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Susceptibility of Listeria monocytogenes and Staphylococcus aureus Grown Under High Salt Conditions to X-ray Irradiation

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Abstract

Among ionizing radiations, X-ray irradiation has been proposed as an alternative approach to inactivate various pathogens. However, erroneous conclusions and misinterpretations of results may adversely affect its application if the factors affecting X-ray resistance of foodborne pathogens are not considered during X-ray irradiation studies. This study investigated the effect of prior exposure to high salt conditions on the susceptibility of two gram-positive pathogenic bacteria, Listeria monocytogenes and Staphylococcus aureus, to X-ray irradiation. Accordingly, a bacterial cocktail containing three strains of each pathogen was exposed to osmotic stress by suspension in a saturated 15% w/v NaCl solution (water activity = 0.88) for 0 (control), 4, 12, and 24 h. Subsequent X-ray irradiation at 0.8 kGy resulted in reduced counts of both L. monocytogenes (1.55, 2.32, 3.06, and 3.38 log CFU/mL, respectively) and S. aureus (2.44, 2.98, 3.58, and 4.07 log CFU/mL, respectively) held in NaCl solution for 0, 4, 12, and 24 h. The results of this study revealed that exposure to high salt conditions decreased the resistance of L. monocytogenes and S. aureus to X-ray irradiation. Mechanistic studies further identified the damage associated with reactive oxygen species and interrupted peptidoglycan synthesis as major factors contributing to the changes in sensitivity to X-ray irradiation under high salt conditions. Thus, X-ray irradiation may be beneficial for reducing the viability of gram-positive pathogens that are highly resistant to NaCl without heterogeneous stress adaptation.

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Acosta, O., Usaga, J., Churey, J. J., Worobo, R. W., & Padilla-Zakour, O. I. (2017). Effect of water activity on the thermal tolerance and survival of Salmonella enterica serovars Tennessee and Senftenberg in goat’s milk caramel. Journal of Food Protection, 80, 922–927.

    Article  CAS  PubMed  Google Scholar 

  • Algammal, A. M., Hetta, H. F., Elkelish, A., Alkhalifah, D. H. H., Hozzein, W. N., Batiha, G. E., Nahhas, N. E., & Mabrok, M. A. (2020). Methicillin-resistant Staphylococcus aureus (MRSA): One health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistance, and zoonotic impact. Infection and Drug Resistance, 13, 3255–3265.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alreshidi, M. M., Dunstan, R. H., Onyango, L. A., & Roberts, T. K. (2013). Staphylococcal phenomics: Metabolomic and proteomic responses to environmental stressors. Microbial pathogens and strategies for combating them: science, technology and education, A. Mendez-Vilas, Ed, 690–701.

  • Beales, N. (2004). Adaptation of microorganisms to cold temperatures, weak acid preservatives, low pH, and osmotic stress: A review. Comprehensive Reviews in Food Science and Food Safety, 3, 1–20.

    Article  CAS  PubMed  Google Scholar 

  • Borisova, M., Gaupp, R., Duckworth, A., Schneider, A., Dalügge, D., Mühleck, M., Deubel, D., Unsleber, S., Yu, W., Muth, G., Bischoff, M., Götz, F., & Mayer, C. (2016). Peptidoglycan recycling in Gram-positive bacteria is crucial for survival in stationary phase. mBio, 7(5), e00923–16.

  • Chang, Y., Bai, J., Yu, H., Chang, P. S., & Nitin, N. (2021). Synergistic inactivation of bacteria using a combination of erythorbyl laurate and UV type-A light treatment. Frontiers in Microbiology, 12, 682900.

    Article  PubMed Central  Google Scholar 

  • CDC. (2020). National Outbreak Reporting System (NORS). Retrieved May 22, 2020, from https://wwwn.cdc.gov/norsdashboard/

  • Cebrián, G., Sagarzazu, N., Pagán, R., Condón, S., & Mañas, P. (2010). Development of stress resistance in Staphylococcus aureus after exposure to sublethal environmental conditions. International Journal of Food Microbiology, 140(1), 26–33.

    Article  PubMed  Google Scholar 

  • Cho, G. L., & Ha, J. W. (2019). Application of X-ray for inactivation of foodborne pathogens in ready-to-eat sliced ham and mechanism of the bactericidal action. Food Control, 96, 343–350.

    Article  CAS  Google Scholar 

  • Clements, M. O., & Foster, S. J. (1999). Stress resistance in Staphylococcus aureus. Trends in Microbiology, 7(11), 458–462.

    Article  CAS  PubMed  Google Scholar 

  • Clements, M. O., Watson, S. P., & Foster, S. J. (1999). Characterization of the major superoxide dismutase of Staphylococcus aureus and its role in starvation survival, stress resistance, and pathogenicity. Journal of Bacteriology, 181, 3898–3903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • den Besten, H. M., Mols, M., Moezelaar, R., Zwietering, M. H., & Abee, T. (2009). Phenotypic and transcriptomic analyses of mildly and severely salt-stressed Bacillus cereus ATCC 14579 cells. Applied and Environmental Microbiology, 75, 4111–4119.

    Article  Google Scholar 

  • Deng, L. Z., Tao, Y., Mujumdar, A. S., Pan, Z., Chen, C., Yang, X. H., Liu, Z. L., Wang, H., & Xiao, H. W. (2020). Recent advances in non-thermal decontamination technologies for microorganisms and mycotoxins in low-moisture foods. Trends in Food Science & Technology, 106, 104–112.

    Article  CAS  Google Scholar 

  • Desai, A. N., Anyoha, A., Madoff, L. C., & Lassmann, B. (2019). Changing epidemiology of Listeria monocytogenes outbreaks, sporadic cases, and recalls globally: A review of ProMED reports from 1996 to 2018. International Journal of Infectious Diseases, 84, 48–53.

    Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • EFSA (European Food Safety Authority and European Centre for Disease Prevention and Control). (2018). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA Journal, 16(12), 5500.

    Google Scholar 

  • Estilo, E. E. C., & Gabriel, A. A. (2017). Previous stress exposures influence subsequent UV-C resistance of Salmonella enterica in coconut liquid endosperm. LWT, 86, 139–147.

    Article  CAS  Google Scholar 

  • Gabriel, A. A. (2015). Previous physicochemical stress exposures influence subsequent resistance of Escherichia coli O157:H7, Salmonella enterica, and Listeria monocytogenes to ultraviolet-C in coconut liquid endosperm beverage. International Journal of Food Microbiology, 201, 7–16.

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ha, T. M. H., Yong, D., Lee, E. M. Y., Kumar, P., Lee, Y. K., & Zhou, W. (2017). Activation and inactivation of Bacillus pumilus spores by kiloelectron volt X-ray irradiation. PLoS ONE, 12(5), e0177571.

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang, M., Zhuang, H., Zhao, J., Wang, J., Yan, W., & Zhang, J. (2020). Differences in cellular damage induced by dielectric barrier discharge plasma between Salmonella Typhimurium and Staphylococcus aureus. Bioelectrochemistry, 132, 107445.

    Article  CAS  PubMed  Google Scholar 

  • Hussain Chan, M. W., Mirani, Z. A., Khan, M. N., Ali, A., Khan, A. B., Asadullah, R., & N. (2021). Isolation and characterization of small colony variants of Staphylococcus aureus in various food samples. Biocatalysis and Agricultural Biotechnology, 35, 102097.

    Article  CAS  Google Scholar 

  • Hussain, R. M., Razak, Z. N. R. A., Saad, W. M. M. S., & Mustakim, M. (2017). Mechanism of antagonistic effects of Andrographis paniculata methanolic extract against Staphylococcus aureus. Asian Pacific Journal of Tropical Medicine, 10(7), 685–695.

    Article  PubMed  Google Scholar 

  • Jee, D. Y., & Ha, J. W. (2021). Synergistic interaction of tap water-based neutral electrolyzed water combined with UVA irradiation to enhance microbial inactivation on stainless steel. Food Research International, 150, 110773.

    Article  CAS  PubMed  Google Scholar 

  • Jenul, C., & Horswill, A. R. (2018). Regulation of Staphylococcus aureus Virulence. Microbiology Spectrum, 6, GPP3-0031-2018.

  • Jeon, M. J., & Ha, J. W. (2020a). Bactericidal and synergistic effects of X-ray irradiation and gallic acid against foodborne pathogens on lettuce. Food Microbiology, 92, 103584.

    Article  CAS  PubMed  Google Scholar 

  • Jeon, M. J., & Ha, J. W. (2020b). Synergistic bactericidal effect and mechanism of X-ray irradiation and citric acid combination against food-borne pathogens on spinach leaves. Food Microbiology, 91, 103543.

    Article  CAS  PubMed  Google Scholar 

  • Jeong, Y. J., & Ha, J. W. (2022). Synergistic antimicrobial effect of UV-A irradiation and malic acid combination treatment against foodborne pathogens on spinach and the underlying mechanism. Food and Bioprocess Technology, 15, 379–390.

    Article  CAS  Google Scholar 

  • Kabir, M. N., Aras, S., George, J., Wadood, S., Chowdhury, S., & Fouladkhah, A. C. (2021). High-pressure and thermal-assisted pasteurization of habituated, wild-type, and pressure-stressed Listeria monocytogenes, Listeria innocua, and Staphylococcus aureus. LWT, 137, 110445.

    Article  CAS  Google Scholar 

  • Kang, I. B., Kim, D. H., Jeong, D. N., Park, J. H., & Seo, K. H. (2018). Heat resistance of Salmonella Enteritidis under prolonged exposure to acid-salt combined stress and subsequent refrigeration. International Journal of Food Microbiology, 285, 165–172.

    Article  CAS  PubMed  Google Scholar 

  • Kim, M. K., Mikš-Krajnik, M., Kumar, A., Ghate, V., & Yuk, H. H. (2015). Antibacterial effect and mechanism of high-intensity 405 ± 5 nm light emitting diode on Bacillus cereus, Listeria monocytogenes, and Staphylococcus aureus under refrigerated condition. Journal of Photochemistry and Photobiology B: Biology, 153, 33–39.

    Article  CAS  PubMed  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 

  • Lim, J. S., & Ha, J. W. (2021a). Effect of acid adaptation on the resistance of Escherichia coli O157:H7 and Salmonella enterica serovar Typhimurium to X-ray irradiation in apple juice. Food Control, 120, 107489.

    Article  CAS  Google Scholar 

  • Lim, J. S., & Ha, J. W. (2021b). Growth-inhibitory effect of X-ray irradiation on gram-negative and gram-positive pathogens in apple, orange, and tomato juices. Food and Bioprocess Technology, 14, 1909–1919.

    Article  CAS  Google Scholar 

  • Livak, K. J., & Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25(4), 402–408.

    Article  CAS  PubMed  Google Scholar 

  • McCarthy, A. J., Breathnach, A. S., & Lindsay, J. A. (2012). Detection of mobile-genetic-element variation between colonizing and infecting hospital-associated methicillin-resistant Staphylococcus aureus isolates. Journal of Clinical Microbiology, 50(3), 1073–1075.

    Article  PubMed  PubMed Central  Google Scholar 

  • MedVeďoVá, A., VAlík, Ľ., & Studeničová, A. (2010). The effect of temperature and water activity on the growth of Staphylococcus aureus. Czech Journal of Food Sciences, 27(2), S2-28–S2-35.

  • Monaco, M., Pimentel de Araujo, F., Cruciani, M., Coccia, E. M., & Pantosti, A. (2016). Worldwide epidemiology and antibiotic resistance of Staphylococcus aureus. Current Topics in Microbiology and Immunology, 409, 21–56.

    Google Scholar 

  • Montanari, C., Serrazanetti, D. I., Felis, G., Torriani, S., Tabanelli, G., Lanciotti, R., & Gardin, F. (2015). New insights in thermal resistance of staphylococcal strains belonging to the species Staphylococcus epidermidis, Staphylococcus lugdunensis and Staphylococcus aureus. Food Control, 50, 605–612.

    Article  CAS  Google Scholar 

  • Niemira, B. A. (2010). Irradiation sensitivity of planktonic and biofilm-associated Listeria monocytogenes and L. innocua as influenced by temperature of biofilm formation. Food and Bioprocess Technology, 3, 257–264.

    Article  Google Scholar 

  • Olaimat, A. N., Ghoush, M. A., Al-Holy, M., Hilal, H. A., Al-Nabulsi, A. A., Osaili, T. M., Ayyash, M., & Holley, R. (2021). Survival and growth of Listeria monocytogenes and Staphylococcus aureus in ready-to-eat Mediterranean vegetable salads: Impact of storage temperature and food matrix. International Journal of Food Microbiology, 109149.

  • Oliveira, A. R., Domingues, F. C., & Ferreira, S. (2017). The influence of resveratrol adaptation on resistance to antibiotics, benzalkonium chloride, heat and acid stresses of Staphylococcus aureus and Listeria monocytogenes. Food Control, 73, 1420–1425.

    Article  CAS  Google Scholar 

  • Ozogul, F., & Ozden, O. (2013). The effects of gamma irradiation on the biogenic amine formation in sea bream (Sparus aurata) stored in ice. Food and Bioprocess Technology, 6, 1343–1349.

    Article  CAS  Google Scholar 

  • Park, J. S., & Ha, J. W. (2019). X-ray irradiation inactivation of Escherichia coli O157:H7, Salmonella enterica Serovar Typhimurium, and Listeria monocytogenes on sliced cheese and its bactericidal mechanisms. International Journal of Food Microbiology, 289, 127–133.

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Baltar, A., Serrano, A., Bravo, D., Montiel, R., & Medina, M. (2019). Combined effect of high pressure processing with enterocins or thymol on the inactivation of Listeria monocytogenes and the characteristics of sliced dry-cured ham. Food and Bioprocess Technology, 12, 288–297.

    Article  Google Scholar 

  • Pitinidhipat, N., & Yasurin, P. (2012). Antibacterial activity of Chrysanthemum indicum, Centella asiatica and Andrographis paniculata against Bacillus cereus and Listeria monocytogenes under osmotic stress. AU Journal of Technology, 15(4), 239–245.

    Google Scholar 

  • Qiao, J., Zhu, M., Lu, Z., Lv, F., Zhao, H., & Bie, X. (2020). The antibiotics resistance mechanism and pathogenicity of cold stressed Staphylococcus aureus. LWT, 126, 109274.

    Article  CAS  Google Scholar 

  • Schuster, C. F., Wiedemann, D. M., Kirsebom, F. C., Santiago, M., Walker, S., & Gründling, A. (2020). High-throughput transposon sequencing highlights the cell wall as an important barrier for osmotic stress in methicillin resistant Staphylococcus aureus and underlines a tailored response to different osmotic stressors. Molecular Microbiology, 113, 699–717.

    Article  CAS  PubMed  Google Scholar 

  • Seok, J. H., & Ha, J. W. (2021). Synergistic mechanism and enhanced inactivation exhibited by UVA irradiation combined with citric acid against pathogenic bacteria on sliced cheese. Food Control, 124, 107861.

    Article  CAS  Google Scholar 

  • Stewart, C. M., & Cole., M.B., Legan, J.D., Slade, L., & Schaffner, D.W. (2005). Solute-specific effects of osmotic stress on Staphylococcus aureus. Journal of Applied Microbiology, 98, 193–202.

    Article  CAS  PubMed  Google Scholar 

  • Sutherland, J. P., Bayliss, A. J., & Roberts, T. A. (1994). Predictive modelling of growth of Staphylococcus aureus: The effects of temperature, pH and sodium chloride. International Journal of Food Microbiology, 21, 217–236.

    Article  CAS  PubMed  Google Scholar 

  • Tong, S. Y., Davis, J. S., Eichenberger, E., Holland, T. L., & Fowler, V. G., Jr. (2015). Staphylococcus aureus infections: Epidemiology, pathophysiology, clinical manifestations, and management. Clinical Microbiology Reviews, 28, 603–661.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Udomkun, P., Wiredu, A. N., Nagle, M., Müller, J., Vanlauwe, B., & Bandyopadhyay, R. (2017). Innovative technologies to manage aflatoxins in foods and feeds and the profitability of application–A review. Food Control, 76, 127–138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • USFDA. (2004). Bad bug book: Foodborne pathogenic microorganisms and natural toxins handbook. International Medical Pub.

  • Vijaranakul, U., Nadakavukaren, M. J., de Jonge, B. L., Wilkinson, B. J., & Jayaswal, R. K. (1995). Increased cell size and shortened peptidoglycan interpeptide bridge of NaCl-stressed Staphylococcus aureus and their reversal by glycine betaine. Journal of Bacteriology, 177(17), 5116–5121.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yi, L., Luo, L., Chen, J., Sun, H., Wang, X., Yi, Y., & Lv, X. (2020). Cell wall and DNA damage of Staphylococcus aureus by bacteriocin BM1157. LWT, 134, 109842.

    Article  CAS  Google Scholar 

  • Yoon, H., Park, B. Y., Oh, M. H., Choi, K. H., & Yoon, Y. (2013). Effect of NaCl on heat resistance, antibiotic susceptibility, and Caco-2 cell invasion of Salmonella. Biomed Research International, 2013.

  • Zhang, H., Ha, T. M. H., Sech, H. L., & Zhou, W. (2020). Inactivation of Escherichia coli O157:H7 and Salmonella Typhimurium in edible bird’s nest by low-energy X-ray irradiation. Food Control, 110, 107031.

    Article  CAS  Google Scholar 

  • Zhang, L., Kou, X., Zhang, S., Cheng, T., & Wanga, S. (2018). Effect of water activity and heating rate on Staphylococcus aureus heat resistance in walnut shells. International Journal of Food Microbiology, 266, 282–288.

    Article  PubMed  Google Scholar 

  • Zhang, L., Ma, H., & Wang, S. (2021). Pasteurization mechanism of S. aureus ATCC 25923 in walnut shells using radio frequency energy at lab level. LWT, 143, 111129.

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  1. Department of Food Science and Biotechnology, Global K-Food Research Center, Hankyong National University, Anseong-si 17579, South Korea

    Jong-Heon Seok & Jae-Won Ha

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Jong-Heon Seok: methodology; investigation; data curation; writing—original draft. Jae-Won Ha: conceptualization; investigation; methodology; supervision; project administration; writing—review and editing; funding acquisition.

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Seok, JH., Ha, JW. Susceptibility of Listeria monocytogenes and Staphylococcus aureus Grown Under High Salt Conditions to X-ray Irradiation. Food Bioprocess Technol 16, 2800–2812 (2023). https://doi.org/10.1007/s11947-023-03103-3

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