Abstract
Saccharomyces cerevisiae is one of the common spoilage microorganisms in fruit juices. This paper investigated the influences of carvacrol on S. cerevisiae inactivation by mild pressure carbon dioxide (MPCO2). The results demonstrated that carvacrol synergistically enhanced the antifungal activity against S. cerevisiae of MPCO2. With the increase of carvacrol concentration (20–160 µg/mL), CO2 pressure (1.5–3.5 MPa), process temperature (20–40 °C), and treatment time (15–60 min), the inactivation effect of carvacrol combined with MPCO2 on S. cerevisiae was gradually increased and significantly stronger than either single treatment. In the presence of carvacrol, MPCO2 severely disordered the plasma membrane of S. cerevisiae, including the increase of membrane permeability, and the loss of membrane potential and integrity. MPCO2 and carvacrol in combination also aggravated the mitochondrial depolarization of S. cerevisiae and reduced intracellular ATP and protein content. This study suggests the potential of carvacrol and pressurized CO2 as an alternative technology for food pasteurization.
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References
Addo KA, Li H, Yu Y, Xiao X (2023) Unraveling the mechanism of the synergistic antimicrobial effect of cineole and carvacrol on Escherichia coli O157:H7 inhibition and its application on fresh-cut cucumbers. Food Control 144:109339. https://doi.org/10.1016/j.foodcont.2022.109339
Amine B, Nadir A, Nouara KO, Akila AT, Kamelia K, Ghania KB et al (2023) Impact of thermal and non-thermal pasteurization on the microbial inactivation of fruit juice: review. J Food Microbiol Saf Hyg 8(2):1–11. https://doi.org/10.35248/2476-2059.23.8.198
Armstrong JA, Sutton R, Criddle DN (2020) Pancreatic acinar cell preparation for oxygen consumption and lactate production analysis. Bio Protoc 10(10):e3627. https://doi.org/10.21769/BioProtoc.3627
Cardoso LT, Alexandre B, Cacciatore FA, Magedans YVDS, Fett-Neto AG, Contri RV, Malheiros PDS (2023) Carvacrol-loaded nanoemulsions produced with a natural emulsifier for lettuce sanitization. Food Res Int 168:112748. https://doi.org/10.1016/j.foodres.2023.112748
Carraro M, Bernardi P (2016) Calcium and reactive oxygen species in regulation of the mitochondrial permeability transition and of programmed cell death in yeast. Cell Calcium 60(2):102–107. https://doi.org/10.1016/j.ceca.2016.03.005
Chaillot J, Tebbji F, Remmal A, Boone C, Brown GW, Bellaoui M, Sellam A (2015) The monoterpene carvacrol generates Endoplasmic Reticulum stress in the pathogenic fungus Candida albicans. Antimicrob Agents Chemother 59(8):4584–4592. https://doi.org/10.1128/AAC.00551-15
Chavan PS, Tupe SG (2014) Antifungal activity and mechanism of action of carvacrol and thymol against vineyard and wine spoilage yeasts. Food Control 46:115–120. https://doi.org/10.1016/j.foodcont.2014.05.007
Errakhi R, Meimoun P, Lehner A, Vidal G, Briand J, Corbineau F et al (2008) Anion channel activity is necessary to induce ethylene synthesis and programmed cell death in response to oxalic acid. J Exp Bot 59(11):3121–3129. https://doi.org/10.1093/jxb/ern166
Garcia-Gonzalez L, Geeraerd AH, Spilimbergo S, Elst K, Van Ginneken L, Debevere J et al (2007) High pressure carbon dioxide inactivation of microorganisms in foods: the past, the present and the future. Int J Food Microbiol 117(1):1–28. https://doi.org/10.1016/j.ijfoodmicro.2007.02.018
Garcia-Gonzalez L, Geeraerd AH, Mast J, Briers Y, Elst K, Ginneken V et al (2010) Membrane permeabilization and cellular death of Escherichia coli, Listeria monocytogenes and Saccharomyces cerevisiae as induced by high pressure carbon dioxide treatment. Food Microbiol 27(4):541–549. https://doi.org/10.1016/j.fm.2009.12.004
Gong HS, Meng XC, Wang H (2010) Mode of action of plantaricin MG, a bacteriocin active against Salmonella typhimurium. J Basic Microbiol 50(S1):S37–S45. https://doi.org/10.1002/jobm.201000130
Guo Q, Qing YD, Qing LY, Du GG, Shi KH, Tang JY et al (2023) Improving microbiological and physicochemical properties of fresh-cut apples using carvacrol emulsions. Food Biosci 52:102450. https://doi.org/10.1016/j.fbio.2023.102450
Haas GJ, Prescott HE Jr, Dudley E, Dik R, Hintlian C, Keane L (1989) Inactivation of microorganisms by carbon dioxide under pressure. J Food Saf 9(4):253–265. https://doi.org/10.1111/j.1745-4565.1989.tb00525.x
Hong SI, Park WS, Pyun YR (2001) Non-thermal inactivation of Lactobacillus plantarum as influenced by pressure and temperature of pressurized carbon dioxide. Int J Food Sci Tech 34(2):125–130. https://doi.org/10.1046/j.1365-2621.1999.00241.x
Hutkins RW, Nannen NL (1993) pH homeostasis in lactic-acid bacteria. J Dairy Sci 76(8):2354–2365. https://doi.org/10.3168/jds.S0022-0302(93)77573-6
Jin TZ, Aboelhaggag RM (2022) Combined pulsed electric field with antimicrobial caps for extending shelf life of orange juice. Beverages 8(4):72. https://doi.org/10.3390/beverages8040072
Kachur K, Suntres Z (2020) The antibacterial properties of phenolic isomers, carvacrol and thymol. Crit Rev Food Sci Nutr 60(18):3042–3053. https://doi.org/10.1080/10408398.2019.1675585
Kamihira M, Taniguchi M, Kobayashi TJA, Chemistry B (1987) Sterilization of microorganisms with supercritical carbon dioxide. Agric Biol Chem 51(2):407–412. https://doi.org/10.1271/bbb1961.51.407
Kim WJ, Kang DH (2023) Synergistic effects of 915 MHz microwave heating and essential oils on inactivation of foodborne pathogen in hot-chili sauce. Int J Food Microbiol 398:110210. https://doi.org/10.1016/j.ijfoodmicro.2023.110210
Li H, Deng L, Chen Y, Liao XJ (2012a) Inactivation, morphology, interior structure and enzymatic activity of high pressure CO2-treated Saccharomyces cerevisiae. Innov Food Sci Emerg Technol 14:99–106. https://doi.org/10.1016/j.ifset.2011.11.009
Li H, Zhao L, Wu J, Zhang Y, Liao X (2012b) Inactivation of natural microorganisms in litchi juice by high-pressure carbon dioxide combined with mild heat and nisin. Food Microbiol 30(1):139–145. https://doi.org/10.1016/j.fm.2011.10.007
Lian ZM, Yang D, Wang YT, Zhao L, Rao L, Liao XJ (2023) Investigating the microbial inactivation effect of low temperature high pressure carbon dioxide and its application in frozen prawn (Penaeus vannamei). Food Control 145:109401. https://doi.org/10.1016/j.foodcont.2022.109401
Liu X, Li YF, Zhang R, Huangfu LL, Du GH, Xiang QS (2021) Inactivation effects and mechanisms of plasma-activated water combined with sodium laureth sulfate (SLES) against Saccharomyces cerevisiae. Appl Microbiol Biotechnol 105(7):2855–2865. https://doi.org/10.1007/s00253-021-11227-9
Lu R, Zhang X, Cheng X, Zhang Y, Zan X, Zhang L (2020) Medical applications based on supramolecular self-assembled materials from tannic acid. Front Chem 8:583484. https://doi.org/10.3389/fchem.2020.583484
Mansur AR, Lee HS, Lee CJ (2023) A review of the efficacy of ultraviolet c irradiation for decontamination of pathogenic and spoilage microorganisms in fruit juices. J Microbial Biotechnol 33(4):419–429. https://doi.org/10.4014/jmb.2212.12022
Meyssami B, Balaban MO, Teixeira AA (1992) Prediction of pH in model systems pressurized with carbon dioxide. Biotechnol Prog 8(2):149–154. https://doi.org/10.1021/bp00014a009
Mortazavi N, Aliakbarlu J (2019) Antibacterial effects of ultrasound, cinnamon essential oil, and their combination against Listeria monocytogenes and Salmonella Typhimurium in milk. J Food Sci 84(12):3700–3706. https://doi.org/10.1111/1750-3841.14914
Mosqueda-Melgar J, Raybaudi-Massilia RM, Martin-Belloso O (2008) Inactivation of Salmonella enterica Ser. Enteritidis in tomato juice by combining of high-intensity pulsed electric fields with natural antimicrobials. J Food Sci 73(2):M47–M53. https://doi.org/10.1111/j.1750-3841.2007.00646.x
Moulin C, Caumont-Sarcos A, Ieva R (2019) Mitochondrial presequence import: multiple regulatory knobs fine-tune mitochondrial biogenesis and homeostasis. Biochim Biophys Acta Mol Cell Res 1866(5):930–944. https://doi.org/10.1016/j.bbamcr.2019.02.012
Neves MF, Trombin VG, Marques VN, Martinez LF (2020) Global orange juice market: a 16-year summary and opportunities for creating value. Trop Plant Pathol 45(3):166–174. https://doi.org/10.1007/s40858-020-00378-1
Niu L, Liu J, Wang X, Wu Z, Xiang Q, Bai Y (2022) Effect of combined treatment with cinnamon oil and petit-high pressure CO2 against Saccharomyces cerevisiae. Foods 11(21):3474. https://doi.org/10.3390/foods11213474
Peleg M, Cole MB (1998) Reinterpretation of microbial survival curves. Crit Rev Food Sci Nutr 38(5):353–380. https://doi.org/10.1080/10408699891274246
Rao A, Zhang YQ, Muend S, Rao R (2010) Mechanism of antifungal activity of terpenoid phenols resembles calcium stress and inhibition of the TOR pathway. Antimicrob Agents Chemother 54(12):5062–5069. https://doi.org/10.1128/AAC.01050-10
Spilimbergo S (2002) A study about the effect of dense CO2 on microorganisms. Dissertation, University of Padova
Tchuenchieu A, Sado Kamdem S, Bevivino A, Etoa FX, Essia Ngang JJ (2022) Development of a predictive model of the microbial inactivation of L. monocytogenes during low thermal treatment of fruit juices in combination with carvacrol as aroma compound. Curr Res Food Sci 5:374–381. https://doi.org/10.1016/j.crfs.2022.02.002
Ultee A, Kets EP, Smid EJ (1999) Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol 65(10):4606–4610. https://doi.org/10.1128/AEM.65.10.4606-4610.1999
van Boekel MAJS (2002) On the use of the Weibull model to describe thermal inactivation of microbial vegetative cells. Int J Food Microbiol 74(1–2):139–159. https://doi.org/10.1016/S0168-1605(01)00742-5
Xiang QS, Wang WJ, Zhao DB, Niu LY, Li K, Bai YH (2019) Synergistic inactivation of Escherichia coli O157:H7 by plasma-activated water and mild heat. Food Control 106:106741. https://doi.org/10.1016/j.foodcont.2019.106741
Yang D, Wang Y, Zhao L, Rao L, Liao X (2022) Extracellular pH decline introduced by high pressure carbon dioxide is a main factor inducing bacteria to enter viable but non-culturable state. Food Res Int 151:110895. https://doi.org/10.1016/j.foodres.2021.110895
Zhan CF, Wu MC, Fang HD, Liu XY, Pan JY, Fan XY et al (2023) Characterization of the chemical fungicides-responsive and bacterial pathogen-preventing Bacillus licheniformis in rice spikelet. Food Qual Saf-Oxford 7:1–11. https://doi.org/10.1093/fqsafe/fyad005
Zhao L, Qin X, Han W, Wu X, Wang Y, Hu X et al (2018) Novel application of CO2-assisted high pressure processing in cucumber juice and apple juice. LWT 96:491–498. https://doi.org/10.1016/j.lwt.2018.06.003
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Research in this study was funded by the National Natural Science Foundation of China (No. 32001801).
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LN, QX, and YB conceived and designed the experiments. LN, ZW, and JL carried out the experiments. LN, ZW, and JL analyzed the data and wrote the original draft. YB revised the manuscript.
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Communicated by Yusuf Akhter.
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Niu, L., Wu, Z., Liu, J. et al. Enhancement effect of carvacrol on yeast inactivation by mild pressure carbon dioxide. Arch Microbiol 205, 353 (2023). https://doi.org/10.1007/s00203-023-03689-4
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DOI: https://doi.org/10.1007/s00203-023-03689-4