Abstract
Aspergillus ochraceus is a soil fungus known to produce ochratoxin A, a harmful secondary metabolite. Prevention and control of fungal pathogens mostly rely on chemical fungicides, which is one of the contributing factors in the emergence of the fungal resistance, hence novel methods for fungal eradication have been extensively researched. The cold atmospheric pressure (CAP) plasma generated in ambient air has been recently applied in microbial decontamination. Here we used the diffuse coplanar surface barrier discharge in inactivation of a toxigenic strain A. ochraceus. The plasma-treated conidia and mycelium exhibited morphological changes such as ruptures and desiccation. Mycelium dehydration and changes in the chemical composition of hyphal surface accompanied plasma treatment. The growth of 26 h old mycelia were significantly restricted after 30 s of plasma treatment. The conidial vitality declined 4 logs after 180 s of plasma exposure leading to almost complete decontamination. After shorter plasma treatment of conidia, the ochratoxin A (OTA) production increased at the early stage of cultivation, but the overall level was significantly reduced compared to untreated samples after longer cultivation. Our results indicated that the fungal growth and the OTA production were significantly changed by plasma treatment and underscored CAP plasma as a promising method in the decontamination of A. ochraceus without a risk to generate strains with increased OTA production.
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References
Arjunan KP, Sharma VK, Ptasinska S (2015) Effects of atmospheric pressure plasmas on isolated and cellular DNA—a review. Int J Mol Sci 16:2971–3016
Bistis GN, Perkins DD, Read ND (2003) Different cell types in Neurospora crassa. Fung Genet Rep 50:17–19
Bourke P, Ziuzina D, Han L, Cullen PJ, Gilmore BF (2017) Microbiological interactions with cold plasma. J Appl Microbiol 123:308–324
Černák M, Černáková L, Hudec I, Kováčik D, Zahoranová A (2009) Diffuse coplanar surface barrier discharge and its applications for in-line processing of low-added-value materials. Eur Phys J Appl Phys 47:22806
Černák M, Kováčik D, Ráheľ J, Sťahel P, Zahoranová A, Kubincová J, Tóth A, Černáková Ľ (2011) Generation of a high-density highly non-equilibrium air plasma for high-speed large-area flat surface processing. Plasma Phys Control Fusion 53:124031
Cullen PJ, Lalor J, Scally L, Boehm D, Milosavljević V, Bourke P, Keener K (2017) Translation of plasma technology from the lab to the food industry. Plasma Process Polym. https://doi.org/10.1002/ppap.201700085
Dasan BG, Mutlu M, Boyaci IH (2015) Decontamination of Aspergillus flavus and Aspergillus parasiticus spores on hazelnuts via atmospheric pressure fluidized bed plasma reactor. Int J Food Microbiol 216:50–59
Dasan BG, Boyaci IH, Mutlu M (2016) Inactivation of aflatoxigenic fungi (Aspergillus spp.) on granular food model, maize, in an atmospheric pressure fluidized bed plasma system. Food Control 70:1–8
Durand N, Fontana A, Meile JC, Suarez-Quiroz ML, Schorr-Galindo S, Montet D (2018) Differentiation and quantification of the ochratoxin A producers Aspergillus ochraceus and Aspergillus westerdijkiae using PCR-DGGE. J Basic Microbiol 59:158–165
Durek J, Schlüter O, Roscher A, Durek P, Fröhling A (2018) Inhibition or stimulation of ochratoxin a synthesis on inoculated barley triggered by diffuse coplanar surface barrier discharge plasma. Front Microbiol 9:1–9
Gallo A, Ferrara M, Perrone G (2017) Recent advances on the molecular aspects of ochratoxin A biosynthesis. Curr Opin Food Sci 17:49–56
Grintzalis K, Vernardis SI, Klapa MI, Georgiou CD (2014) Role of oxidative stress in sclerotial differentiation and aflatoxin B1 biosynthesis in Aspergillus flavus. Appl Environ Microbiol 80:55
Gupta RC, Lasher MA, Mukherjee IRM, Srivastava A, Lall R (2017) Aflatoxins, ochratoxins, and citrinin. In: Gupta RC (ed) Reproductive and developmental toxicology. Elsevier, Amsterdam, pp 945–962
Hojnik N, Cvelbar U, Tavčar-Kalcher G, Walsh JL, Križaj I (2017) Mycotoxin decontamination of food: cold atmospheric pressure plasma versus “classic” decontamination. Toxins (Basel) 9:1–19
Homola T, Matoušek J, Medvecká V, Zahoranová A, Kormunda M, Kováčik D, Černák M (2012) Atmospheric pressure diffuse plasma in ambient air for ITO surface cleaning. Appl Surf Sci 258:7135–7139
Hua H, Xing F, Selvaraj JN, Wang Y, Zhao Y, Zhou L, Liu X, Liu Y (2014) Inhibitory effect of essential oils on Aspergillus ochraceus growth and ochratoxin a production. PLoS ONE 9:1–10
Ismaiel AA, Papenbrock J (2015) Mycotoxins: producing fungi and mechanisms of phytotoxicity. Agriculture 5:492–537
Laroussi M (2005) Low temperature plasma-based sterilization: overview and state-of-the-art. Plasma Process Polym 2:391–400
Ma Y, Zhang GJ, Shi XM, Xu GM, Yang Y (2008) Chemical mechanisms of bacterial inactivation using dielectric barrier discharge plasma in atmospheric air. IEEE Trans Plasma Sci 36:1615–1620
Mai-Prochnow A, Clauson M, Hong J, Murphy AB (2016) Gram positive and Gram negative bacteria differ in their sensitivity to cold plasma. Sci Rep 6:1–11
Mcintyre M, Müller C, Dynesen J, Nielsen J (2001) Metabolic engineering. Adv Biochem Eng Biotechnol 73:103–128
Metselaar KI, den Besten HM, Abee T, Moezelaar R, Zwietering MH (2013) Isolation and quantification of highly acid resistant variants of Listeria monocytogenes. Int J Food Microbiol 666:508–514
Muranyi P, Wunderlich J, Heise M (2007) Sterilization efficiency of a cascaded dielectric barrier discharge. J Appl Microbiol 103:1535–1544
Ouf SA, Basher AH, Mohamed AAH (2015) Inhibitory effect of double atmospheric pressure argon cold plasma on spores and mycotoxin production of Aspergillus niger contaminating date palm fruits. J Sci Food Agric 95:3204–3210
Ringot D, Chango A, Schneider Y, Larondelle Y (2006) Toxicokinetics and toxicodynamics of ochratoxin A, an update. Chemico 159:18–46
Sakudo A, Toyokawa Y, Misawa T, Imanishi Y (2017) Degradation and detoxification of aflatoxin B1 using nitrogen gas plasma generated by a static induction thyristor as a pulsed power supply. Food Control 73:619–626
Shi H, Ileleji K, Stroshine RL, Keener K, Jensen JL (2017) Reduction of aflatoxin in corn by high voltage atmospheric cold plasma. Food Bioprocess Technol 10:1042–1052
Šimončicová J, Kaliňáková B, Kováčik D, Medvecká V, Lakatoš B, Kryštofová S, Hoppanová L, Palušková V, Hudecová D, Ďurina P, Zahoranová A (2018) Cold plasma treatment triggers antioxidative defense system and induces changes in hyphal surface and subcellular structures of Aspergillus flavus. Appl Microbiol Biotechnol 102:6647–6658
Suhem K, Matan N, Nisoa M, Matan N (2013) Inhibition of Aspergillus flavus on agar media and brown rice cereal bars using cold atmospheric plasma treatment. Int J Food Microbiol 161:107–111
Tao Y, Xie S, Xu F, Liu A, Wang Y, Chen D, Pan Y, Huang L, Peng D, Wang X, Yuan Z (2018) Ochratoxin A: toxicity, oxidative stress and metabolism. Food Chem Toxicol 112:320–331
Van der Merwe KJ, Steyn PS, Fourie L, Scott DB, Theron JJ (1965) Ochratoxin A, a toxic metabolite produced by Aspergillus ochraceus Wilh. Nature 205:1112
Varga J, Baranyi N, Chandrasekaran M, Vágvölgyi C (2015) Mycotoxin producers in the Aspergillus genus: an update. Acta Biol Szeged 59:151–167
Veroli GY, Di Fornari C, Goldlust I, Mills G, Koh SB, Bramhall JL, Richards FM, Jodrell DI (2015) An automated fitting procedure and software for dose-response curves with multiphasic features. Sci Rep 5:14701
Wang Y, Wang L, Liu F, Wang Q, Selvaraj JN, Xing F, Zhao Y, Liu Y (2016) Ochratoxin A producing fungi, biosynthetic pathway and regulatory mechanisms. Toxins (Basel) 8:1–15
WHO—World Health Organization & International Agency for Research on Cancer (1993) Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. WHO 56
Yong IH, Lee H, Park S, Park J, Choe W, Jung S, Jo C (2017) Flexible thin-layer plasma inactivation of bacteria and mold survival in beef jerky packaging and its effects on the meat’s physicochemical properties. Meat Sci 123:151–156
Yoshino K, Matsumoto H, Iwasaki T, Kinoshita S, Noda K, Iwamori S (2013) Monitoring of sterilization in an oxygen plasma apparatus, employing a quartz crystal microbalance (QCM) method. Vacuum 93:84–89
Zahoranová A, Henselová M, Hudecová D, Kaliňáková B, Kováčik D, Medvecká V, Černák M (2016) Effect of cold atmospheric pressure plasma on the wheat seedlings vigor and on the inactivation of microorganisms on the seeds surface. Plasma Chem Plasma Process 36:397–414
Zahoranová A, Hoppanová L, Šimončicová J, Tučeková Z, Medvecká V, Hudecová D, Kaliňáková B, Kováčik D, Černák M (2018) Effect of cold atmospheric pressure plasma on maize seeds: enhancement of seedlings growth and surface microorganisms inactivation. Plasma Chem Plasma Process 38:969–988
Acknowledgements
This study was supported by the Slovak Research and Development Agency under the Contract No. APVV-16-0216.
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Conceptualization: JD, LH; Methodology: JD, LH, BK; Formal analysis and investigation: JD, PĎ, LH, DK, VM; Writing—original draft preparation: LH; Writing—review and editing: SK; Supervision: BK, AZ. All authors have read and approved the final version of the manuscript.
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Hoppanová, L., Dylíková, J., Kováčik, D. et al. The effect of cold atmospheric pressure plasma on Aspergillus ochraceus and ochratoxin A production. Antonie van Leeuwenhoek 113, 1479–1488 (2020). https://doi.org/10.1007/s10482-020-01457-8
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DOI: https://doi.org/10.1007/s10482-020-01457-8