Effect of pH and temperature in production of mycotoxins and antibiotics by phytopathogenic moulds for Persian lime (Citrus latifolia T.) in a complex lime pericarp-base medium
DOI:
https://doi.org/10.9755/ejfa.2017.v29.i10.1293Keywords:
Alternaria, antibiotics, Aspergillus, citric fruits moulds, mycotoxins, Persian limeAbstract
Post-harvest decay of citrus fruits is caused by moulds capable of producing mycotoxins with great impact on health. The objective of this study was to determine the effect of pH and temperature in synthesis of mycotoxins and antibiotics in Persian lime pathogenic and mycotoxigenic moulds, and to investigate the diffusion of mycotoxins inside the citrus fruit. As a result, several mycotoxins were identified, such as aflatoxins and fumonisins. In most of the analysed moulds, synthesis of the secondary metabolites was observed on acidic pH at 20 °C; some antibiotics were found as well. Diffusion of A. niger mycotoxins and antibiotics was observed in the interior of the lime fruit, achieving highest concentration in the septa. Knowing the behaviour of these moulds is useful for evaluation of health risk due to mycotoxins and control of pathogenic and mycotoxigenic post-harvest moulds.
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References
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Ariza, M. R., T. O. Larsen, B. O. Petersen, H. O. Duus and A. F. Barrero. 2002. Penicillium digitatum metabolites on synthetic media and citrus fruits. J. Agric. Food Chem. 50(22): 6361-6365.
Bamba, R. and G. Sumbali. 2005. Co-occurence of aflatoxin B1 and cyclopiazonic acid in sour lime (Citrus aurantifolia Swingle) during pot-harvest pathogenesis by Aspergillus flavus. Mycopathologia. 159(3): 407-411.
Barkai-Golan, R. and N. Paster. 2008. Mouldy fruits and vegetables as a source of mycotoxins: part one. World Mycotoxin J. 1(2): 147-159.
Borutova, R., Y. A. Aragon, K. Nährer and F. Berthiller. 2012. Co-occurrence and statistical correlations between mycotoxins in feedstuffs collected in the Asia–Oceania in 2010. Anim. Feed Sci. Tech. 178(3): 190-197.
Brzonkalik, K., T. Herrling, C. Syldatk and A. Neumann. 2011. The influence of different nitrogen and carbon sources on mycotoxin production in Alternaria alternata. Int. J. Food Microbiol. 147(2): 120–126.
Chen, J., C.J. Mirocha, W. Xie, L. Hogge, D. Olson. 1992. Production of the mycotoxin fumonisin B1 by Alternaria alternata f.sp. Lycopersici. Appl. Environ. Microbiol. 3928-3931.
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Esteban, A., M. L. Abarca, M. R. Bragulat and F. J. Cabañes. 2004. Effects of temperature and incubation time on production of ochratoxin A by black aspergilli. Res. Microb. 155(10): 861–866.
Faid M., A. Tantaoui-Elaraki. 1989. Production of Toxic Metabolites by Penicillium italicum y P. digitatum Isolated from Citrus Fruits. J. Food Protec.52 (3):194-197.
Fan, C., X. Cao, M. Liu, and W. Wang. 2016. Determination of Alternaria mycotoxins in wine and juice using ionic liquid modified countercurrent chromatography as a pretreatment method followed by high-performance liquid chromatography. J. Chromatogr. A. 1436:133-140.
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Frisvad, J. C., J. L. Smedsgaard, T. O. Larsen and R. A. Samson. 2004. Mycotoxins, drugs and other extrolites produced by species in Penicillium subgenus Penicillium. Stud. Mycol. 49: 201-241.
Frisvad, J. C., J. Smedsgaard, R. A. Samson, T. O. Larsen and U. Thrane. 2007. Fumonisin B2 Production by Aspergillus niger. J. Agric. Food Chem. 55(23): 9727–9732.
González-Sánchez, F. and R. Silva-Echeverría. 2003. Caracterización de las Cadenas Prioritarias e Identificación de las Demandas Tecnológicas: Cadena de Limón Mexicano. Colima. Universidad de Colima y Fundación Produce Colima, A. C. (Eds.).
Graham, F., L. Paradis, P. Bégin, J. Paradis, Y. Babin and A. Des Roches. 2014. Risk of allergic reaction and sensitization to antibiotics in foods. Ann. Allerg. Asthma Im. 113(3): 329–330.
Grenier, B. and I. P. Oswald. 2011. Mycotoxin co-contamination of food and feed: meta-analysis of publications describing toxicological interactions. World Mycotoxin J. 4 (3): 285-313
Huynh, V. L. and A. B. Lloyd. 1984. Synthesis and Degradation of Aflatoxins by Aspergillus parasiticus. I. Synthesis of aflatoxin Bl by young mycelium and its degradation in aging mycelium. Aust. J. of Biol. Science. 37(2): 37-44.
IARC (International Agency for Research on Cancer). WHO (World Health Organization). Monographs on the evaluation of carcinogenic risks to humans 2002. Lyon: IARCPress.
Jackson, L. S. and F. Al-Taher. 2008. Factors affecting mycotoxin production in fruits. In: Barkai-Golan R. and N. Paster, (Eds). Mouldy fruits and vegetables as a source of mycotoxins. Amsterdam: Elsevier Academic Press. pp. 75-104.
Laidou, I. A., C. C. Thanassoulopoulos and M. Liakopoulou-Kyriakides. 2001. Diffusion of patulin in the flesh of pears inoculated with four post‐harvest pathogens. J. Phytopathol. 149(7‐8): 457-461.
Magnani, R. F., G. D. De Souza and D. Rodrigues-Filho. 2007. Analysis of alternariol and alternariol monomethyl ether on flavedo and albedo tissues of tangerines (Citrus reticulata) with symptoms of alternaria brown spot. J. Agric. Food Chem. 55(13):4980-6.
Marino, A., A. Nostro and C. Fiorentino. 2009. Ochatoxin A production by Aspergillus westerdjkie in orange fruit and juice. Int. J. Food Microbiol. 132(2): 185–189.
Morgensen, J. M., J. C. Frisvad, U. Thrane and K. F. Nielsen. 2010. Production of fumonisin B2 and B4 by Aspergillus niger on grapes and raisins. J. Agric. Food Chem. 58(2): 954–958.
Ochoa, J. L., L. G. Hernández-Montiel, H. Latisniere-Barragán, J. L. León-De-La-Luz and C. P. Larralde Corona. 2007. Aislamiento e identificación de hongos patógenos de naranja Citrus sinensis L Osbeck cultivada en Baja California Sur, México. Ciencia y tecnología alimentaria. 5(005): 352-359.
Palou L., J. Usall, J. Pons, M.C. Cerdà, I. Viñas. 2001. Micoflora en centrales citrícolas de Tarragona. Investigación Agraria. Producción y Protección Vegetales. 16(3):448-462.
Passamani, F. R. F., T. Hernandes, N. A. Lopes, S. C. Bastos, W. D. Santiago, M. D. G. Cardoso and L. R. Batista. 2014. Effect of temperature, water activity, and pH on growth and production of ochratoxin A by Aspergillus niger and Aspergillus carbonarius from brazilian grapes. J. Food Protect. 77(11): 1947-1952.
Paulsch, W. E., E. A. Sizoo and H. P. Van Egmond. 1988. Liquid chromatographic determination of aflatoxins in feedstuffs containing citrus pulp. Association of Official Analytical Chemists 71(5): 957-961.
Perrone, G., A. Susca, G. Cozzi, K. Ehrlich, J. Varga, J. C. Frisvad, M. Meijer, P. Noomin, W. Mahakarnchanakul and R. A. Samson. 2007. Biodiversity of Aspergillus species in some important agricultural products. Stud. Mycol. 59: 53–66.
Phillips, I., M. Casewell, T. Cox, B. De Groot, C. Friis, R. Jones, C. Nightingale, R. Preston and J. Waddell. 2004. Does the use of antibiotics in food animals pose a risk to human health? A critical review of published data. J. Antimicrob. Chemoth. 53(1): 28–52
Pitt, J. I. and A. D. Hocking. 2009. Fungi and Food Spoilage. Third edition New York: Springer.
Pose, G., A. Patriarca, V. Kyanko, A. Pardo and V. Fernández-Pinto. 2010. Water activity and temperature effects on mycotoxin production by Alternaria alternata on a synthetic tomato medium. Int. J. Food Microbiol. 142(3): 348–353.
Restani, P. 2008. Diffution of mycotoxins in fruits and vegetables. In: Mouldy fruits and vegetables. Barkai-Golan R. and N. Paster (Eds). Amsterdam. Elsevier Academic Press. pp.105-114.
Romanazzi, G., J.L. Smilanick., E. Feliziani and S. Droby. 2016. Integrated management of postharvest gray mold on fruit crops. Postharvest Biol.Tec. 113:69-76.
Rychlik, M. and P. Schieberle. 2001. Model studies on the diffusion behavior of the mycotoxin patulin in apples, tomatoes, and wheat bread. Eur. Food Res. Tech. 212(3): 274-278.
Sandoval-Contreras, T. 2011. Caracterización fenotípica y genotípica de mohos y levaduras en limón mexicano (Citrus aurantifolia S.) y limón Persa (Citrus latifolia T.) procedentes de campos de cultivo y empacadoras de Jalisco y Colima. Tesis de Maestría. Centro Universitario de Ciencias Exactas e Ingenierías. Universidad de Guadalajara. México.
Sanzani, S.M., M. Reverberi and R. Geisen, R. 2016. Mycotoxins in harvested fruits and vegetables: Insights in producing fungi, biological role, conducive conditions, and tools to manage postharvest contamination. Postharvest Biol. Tec. 122: 95-105.
Stechina, D. E. 2005. Estudios de obtención de pectina aplicando procesos de membrana. Tesis de Maestría. Universidad Nacional Del Litoral. Argentina.
Stinson, E. E., F. O. Stanley, E, G. Heislerm, J. Siciliano and D. Bills. 1981. Mycotoxin production in whole tomatoes, apples, oranges, and lemons. J. Agric. Food Chem. 29 (4): 790–792.
Varga, J., S. Kocsubé, K. Suria, G. Y. Szigeti, A. Szekeres, M. Varga, B. Tóth and T.Bartók. 2010. Fumonisin contamination and fumonisin producing black Aspergilli in dried vine fruits of different origin. Int. J. Food Microbiol. 143(3): 143–149.
Varma, S. K. and R. A. Verma. 1987. Aflatoxin B1 production in orange (Citrus reticulata) juice by isolates of Aspergillus flavus link. Mycopathologia. 97(2): 101-104.
Vishwanath, V., M. Sulyok, R. Labuda, W. Bicker and R. Krska. 2009. Simultaneous determination of 186 fungal and bacterial metabolites in indoor matrices by liquid chromatography/tandem mass spectrometry. Anal. Bioanal. Chem. 395(5): 1355–1372.
Xing, Y., L. Tong, N. Chen, Z. Yu and Y. Zhao. 2015. Simultaneous determination of four aflatoxins in Citrus reticulata Blanco by ultra-performance liquid chromatography coupled with immunomagnetic beads for enrichment and purification. Chinese Journal of Chromatography 33 (12): 1320-1326.
Zachariasova, M.,Z. Dzuman, Z. Veprikova, K. Hajkova, M. Jiru, M. Vaclavikova, A. Zachariasova, M. Pospichalova, M. Florian, and J. Hajslova, J. (2014). Occurrence of multiple mycotoxins in European feedingstuffs, assessment of dietary intake by farm animals. Anim Feed Sci Tech. 193:124-140.
Zhao, K., B. Shao, D. Yang and F. Li. 2014. Natural Occurrence of Four Alternaria Mycotoxins in Tomato- and Citrus-Based Foods in China. J. Agric. Food Chem. 63 (1): 343–348.
Published
2017-11-04
How to Cite
Contreras, T. S.-., A. V.-. López, A. P. S.-. Beltrán, R. T.-. Vitela, and F. Ascencio. “Effect of PH and Temperature in Production of Mycotoxins and Antibiotics by Phytopathogenic Moulds for Persian Lime (Citrus Latifolia T.) in a Complex Lime Pericarp-Base Medium”. Emirates Journal of Food and Agriculture, vol. 29, no. 10, Nov. 2017, pp. 751-9, doi:10.9755/ejfa.2017.v29.i10.1293.
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