Growth and aflatoxin production of Aspergillus flavus in fig-based medium: Effect of minerals and chelating agents

Yıl 2020, Cilt: 26 Sayı: 7, 1223 - 1233, 07.12.2020

Sule Gunaydın Hakan Karaca

Öz

In this study, minerals required for the growth and aflatoxin production of A. flavus were determined. Then, the effectiveness of some chelating agents such as citric acid, phytic acid and ethylenediaminetetraacetic acid (EDTA) in preventing mold growth and toxin production was investigated in a fig-based medium and in two synthetic media, called Czapek-dox agar (CZA) and potato dextrose agar (PDA). A. flavus did not grow in CZA without sodium nitrate during 6-day incubation at 30 °C. The absence of the other components (magnesium sulfate, iron sulfate, potassium chloride and potassium phosphate) did not significantly (p>0.05) affect the growth of the mold. However, the mold produced significantly (p<0.05) higher amounts of aflatoxins in the media without magnesium sulfate and iron sulfate. A. flavus grew faster on fig-based medium and produced higher amounts of aflatoxins in PDA. In all media tested in this study, EDTA was found to be more effective than the other agents in controlling the growth of A. flavus. It was also effective in inhibiting the production of aflatoxins. It was determined that 1.75 mM EDTA reduced aflatoxin production up to 97% in PDA. Citric and phytic acids could inhibit the growth of the mold only in PDA. All chelating agent reduced aflatoxin production over 90% in fig-based medium.

Anahtar Kelimeler

Template mycotoxin, mold, Ethylenediaminetetraacetic acid, Citric acid, Phytic acid, Aflatoxin, Aspergillus flavus

Kaynakça

• [1] Setlem K, Monde B, Ramlal S, Kingston J. “Immuno affinity SELEX for simple, rapid, and cost-effective aptamer enrichment and identification against aflatoxin B1”. Frontiers in Microbiology, 7, 1909, 1-14, 2016.
• [2] IARC-International Agency for Research on Cancer. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans: Some Naturally Occurring Substances: Food Items and Constituents, Heterocyclic Aromatic Amines and Mycotoxins. Geneva, Switzerland, IARC, 1993.
• [3] Sasanian N, Sari AA, Mortazavian AM. “Effect of Thymus daenesis and Satureja hortensis L. essential oils on quality properties of Iranian Doogh.” Journal of Food Safety, Article Number e12527, 1-8, 2018.
• [4] Zhai HC, Zhang SB, Huang SX, Cai JP. “Prevention of toxigenic fungal growth in stored grains by carbon dioxide detection”. Food Additives and Contaminants: Part A, 32(4), 596-603, 2015.
• [5] RASFF. “Rapid Alert System for Food and Feed Annual Report”. European Commission. https://ec.europa.eu/food/sites/food/files/safety/docs/rasff_annual_report_2015.pdf (18.12.2015).
• [6] RASFF. “Rapid Alert System for Food and Feed Annual Report”. European Commission. https://ec.europa.eu/food/sites/food/files/safety/docs/rasff_annual_report_2016.pdf (08.12.2016).
• [7] RASFF. “Rapid Alert System for Food and Feed Annual Report”. European Commission. https://ec.europa.eu/food/sites/food/files/safety/docs/rasff_annual_report_2017.pdf (28.12.2017).
• [8] Shokri H. “Evaluation of inhibitory effects of citric and tartaric acids and their combination on the growth of Trichophyton mentagrophytes, Aspergillus fumigatus, Candida albicans, and Malassezia furfur”. Comparative Clinical Pathology, 20, 543-545, 2011.
• [9] Askarne L, Boubaker H, Boudyach EH, Aoumar AAB. “Use of food additives to control postharvest citrus blue mold disease”. Atlas Journal of Biology, 2, 147-153, 2013.
• [10] Ruhil S, Balhara M, Dhankhar S, Kumar M, Kumar V, Chhillar AK. “Advancement in infection control of opportunistic pathogen (Aspergillus spp.): Adjunctive agents”. Current Pharmaceutical Biotechnology, 14, 226-232, 2013.
• [11] Ruhil S, Kumar V, Balhara M, Malik M, Dhankhar S, Kumar M, Chhillar AK. “In vitro evaluation of combination of polyenes with EDTA against Aspergillus spp. by different methods (FICI and CI model)”. Journal of Applied Microbiology, 117, 643-653, 2014.
• [12] Türkkan M, Erper İ. “Inhibitory influence of organic and inorganic sodium salts and synthetic fungicides against bean root to pathogens”. Gesunde Pflanzen, 67, 83-94, 2015.
• [13] Demir ST, Ozar AI, Gülseri O, Çoksöyler N, Konca R, Aksoy U, Düzbastılar M, Sağdemir A. “Investigations on Occurrence and Prevention of Aflatoxin and Ochratoxin Contamination in Figs in Aegean Region”. Turkish Ministry of Agriculture and Rural Affairs, Ankara, Turkey, Project Report (Project No: KKGA-B-03-F-052), 1990.
• [14] Anonymous. “Sigma-Aldrich products”. https://www.sigmaaldrich.com/catalog/product /sial/70185?lang=en&region=TR (11.11.2018).
• [15] Jimenes-Quero A, Pollet E, Zhao M, Marchioni E, Averous L, Phalip V. “Itaconic and fumaric acid production from biomass hydrolysates by Aspergillus strains”. Journal of Microbiology and Biotechnology, 26, 1557-1565, 2016.
• [16] Jain R, Valiante V, Remme N, Docimo T, Heinekamp T, Hertweck C, Gershenzon J, Haas H, Brakhage AA. “Tha MAP kinase MpkA controls cell wall integrity, oxidative stress response, gliotoxin production and iron adaptation in Aspergillus fumigatus”. Molecular Microbiology, 82, 39-53, 2011.
• [17] Karaca H, Pérez-Gago MB, Taberner V, Palou L. “Evaluating food additives as antifungal agents against Monilinia fructicola in vitro and in hydroxypropyl methylcellulose-lipid composite edible coatings for plums”. International Journal of Food Microbiology, 179, 72-79, 2014.
• [18] FDA-United States Food and Drug Administration. “Department of Health and Human Services. BAM Media M127: Potato Dextrose Agar”. https://www.fda.gov/food/foodscienceresearch/laboratorymethods/ucm063519.htm (12.11.2018).
• [19] USDA-United States Department of Agriculture. “Agricultural Research Service, Natural Nutrient Database for Standard Reference Legacy Release”. https://ndb.nal.usda.gov/ndb/foods/show/09094?fgcd=&manu=&format=&count=&max=25&offset=&sort=default&order=asc&qlookup=DRIED+FIGS%2C+UPC%3A+722648711338&ds=&qt=&qp=&qa=&qn=&q=&ing= (12.11.2018).
• [20] Diener UL, Davis ND. “Aflatoxin Formation in Peanuts by Aspergillus flavus”. Agricultural Experiment Station, Auburn University, AL, USA, Bulletin 493, 1977.
• [21] Ellis WO, Smith JP, Simpson BK, Ramaswamy H, Doyon G. “Growth of and aflatoxin production by Aspergillus flavus in peanuts stored under modified atmosphere packaging (MAP) conditions”. International Journal of Food Microbiology, 22, 173-187, 1994.
• [22] Stroka J, Anklam E, Jörissen U, Gilbert J. “Immunoaffinity column cleanup with liquid chromatography using post-colum bromination for determination of aflatoxins in peanut butter, pistachio paste, fig paste and paprika powder: Collaborate study”. Journal of the Association of Official Analytical Chemists International, 83, 320-340, 2000.
• [23] Davis ND, Diener UL, Agnihotri VP. “Production of aflatoxin B1 and G1 in chemically defined medium”. Mycopathologia, 31, 251-256, 1967.
• [24] Aziz NH, Moussa AE. “Influence of white light, near UV irradiation and other environmental conditions on production of aflatoxin B1 by Aspergillus flavus and ochratoxin A by Aspergillus ochraceus”. Nahrung, 41, 150-154, 1997.
• [25] Zohri AA, Saber SM, Mostafa ME. “Effect of selenite and tellurite on the morphological growth and toxin production of Aspergillus parasiticus var. globosus IMI 120920”. Mycopathologia, 139, 51-57, 1997.
• [26] Holmquist GU, Walker HW, Stahr HM. “Influence of temperature, pH, water activity and antifungal agents on growth of Aspergillus flavus and A. parasiticus”. Journal of Food Science, 48, 778-782, 1983.
• [27] Shahin AA, Aziz NH. “Influence of gamma rays and sodium chloride on aflatoxin production by Aspergillus flavus”. Microbios, 90, 163-175, 1997.
• [28] Stiles J, Penkar S, Plocková M, Chumchalová J, Bullerman LB. “Antifungal activity of sodium acetate and Lactobacillus rhamnosus”. Journal of Food Protection, 65, 1188-1191, 2002.
• [29] Abu-Mejdad NMJA. “Response of some fungal species to the effect of copper, magnesium and zinc under the laboratory condition”. European Journal of Experimental Biology, 3, 535-540, 2013.
• [30] Stone RW, Farrell MA. “Synthetic media for penicillin production”. Science, 104, 445-446, 1946.
• [31] Jackson MJ, Slininger PJ, Bothast RJ. “Effect of zinc, iron, cobalt, and manganese on Fusarium moniliforme NRRL 13616 growth and fusarin C biosynthesis in submerged cultures”. Applied and Environmental Microbiology, 55, 649-655, 1989.
• [32] Payne GA, Hagler WM. “Effect of specific amino acids on growth and aflatoxin production by Aspergillus parasiticus and Aspergillus flavus in defined media”. Applied and Environmental Microbiology, 46, 805-812, 1983.
• [33] Ehrlich KC, Kobbeman K, Montalbano BG, Cotty PJ. “Aflatoxin-producing Aspergillus species from Thailand”. International Journal of Food Microbiology, 114, 153-159, 2007.
• [34] Kranthi VS, Rao DM, Jaganmohan P. “Production of protease by Aspergillus flavus through solid state fermentation using different oil seed cakes”. International Journal of Microbiology Research, 3, 12-15, 2012.
• [35] Mehl HL, Cotty PJ. “Nutrient environments influence competition among Aspergillus flavus genotypes”. Applied and Environmental Microbiology, 79, 1473-1480, 2013.
• [36] McAlpin CE, Wicklow DT. “Culture media and sources of nitrogen promoting the formation of stromata and ascocarps in Petromyces Alliaceus (Aspergillus section Flavi)”. Canadian Journal of Microbiology, 51, 765-771, 2005.
• [37] Wang B, Han X, Bai Y, Lin Z, Qui M, Nie X, Wang S, Zhang F, Zhuang Z, Yuan J, Wang S. “Effects of nitrogen metabolism on growth and aflatoxin biosynthesis in Aspergillus flavus”. Journal of Hazardous Materials, 15, 691-700, 2017.
• [38] Morton SG, Eadie T, Llewellyn GC. “Aflatoxigenic potential of dried figs, apricots, pineapple, and raisins”. Journal-Association of Official Analytical Chemists, 62, 958-962, 1979. [39] Ikechi-Nwogu CG, Elenwo EN. “Comparing the growth of fungal cultures on groundnut dextrose medium and potatoes dextrose medium”. Journal of Science, 1, 46-52, 2012.
• [40] Cotty PJ. “Comparison of four media for the isolation of Aspergillus flavus group fungi”. Mycopathologia, 125, 157-162, 1994.
• [41] Schultz J, Muller W. “Effects of organic acids on mould growth in feed containing meat”. Tierärztliche Umschau, 54, 98-101, 1999.
• [42] Basaran P. “Antifungal effect of acids and surface active compounds for post-harvest control of Aspergillus parasiticus growth on hazelnut”. Journal of Food Processing and Preservation, 35, 236-246, 2011.
• [43] Wu HS, Chen XQ, Yang XN, Liu YD, Zhao GM. “In vitro growth of Fusarium oxysporum f. sp niveum in chemically defined citric acid”. Asia Life Sciences, 20, 63-75, 2011.
• [44] Dayi C, Ling X, Rong Y. “Phytic acid inhibits the production of aflatoxin B1”. Journal of Food Processing and Preservation, 19, 27-32, 1995.
• [45] Yang Q, Zhang H, Zhang X, Zheng X, Qian J. “Phytic acid enhances biocontrol activity of Rhodotorula mucilaginosa against Penicillium expansum contamination and patulin production in apples”. Frontiers in Microbiology, 6, 1-9, 2015.
• [46] Askarne L, Talibi I, Boubaker H, Serghini MA. “Effects of organic acids and salts on the development of Penicillium italicum: The causal agent of citrus blue mold”. The Plant Pathology Journal, 10, 99-107, 2011.
• [47] Gowda NKS, Malathi V, Suganthi RU. “Effect of some chemical and herbal compounds on growth of Aspergillus parasiticus and aflatoxin production”. Animal Feed Science and Technology, 116, 281-291, 2004.
• [48] Zhang H, Yang Q, Lin H, Ren X, Zhau L, Hou J. “Phytic acid enhances biocontrol efficacy of Rhodotorula mucilaginosa against postharvest gray mold spoilage and natural spoilage of strawberries”. LWT-Food Science and Technology, 52, 110-115, 2013.
• [49] Mahunu GK, Zhang H, Yang Q, Zhang X, Li D, Zhou Y. “Improving the biocontrol efficacy of Pichia caribbica with phytic acid against postharvest blue mold and natural decay in apples”. Biological Control, 92, 172-180, 2016.
• [50] Abrunhosa L, Venãncio A. “In vitro antifungal effect of EDTA disodium salt in tested black Aspergilli”. Asian Journal of Biochemistry, 3, 176-181, 2008.
• [51] De Lucca AJ. 2006. “In vitro inhibitory and fungicidal properties of EDTA for Aspergillus and Fusarium species”. Interscience Conference on Antimicrobial Agents and Chemotherapy, San Francisco, CA, USA, 27-30 September 2006.
• [52] Pilegaard K. “Processes regulating nitric oxide emissions from soils”. Philosophical Transactions of the Royal Society B Biological Sciences, 368, 1-8, 2013.
• [53] Maas P, Sandt T, Klapwijk B, Lens P. “Biological reduction of nitric oxide in aqueous Fe(II)EDTA solutions”. Biotechnology Progress, 19, 1323-1328, 2003.
• [54] Lazar EE, Wills RBH, Ho BT, Harris AM, Spohr LJ. “Antifungal effect of gaseous nitric oxide on mycelium growth, sporulation and spore germination of the postharvest horticulture pathogens, Aspergillus niger, Monilinia fructicola and Penicillium italicum”. Letters in Applied Microbiology, 46, 688-692, 2008.
• [55] Stanojevic D, Comic L, Stefanovic O, Solujic-Sukdolak S. “Antimicrobial effects of sodium benzoate, sodium nitrite and potassium sorbate and their synergistic action in vitro”. Bulgarian Journal of Agricultural Science, 15, 307-311, 2009.
• [56] Fratamico PM, Bhunisa AK, Smith JL. Foodborne Pathogens Microbiology and Molecular Biology. 1st ed. Norwich, England, Academic Press, 2005.
• [57] Gur E, Demirag K. Chelating Agents. Editor: Altug T. Food Additives, 193-199, İzmir, Turkey, Sidas Publishing, 2009.
• [58] Reddy TV, Viswanathan L, Venkitasubramanian TA. “Factors affecting aflatoxin production by Aspergillus parasiticus in a chemically defined medium”. Journal of General Microbiology, 114, 409-413, 1979.
• [59] Marsh PB, Simpson ME, Trucksess MW. “Effects of trace metals on production of aflatoxins by Aspergillus parasiticus”. Applied Microbiology, 30, 52-57, 1975.
• [60] Tiwari RP, Mittal V, Bhalla TC, Saini SS, Singh G, Vadehra DV. “Effect of metal ions on aflatoxin production by Aspergillus parasiticus”. Folia Microbiologica, 31, 124-128, 1986.
• [61] Cuero R, Ouellet T, Yu J, Mogongwa N. “Metal ion enhancement of fungal growth gene expression and aflatoxin synthesis in Aspergillus flavus: RT-PCR characterization”. Journal of Applied Microbiology, 94, 953-961, 2003.
• [62] Guo B, Chen ZY, Lee RD, Scully BT. “Drought stress and preharvest aflatoxin contamination in agricultural commodity: Genetics, genomics and proteomics”. Journal of Integrative Plant Biology, 50, 1281-1291, 2008.
• [63] Schmidr-Heydt M, Magan N, Geisen R. “Stress induction of mycotoxin biosynthesis genes by abiotic factors”. FEMS Microbiology Letters, 284, 142-149, 2008.
• [64] Kachholz T, Demain AL. “Nitrate repression of averufin and aflatoxin biosynthesis”. Journal of Natural Products, 46, 499-506, 1983.
• [65] Ehrlich KC, Cotty PJ. “Variability in nitrogen regulation of aflatoxin production by Aspergillus flavus strains”. Applied Microbiology and Biotechnology, 60, 174-178, 2002.
• [66] Fakruddin M, Chowdhury A, Hossain MN, Ahmed MM. “Characterization of aflatoxin producing Aspergillus flavus from food and feed samples”. Springerplus, 4, 2-6, 2015.
• [67] Riba A, Bouras N, Mokrane S, Mathieu F, Lebrihi A, Sabaou N. “Aspergillus section Flavi and aflatoxins in Algerian wheat and derived products”. Food and Chemical Toxicology, 48, 2772-2777, 2010.
• [68] Wongjiratthiti A, Yottakot S. “Utilisation of local crops as alternative media for fungal growth”. Pentanika Journal of Tropical Agricultural Science, 40, 295-304, 2017.
• [69] Barolo MI, Mostacero NR, Lopez SN. “Ficus carica L. (Moraceae): An ancient source of food and health”. Food Chemistry, 164, 119-127, 2014.
• [70] Wildmann JD, Stoloff L, Jacobs R. “Aflatoxin production by a potent Aspergillus flavus Link isolate”. Biotechnology and Bioengineering, 9, 429-437, 1967.