Abstract
The present study aimed to elucidate the antifungal effect and underlying mechanism of plasma-activated water (PAW) combined with sodium laureth sulfate (SLES) against Saccharomyces cerevisiae. S. cerevisiae, initially at 6.95 log10 colony-forming unit (CFU)/mL, decreased to an undetectable level following the synergistic treatment of PAW and SLES (0.50 mg/mL) for 20 min. After PAW treatment combined with SLES (2.5 mg/mL) for 30 min, the S. cerevisiae cells on polyethylene films also reduced to an undetectable level from the initial load of 5.84 log10 CFU/cm2. PAW + SLES treatment caused severe disruption of membrane integrity and increased lipid oxidation within the cell membrane and the intracellular reactive oxygen species levels in S. cerevisiae cells. Besides, the disruption of the mitochondrial membrane potential (∆ψm) was also observed in S. cerevisiae cells after treatment of PAW and SLES at 0.01 mg/mL for 5 min. These data suggest that the combined treatment of PAW and SLES causes oxidation injury to cell membranes and abnormal ∆ψm in S. cerevisiae, which may be eventually responsible for cell death. This study demonstrates the potential application of PAW combined with SLES as an alternative disinfection method.
Key Points • PAW + SLES exhibited synergistic antifungal activity against S. cerevisiae. • PAW + SLES resulted in severe disruption of membrane integrity and permeability. • PAW + SLES induced accumulation of reactive oxygen species in S. cerevisiae cells. |
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References
Atale N, Gupta S, Yadav UCS, Rani V (2014) Cell-death assessment by fluorescent and nonfluorescent cytosolic and nuclear staining techniques. J Microsc 255:7–19. https://doi.org/10.1111/jmi.12133
Bai Y, Muhammad AI, Hu YQ, Koseki S, Liao XY, Chen SG, Ye XQ, Liu DH, Ding T (2020) Inactivation kinetics of Bacillus cereus spores by plasma activated water (PAW). Food Res Int 131:109041. https://doi.org/10.1016/j.foodres.2020.109041
Bintsis T (2017) Foodborne pathogens. AIMS Microbiol 3:529–563. https://doi.org/10.3934/microbiol.2017.3.529
Chen D, Zhao T, Doyle MP (2015) Single- and mixed-species biofilm formation by Escherichia coli O157:H7 and Salmonella, and their sensitivity to levulinic acid plus sodium dodecyl sulfate. Food Control 57:48–53. https://doi.org/10.1016/j.foodcont.2015.04.006
Choi EJ, Park HW, Kim SB, Ryu S, Lim J, Hong EJ, Byeon YS, Chun HH (2019) Sequential application of plasma-activated water and mild heating improves microbiological quality of ready-to-use shredded salted kimchi cabbage (Brassica pekinensis L.). Food Control 98:501–509. https://doi.org/10.1016/j.foodcont.2018.12.007
Frias E, Iglesias Y, Alvarez-Ordonez A, Prieto M, Gonzalez-Raurich M, Lopez M (2020) Evaluation of cold atmospheric pressure plasma (CAPP) and plasma-activated water (PAW) as alternative non-thermal decontamination technologies for tofu: Impact on microbiological, sensorial and functional quality attributes. Food Res Int 129:108859. https://doi.org/10.1016/j.foodres.2019.108859
Guo L, Xu RB, Gou L, Liu ZC, Zhao YM, Liu DX, Zhang L, Chen HL, Kong MG (2018) Mechanism of virus inactivation by cold atmospheric-pressure plasma and plasma-activated water. Appl Environ Microbiol 84:e00726–e00718. https://doi.org/10.1128/AEM.00726-18
Han JY, Song WJ, Kang JH, Min SC, Eom S, Hong EJ, Ryu S, Kim SB, Cho S, Kang DH (2020) Effect of cold atmospheric pressure plasma-activated water on the microbial safety of Korean rice cake. LWT-Food Sci Technol 120:108918. https://doi.org/10.1016/j.lwt.2019.108918
Heredia N, García S (2018) Animals as sources of food-borne pathogens: A review. Anim Nutr 4:250–255. https://doi.org/10.1016/j.aninu.2018.04.006
Hernández-Hernández HM, Moreno-Vilet L, Villanueva-Rodríguez SJ (2019) Current status of emerging food processing technologies in Latin America: Novel non-thermal processing. Innov Food Sci Emerg Technol 58:102233. https://doi.org/10.1016/j.ifset.2019.102233
Huis in’t Veld JHJ (1996) Microbial and biochemical spoilage of foods: An overview. Int J Food Microbiol 33:1–18. https://doi.org/10.1016/0168-1605(96)01139-7
Kalyanaraman B, Darley-Usmar V, Davies KJA, Dennery PA, Forman HJ, Grisham MB, Mann GE, Moore K, Roberts LJ, Ischiropoulos H (2012) Measuring reactive oxygen and nitrogen species with fluorescent probes: Challenges and limitations. Free Radic Biol Med 52:1–6. https://doi.org/10.1016/j.freeradbiomed.2011.09.030
Kamgang-Youbi G, Herry JM, Meylheuc T, Brisset JL, Bellon-Fontaine MN, Doubla A, Naitali M (2009) Microbial inactivation using plasma-activated water obtained by gliding electric discharges. Lett Appl Microbiol 48:13–18. https://doi.org/10.1111/j.1472-765X.2008.02476.x
Kang J, Song KB (2015) Inactivation of pre-existing bacteria and foodborne pathogens on perilla leaves using a combined treatment with an organic acid and a surfactant. Hortic Environ Biotechnol 56:195–199. https://doi.org/10.1007/s13580-015-0093-2
Kim SS, Park SH, Kim SH, Kang DH (2019) Synergistic effect of ohmic heating and UV-C irradiation for inactivation of Escherichia coli O157:H7, Salmonella Typhimurium and Listeria monocytogenes in buffered peptone water and tomato juice. Food Control 102:69–75. https://doi.org/10.1016/j.foodcont.2019.03.011
Kramer B, Hasse D, Guist S, Schmitt-John T, Muranyi P (2020) Inactivation of bacterial endospores on surfaces by plasma processed air. J Appl Microbiol 128:920–933. https://doi.org/10.1111/jam.14528
Lacombe A, Niemira BA, Gurtler JB, Kingsley DH, Li XH, Chen HQ (2018) Surfactant-enhanced organic acid inactivation of Tulane virus, a human norovirus surrogate. J Food Prot 81:279–283. https://doi.org/10.4315/0362-028X.JFP-17-330
Li J, Cheng H, Liao XY, Liu DH, Xiang QS, Wang J, Chen SG, Ye XQ, Ding T (2019) Inactivation of Bacillus subtilis and quality assurance in Chinese bayberry (Myrica rubra) juice with ultrasound and mild heat. LWT-Food Sci Technol 108:113–119. https://doi.org/10.1016/j.lwt.2019.03.061
Liao XY, Cullen PJ, Muhammad AI, Jiang ZM, Ye XQ, Liu DH, Ding T (2020) Cold plasma-based hurdle interventions: New strategies for improving food safety. Food Eng Rev 12:321–332. https://doi.org/10.1007/s12393-020-09222-3
Liao XY, Muhammad AI, Chen SG, Hu YQ, Ye XQ, Liu DH, Ding T (2019) Bacterial spore inactivation induced by cold plasma. Crit Rev Food Sci Nutr 59:2562–2572. https://doi.org/10.1080/10408398.2018.1460797
Lin CM, Chu YC, Hsiao CP, Wu JS, Hsieh CW, Hou CY (2019) The optimization of plasma-activated water treatments to inactivate Salmonella Enteritidis (ATCC 13076) on shell eggs. Foods 8:520. https://doi.org/10.3390/foods8100520
Los A, Ziuzina D, Boehm D, Cullen PJ, Bourke P (2020) Inactivation efficacies and mechanisms of gas plasma and plasma-activated water against Aspergillus flavus spores and biofilms: A comparative study. Appl Environ Microbiol 86:e02619–e02619. https://doi.org/10.1128/AEM.02619-19
Nichols WW (2012) Permeability of bacteria to antibacterial agents. In: Dougherty T, Pucci M (eds) Antibiotic discovery and development. Springer, Boston, pp 849–879. https://doi.org/10.1007/978-1-4614-1400-1_26
Okimotoa Y, Watanabea A, Nikia E, Yamashitab T, Noguchia N (2000) A novel fluorescent probe diphenyl-1-pyrenylphosphine to follow lipid peroxidation in cell membranes. FEBS Lett 474:137–140. https://doi.org/10.1016/s0014-5793(00)01587-8
Royintarat T, Choi EH, Boonyawan D, Seesuriyachan P, Wattanutchariya W (2020) Chemical-free and synergistic interaction of ultrasound combined with plasma-activated water (PAW) to enhance microbial inactivation in chicken meat and skin. Sci Rep 10:1559. https://doi.org/10.1038/s41598-020-58199-w
Rozali SNM, Milani EA, Deed RC, Silva FVM (2017) Bacteria, mould and yeast spore inactivation studies by scanning electron microscope observations. Int J Food Microbiol 263:17–25. https://doi.org/10.1016/j.ijfoodmicro.2017.10.008
Sivandzade F, Bhalerao A, Cucullo L (2019) Analysis of the mitochondrial membrane potential using the cationic JC-1 dye as a sensitive fluorescent probe. Bio Protoc 9:e3128. https://doi.org/10.21769/BioProtoc.3128
Takahashi M, Shibata M, Niki E (2001) Estimation of lipid peroxidation of live cells using a fluorescent probe, diphenyl-1-pyrenylphosphine. Free Radic Biol Med 31:164–174. https://doi.org/10.1016/S0891-5849(01)00575-5
Thirumdas R, Kothakota A, Annapure U, Siliveru K, Blundell R, Gatt R, Valdramidis VP (2018) Plasma activated water (PAW): Chemistry, physico-chemical properties, applications in food and agriculture. Trends Food Sci Technol 77:21–31. https://doi.org/10.1016/j.tifs.2018.05.007
Wang TY, Libardo MDJ, Angeles-Boza AM, Pellois JP (2017) Membrane oxidation in cell delivery and cell killing applications. ACS Chem Biol 12:1170–1182. https://doi.org/10.1021/acschembio.7b00237
Wu D, Forghani F, Daliri EBM, Li J, Liao XY, Liu DH, Ye XQ, Chen SG, Ding T (2020) Microbial response to some nonthermal physical technologies. Trends Food Sci Technol 95:107–117. https://doi.org/10.1016/j.tifs.2019.11.012
Wu MC, Liu CT, Chiang CY, Lin YJ, Lin YH, Chang YW, Wu JS (2019) Inactivation effect of Colletotrichum gloeosporioides by long-lived chemical species using atmospheric-pressure corona plasma-activated water. IEEE Trans Plasma Sci 47:1100–1104. https://doi.org/10.1109/TPS.2018.2871856
Xiang QS, Kang CD, Niu LY, Zhao DB, Li K, Bai YH (2018a) Antibacterial activity and a membrane damage mechanism of plasma-activated water against Pseudomonas deceptionensis CM2. LWT Food Sci Technol 96:395–401. https://doi.org/10.1016/j.lwt.2018.05.059
Xiang QS, Liu XF, Li JG, Liu SN, Zhang H, Bai YH (2018b) Effects of dielectric barrier discharge plasma on the inactivation of Zygosaccharomyces rouxii and quality of apple juice. Food Chem 254:201–207. https://doi.org/10.1016/j.foodchem.2018.02.008
Xiang QS, Liu XF, Liu SN, Ma YF, Xu CQ, Bai YH (2019) Effect of plasma-activated water on microbial quality and physicochemical characteristics of mung bean sprouts. Innov Food Sci Emerg Technol 52:49–56. https://doi.org/10.1016/j.ifset.2018.11.012
Xiang QS, Zhang R, Fan LM, Ma YF, Wu D, Li K, Bai YH (2020) Microbial inactivation and quality of grapes treated by plasma-activated water combined with mild heat. LWT-Food Sci Technol 126:109336. https://doi.org/10.1016/j.lwt.2020.109336
Yost AD, Joshi SG (2015) Atmospheric nonthermal plasma-treated PBS inactivates Escherichia coli by oxidative DNA damage. PLoS One 10:e0139903. https://doi.org/10.1371/journal.pone.0139903
Zaki HMBA, Mohamed HMH, El-Sherif AMA (2015) Improving the antimicrobial efficacy of organic acids against Salmonella enterica attached to chicken skin using SDS with acceptable sensory quality. LWT-Food Sci Technol 64:558–564. https://doi.org/10.1016/j.lwt.2015.06.012
Zhang R, Ma YF, Wu D, Fan LM, Bai YH, Xiang QS (2020) Synergistic inactivation mechanism of combined plasma-activated water and mild heat against Saccharomyces cerevisiae. J Food Prot 83:1307–1314. https://doi.org/10.4315/JFP-20-065
Zhang XJ, Ashby R, Solaiman DKY, Uknalis J, Fan XT (2016) Inactivation of Salmonella spp. and Listeria spp. by palmitic, stearic, and oleic acid sophorolipids and thiamine dilauryl sulfate. Front Microbiol 7:2076. https://doi.org/10.3389/fmicb.2016.02076
Zhao T, Zhao P, Doyle MP (2009) Inactivation of Salmonella and Escherichia coli O157:H7 on lettuce and poultry skin by combinations of levulinic acid and sodium dodecyl sulfate. J Food Prot 72:928–936. https://doi.org/10.4315/0362-028x-72.5.928
Zhou ML, Doyle MP, Chen D (2020) Combination of levulinic acid and sodium dodecyl sulfate on inactivation of foodborne microorganisms: A review. Crit Rev Food Sci Nutr 60:2526–2531. https://doi.org/10.1080/10408398.2019.1650249
Zhou RW, Zhou RS, Prasad K, Fang Z, Speight R, Bazaka K, Ostrikov K (2018) Cold atmospheric plasma activated water as a prospective disinfectant: The crucial role of peroxynitrite. Green Chem 20:5276–5284. https://doi.org/10.1039/c8gc02800a
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The work was financially supported by the National Key R&D Program of China (No. 2018YFD0400603), the China Postdoctoral Science Foundation (No. 2018M632765), and the Natural Science Foundation of Henan Province (No. 212300410090).
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XL and YFL designed the project, conceptualized the study, and drafted the manuscript. RZ and LLHF carried out the experiments and analyzed data. GHD conceived and coordinated the study. QSX conceived the study and edited the manuscript. All authors have read and approved the published version of the manuscript.
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Liu, X., Li, Y., Zhang, R. et al. Inactivation effects and mechanisms of plasma-activated water combined with sodium laureth sulfate (SLES) against Saccharomyces cerevisiae. Appl Microbiol Biotechnol 105, 2855–2865 (2021). https://doi.org/10.1007/s00253-021-11227-9
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DOI: https://doi.org/10.1007/s00253-021-11227-9