2013. Evaluation of the strain variability of Salmonella enterica acid and heat resistance. Food Microbiology 34 (2):259–67. doi: 10.1016/j.fm.2012.10.009.
   PubMed Web of Science ®Google Scholar
• Lianou, A., G. J. E. Nychas, and K. P. Koutsoumanis. 2017. Variability in the adaptive acid tolerance response phenotype of Salmonella enterica strains. Food Microbiology 62:99–105. doi: 10.1016/j.fm.2016.10.011.
   PubMed Web of Science ®Google Scholar
• Logan, B. K., and S. Distefano. 1998. Ethanol content of various foods and soft drinks and their potential for interference with a breath-alcohol test. Journal of Analytical Toxicology 22 (3):181–3. doi: 10.1093/jat/22.3.181.
   PubMed Web of Science ®Google Scholar
• Lou, Y., and A. E. Yousef. 1996. Resistance of Listeria monocytogenes to heat after adaptation to environmental stresses. Journal of Food Protection 59 (5):465–71. doi: 10.4315/0362-028X-59.5.465.
   PubMed Web of Science ®Google Scholar
• Lou, Y., and A. E. Yousef. 1997. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Applied and Environmental Microbiology 63 (4):1252–5. doi: 10.1128/AEM.63.4.1252-1255.1997.
   PubMed Web of Science ®Google Scholar
• Yeung, P. S. and K. J. Boor. 2004. Effects of acid stress on Vibrio parahaemolyticus survival and cytotoxicity. Journal of Food Protection 67 (7):1328–34. doi: 10.4315/0362-028x-67.7.1328.
   PubMed Web of Science ®Google Scholar
• Markkula, A., M. Lindstrom, P. Johansson, J. Bjorkroth, and H. Korkeala. 2012. Roles of four putative DEAD-box RNA helicase genes in growth of Listeria monocytogenes EGD-e under heat, pH, osmotic, ethanol, and oxidative stress conditions. Applied and Environmental Microbiology 78 (19):6875–82. doi: 10.1128/AEM.01526-12.
   PubMed Web of Science ®Google Scholar
• McDonnell, G., and A. D. Russell. 1999. Antiseptics and disinfectants: Activity, action, and resistance. Clinical Microbiology Reviews 12 (1):147–79. doi: 10.1128/CMR.12.1.147.
   PubMed Web of Science ®Google Scholar
• McMahon, C. M. M., C. M. Byrne, J. J. Sheridan, D. A. McDowell, I. S. Blair, and T. Hegarty. 2000. The effect of culture growth phase on induction of the heat shock response in Yersinia enterocolitica and Listeria monocytogenes. Journal of Applied Microbiology 89 (2):198–206. doi: 10.1046/j.1365-2672.2000.01097.x.
   PubMed Web of Science ®Google Scholar
• Møretrø, T., E. Heir, L. L. Nesse, L. K. Vestby, and S. Langsrud. 2012. Control of Salmonella in food related environments by chemical disinfection. Food Research International 45 (2):532–44. doi: 10.1016/j.foodres.2011.02.002.
   Web of Science ®Google Scholar
• Møretrø, T., and S. Langsrud. 2017. Residential bacteria on surfaces in the food industry and their implications for food safety and quality. Comprehensive Reviews in Food Science and Food Safety 16 (5):1022–41. doi: 10.1111/1541-4337.12283.
   PubMed Web of Science ®Google Scholar
• Osaili, T. M., R. R. Shaker, A. N. Olaimat, A. A. Al-Nabulsi, M. A. Al-Holy, and S. J. Forsythe. 2008. Detergent and sanitizer stresses decrease the thermal resistance of Enterobacter sakazakii in infant milk formula. Journal of Food Science 73 (3):M154–M157.
   Google Scholar
• Park, S., X. You, and J. A. Imlay. 2005. Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx- mutants of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 102 (26):9317–22. doi: 10.1073/pnas.0502051102.
   PubMed Web of Science ®Google Scholar
• Patrignani, F., L. Iucci, N. Belletti, F. Gardini, M. E. Guerzoni, and R. Lanciotti. 2008. Effects of sub-lethal concentrations of hexanal and 2-(E)-hexenal on membrane fatty acid composition and volatile compounds of Listeria monocytogenes, Staphylococcus aureus, Salmonella enteritidis and Escherichia coli. International Journal of Food Microbiology 123 (1-2):1–8. doi: 10.1016/j.ijfoodmicro.2007.09.009.
   PubMed Web of Science ®Google Scholar
• Pontinen, A., M. Lindstrom, M. Skurnik, and H. Korkeala. 2017. 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. doi: 10.1016/j.fm.2017.01.018.
   PubMed Web of Science ®Google Scholar
• Russo, E. T., G. Biggerstaff, M. R. Hoekstra, S. Meyer, N. Patel, B. Miller, and R. Quick. 2013. A recurrent, multistate outbreak of Salmonella serotype Agona infections associated with dry, unsweetened cereal consumption, United States, 2008. Journal of Food Protection 76 (2):227–30., doi: 10.4315/0362-028X.JFP-12-209.
   PubMed Web of Science ®Google Scholar
• Shibasaki, I. 1982. Food preservation with nontraditional antimicrobial agents. Journal of Food Safety 4 (1):35–58. doi: 10.1111/j.1745-4565.1982.tb00432.x.
   Google Scholar
• Singh, S., and R. Shalini. 2016. Effect of hurdle technology in food preservation: A review. Critical Reviews in Food Science and Nutrition 56 (4):641–9. doi: 10.1080/10408398.2012.761594.
   PubMed Web of Science ®Google Scholar
• Slany, M., J. Oppelt, and L. Cincarova. 2017. Formation of Staphylococcus aureus biofilm in the presence of sublethal concentrations of disinfectants studied via a transcriptomic analysis using transcriptome sequencing (RNA-seq). Applied and Environmental Microbiology 83 (24):e0164317. doi: 10.1128/AEM.01643-17.
   Web of Science ®Google Scholar
• Sowbhagya, H. B., and V. N. Chitra. 2010. Enzyme-assisted extraction of flavorings and colorants from plant materials. Critical Reviews in Food Science and Nutrition 50 (2):146–61. doi: 10.1080/10408390802248775.
   PubMed Web of Science ®Google Scholar
• Spector, M. P., and W. J. Kenyon. 2012. Resistance and survival strategies of Salmonella enterica to environmental stresses. Food Research International 45 (2):455–81. doi: 10.1016/j.foodres.2011.06.056.
   Web of Science ®Google Scholar
• Takahashi, H., S. Kuramoto, S. Miya, and B. Kimura. 2011. Desiccation survival of Listeria monocytogenes and other potential foodborne pathogens on stainless steel surfaces is affected by different food soils. Food Control 22 (3-4):633–7. doi: 10.1016/j.foodcont.2010.09.003.
   Web of Science ®Google Scholar
• Talebi, M., L. A. Frink, R. A. Patil, and D. W. Armstrong. 2017. Examination of the varied and changing ethanol content of commercial Kombucha products. Food Analytical Methods 10 (12):4062–7. doi: 10.1007/s12161-017-0980-5.
   Web of Science ®Google Scholar
• Wang, L., M. Qiao, Q. Meng, J. Qiao, and Y. Wu. 2020. Effects of RNase III rncS gene deletion on stress response, biofilm formation and virulence of Listeria monocytogenes. Kafkas Universitesi Veteriner Fakultesi Dergisi 26:269–77.
   Web of Science ®Google Scholar
• Wang, M. L., Y. M. Choong, N. W. Su, and M. H. Lee. 2003. A rapid method for determination of ethanol in alcoholic beverages using capillary gas chromatography. Journal of Food and Drug Analysis 11:133–40.
   Web of Science ®Google Scholar
• Wang, S., D. Weller, J. Falardeau, L. K. Strawn, F. O. Mardones, A. D. Adell, and A. I. M. Switt. 2016. Food safety trends: From globalization of whole genome sequencing to application of new tools to prevent foodborne diseases. Trends in Food Science & Technology 57:188–98. doi: 10.1016/j.tifs.2016.09.016.
   Web of Science ®Google Scholar
• Winfield, M. D., and E. A. Groisman. 2003. Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Applied and Environmental Microbiology 69 (7):3687–94. doi: 10.1128/aem.69.7.3687-3694.2003.
   PubMed Web of Science ®Google Scholar
• Wu, W. W., G. Wang, S. J. Baek, and R. F. Shen. 2006. Comparative study of three proteomic quantitative methods, DIGE, cICAT, and iTRAQ, using 2D gel- or LC-MALDI TOF/TOF . Journal of Proteome Research 5 (3):651–8. doi: 10.1021/pr050405o.
   PubMed Web of Science ®Google Scholar
• Yang, Y., M. I. Kadim, W. J. Khoo, Q. Zheng, M. I. Setyawati, Y. J. Shin, S. C. Lee, and H. G. Yuk. 2014. Membrane lipid composition and stress/virulence related gene expression of Salmonella Enteritidis cells adapted to lactic acid and trisodium phosphate and their resistance to lethal heat and acid stress. International Journal of Food Microbiology 191:24–31. doi: 10.1016/j.ijfoodmicro.2014.08.034.
   PubMed Web of Science ®Google Scholar
• Yoon, Y., H. Lee, S. Lee, S. Kim, and K. H. Choi. 2015. Membrane fluidity-related adaptive response mechanisms of foodborne bacterial pathogens under environmental stresses. Food Research International 72:25–36. doi: 10.1016/j.foodres.2015.03.016.
   Web of Science ®Google Scholar