Mycoflora of fresh chokeberry (Aronia melanocarpa) and ochratoxin-producing ability of Penicillium isolates
Main Article Content
Keywords
ELISA, HPLC, moulds, mycotoxins
Abstract
Black chokeberry (Aronia melanocarpa) is a plant with unique health-promoting properties due to the high content of vitamins and polyphenols in its fruits. Despite their high resistance to spoilage, chokeberry fruits may get contaminated with mycotoxin-producing fungi. In the present study, samples of chokeberry fruits were collected from seven different sites in Bulgaria and their fungal profile was investigated. The most common moulds in fresh chokeberry were Penicillium sp. (77.5% out of all isolates), followed by Alternaria sp. (14.5%) and Bothrytis sp. (8%). Eighteen randomly chosen Penicillium isolates were further screened by enzyme-linked immuno sorbent assay (ELISA) for their ability to produce ochratoxin A (OTA) in liquid yeast extract sucrose medium. Four of the tested isolates (no. 11 from the region of Panagiurishte, no. 2 and 10 from the region of Plovdiv and no. 47 from the region of Koprivshtitsa) showed ability to produce OTA in concentrations 15.42, 14.62, 19.75 and 20.97 ng/ml, respectively (ELISA screening). High-performance liquid chromatography with post column fluorescence derivatisation analysis was also performed for all OTA-positive isolates. The maximum estimated OTA concentration was 27.47 ng/ml for isolate 47 from the region of Koprivshtitsa.
References
Abrunhosa, L., Paterson, R.R.M., Kozakiewicz, Z., Lima, N. and Vanancio, A., 2001. Mycotoxin production from fungi isolated from grapes. Letters in Applied and Environmental Microbiology 60: 2650-2652.
Al-Anati, L. and Petzinger, E., 2006. Immunotoxic activity of ochratoxin A. Journal of Veterinary Pharmacology and Therapeutics 29: 79-90.
Andersen, B., Smedsgaard, J. and Frisvad, J.C., 2004. Penicillium expansum: consistent production of patulin, chaetoglobosins and other secondary metabolites in culture and their natural occurrence in fruit products. Journal of Agricultural and Food Chemistry 52: 2421-2428.
Barkai-Golan, R., 2001. Postharvest diseases of fruits and vegetables. Development and control. Elsevier Science, Amsterdam, the Netherlands, 431 pp.
Barkai-Golan, R. and Paster N., 2008a. Mouldy fruits and vegetables as a source of mycotoxins. World Mycotoxin Journal 1: 147-159.
Barkai-Golan, R. and Paster N., 2008b. Mycotoxins in fruits and vegetables (1st Ed.). Academic Press, Elsevier, Salt Lake City, UT, USA, 408 pp.
Battilani, P., Pietri, A., Bertuzz, T., Languisco, L., Giorni, P. and Kokakiewicz, Z., 2003. Occurrence of ochratoxin A-producing fungi in grapes grown in Italy. Journal of Food Protection 66: 633-636.
Botton, A., Ferrigo, D., Scopel, C., Causin, R., Bonghi, C. and Ramina, A., 2008. A cDNA-AFLP approach to study ochratoxin A production in Aspergillus carbonarius. International Journal of Food Microbiology 127: 105-115.
Castillio, M.D., Gonzalez, H.H.L., Martinez, E.J., Pacin, A.M. and Resnik, S.L., 2004. Mycoflora and potential production of freshly harvested black bean from the Argentinean main production area. Mycopathologia 158: 107-112.
Doster, M.A., Michailides, T.J. and Morgan, D.P., 1996. Aspergillus species and mycotoxins in figs from California orchards. Plant Disease 80: 484-489.
Drush, S. and Ragab, W., 2003. Mycotoxins in fruits, fruit juices, and dried fruits. Journal of Food Protection 66: 1514-1527.
Fernández-Cruz, M.L., Mansilla, M.L. and Tadeo, J.L., 2010. Mycotoxins in fruits and their processed products: analysis, occurrence and health implications. Journal of Advanced Research 1: 113-122.
Fujii, S., Ono, E.Y.S., Ribeiro, R.M.R., Assunção, F.G.A., Takabayashi, C.R., Oliveira, T.C.R.M., Itano, E.N., Ueno, Y., Kawamura, O. and Hirooka, E.Y., 2007. A comparison between enzyme immunoassay and HPLC for ochratoxin A detection in green, roasted and instant coffee. Brazilian Archives of Biology and Technology 50: 349-359.
Flaj, D., Domijan, A.-M., Ivic, D., Cvetkovic, B. and Peraica, M., 2009. ELISA and HPLC analysis of ochratoxin A in red wines of Croatia. Food Control 20: 590-592.
Galvano, F., Ritieni, A., Piva, G. and Pietri, A., 2005. Mycotoxins in the human food chain. In: Diaz, D. (ed.) The mycotoxin blue book. Nottingham University Press, Nottingham, UK, 350 pp.
Garcia, D.J. Ramos, J.A., Sanchis, V. and Marin, S., 2009. Predicting mycotoxins in foods: a review. Food Microbiology 26: 757-769.
International Agency for Research on Cancer (IARC), 1993. Aflatoxins. In: Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. IARC Monographs on the Evaluation of Carcinogenic Risk to Humans, volume 56. IARC, Lyon, France, pp. 245-395.
Jackson, L.S. and Al-Taher, F., 2008. Factors affecting mycotoxin production in fruits. In: Barkai-Golan, R. and Paster, N. (eds.) Mycotoxins in fruits and vegetables. Academic Press, Elsevier, Salt Lake City, UT, USA, 408 pp.
Khoury, A. and Atoui, A., 2010. Ochratoxin A: general overview and actual molecular status. Toxins 2: 461-493.
Kokotkiewicz, A., Jaremicz, Z. and Luczkiewicz, M., 2010. Aronia plants: a review of traditional use, biological activities, and perspectives for modern medicine. Journal of Medicinal Foods 13: 255-269.
Kralova, J., Hajslova, J., Poustka, J., Hochmann, M., Bjelkova, M. and Odstrcilova, L., 2006. Occurrence of Alternaria toxins in fibre flax, linseed, and peas grown in organic and conventional farms: monitoring pilot study. Czech Journal of Food Sciences 24: 288-296.
Kulling, S.E. and Rawel, H.M., 2008. Chokeberry (Aronia melanocarpa) – a review on the characteristic components and potential health effect. Planta Medica 74: 1625-1634.
Lugauskas, A., Raudonien?, V., Varnait?, R. and Dirgin?iute, V., 2006. Ecological and sanitary significance of micromycetes brought from abroad with various foodstuffs of floral origin. Ekologija 3: 28-41.
Magan, N. and Olsen, M. (eds.), 2004. Mycotoxins in food: detection and control. Woodhead Publishing Limited and CRC Press LLC, Cambridge, UK, 471 pp.
Pardo, E., Sanchis, V., Ramos, A.J. and Marin, S., 2006. Non-specificity of nutritional substrate for ochratoxin A production by isolates of Aspergillus ochraceus. Food Microbiology 23: 351-358.
Pfohl-Leszkowicz, A., Petkova-Bocharova, T., Chernozemsky, I.N. and Castegnaro, M., 2002. Balkan endemic nephropathy and associated urinary tract tumours: a review on aetiological causes and the potential role of mycotoxins. Food Additives and Contaminants 19: 282-302.
Pitt, J.I., 1987. Penicillium viridicatum, Penicillium verrucosum, and production of ochratoxin A. Applied and Environmental Microbiology 53: 266-269.
Pitt, J.I. and Hocking, A.D., 2009. Fungi and food spoilage. Springer Science, New York, NY, USA, 520 pp.
Roze, L.V., Calvo, A.M., Gunterus, A., Beaudry, R., Kall, M. and Linz, J.E., 2004. Ethylene modulates development and toxin biosynthesis in Aspergillus possibly via an ethylene sensor-mediated signalling pathway. Journal of Food Protection 67: 438-447
Sage, L., Garon, D. and Seigle-Murandi, F., 2004. Fungal microflora and ochratoxin – a risk in French vineyards. Journal of Agricultural and Food Chemistry 52: 5764-5768.
Sekar, P., Yumnam, N. and Ponmurugan, K., 2008. Screening and characterization of mycotoxin producing fungi from dried fruits and grains. Advanced Biotech 6: 12-15.
Serra, R., Bragab, A. and Venâncio, A., 2005. Mycotoxin-producing and other fungi isolated from grapes for wine production, with particular emphasis on ochratoxin A. Research in Microbiology 156: 515-521.
Snowdon, A.L., 1990. A color atlas of post-harvest diseases and disorders of fruits and vegetables. Volume 1. General introduction and fruits. CRC Press, Boca Raton, FL, USA, 302 pp.
Stefanaki, I., Foufa, E., Tsatsou-Dritsa, A. and Dias, P., 2003. Ochratoxin A in Greek domestic wines and dried vine fruits. Food Additive and Contaminants 20: 74-83.
Teren, J., Hamari, Z., Rinyu, E. and Kevei, F., 1996. Immunochemical detection of ochratoxin A in black Aspergillus strains. Mycopatholgia 134: 171-176.
Torielli, E., Firrao, G., Locci, R. and Gobi, E., 2006. Ochratoxin A-producing of Penicillium spp. isolated from grapes used for the production of ‘passito’ wines. International Journal of Food Microbiology 106: 307-312.
Tournas, V.H. and Katsoudas, ?., 2005. Mould and yeast flora in fresh berries, grapes and citrus fruits. International Journal of Food Microbiology 105: 11-17.
Trinklein, D., 2010. Aronia: a berry good plant. Missouri Environment and Garden 13: 9.
Varga, J. and Kokakiewicz, Z., 2006. Ochratoxin A in grapes and grape-derived products. Trends in Food Science and Technology 17: 72-81.
Varga, J., Koncz, Z., Kocsubé, S., Mátrai, T., Téren, J., Ostry, V., Skarkova, J., Ruprich, J., Kubatova, A. and Kozakiewicz, Z., 2007. Mycobiota of grapes collected in Hungarian and Czech vineyards in 2004. Acta Alimentaria 36: 329-341.
Zheng, M.Z., Richard, J.L. and Binder, J., 2006. A review of rapid methods for the analysis of mycotoxin. Mucopathologia 161: 261-273.
Al-Anati, L. and Petzinger, E., 2006. Immunotoxic activity of ochratoxin A. Journal of Veterinary Pharmacology and Therapeutics 29: 79-90.
Andersen, B., Smedsgaard, J. and Frisvad, J.C., 2004. Penicillium expansum: consistent production of patulin, chaetoglobosins and other secondary metabolites in culture and their natural occurrence in fruit products. Journal of Agricultural and Food Chemistry 52: 2421-2428.
Barkai-Golan, R., 2001. Postharvest diseases of fruits and vegetables. Development and control. Elsevier Science, Amsterdam, the Netherlands, 431 pp.
Barkai-Golan, R. and Paster N., 2008a. Mouldy fruits and vegetables as a source of mycotoxins. World Mycotoxin Journal 1: 147-159.
Barkai-Golan, R. and Paster N., 2008b. Mycotoxins in fruits and vegetables (1st Ed.). Academic Press, Elsevier, Salt Lake City, UT, USA, 408 pp.
Battilani, P., Pietri, A., Bertuzz, T., Languisco, L., Giorni, P. and Kokakiewicz, Z., 2003. Occurrence of ochratoxin A-producing fungi in grapes grown in Italy. Journal of Food Protection 66: 633-636.
Botton, A., Ferrigo, D., Scopel, C., Causin, R., Bonghi, C. and Ramina, A., 2008. A cDNA-AFLP approach to study ochratoxin A production in Aspergillus carbonarius. International Journal of Food Microbiology 127: 105-115.
Castillio, M.D., Gonzalez, H.H.L., Martinez, E.J., Pacin, A.M. and Resnik, S.L., 2004. Mycoflora and potential production of freshly harvested black bean from the Argentinean main production area. Mycopathologia 158: 107-112.
Doster, M.A., Michailides, T.J. and Morgan, D.P., 1996. Aspergillus species and mycotoxins in figs from California orchards. Plant Disease 80: 484-489.
Drush, S. and Ragab, W., 2003. Mycotoxins in fruits, fruit juices, and dried fruits. Journal of Food Protection 66: 1514-1527.
Fernández-Cruz, M.L., Mansilla, M.L. and Tadeo, J.L., 2010. Mycotoxins in fruits and their processed products: analysis, occurrence and health implications. Journal of Advanced Research 1: 113-122.
Fujii, S., Ono, E.Y.S., Ribeiro, R.M.R., Assunção, F.G.A., Takabayashi, C.R., Oliveira, T.C.R.M., Itano, E.N., Ueno, Y., Kawamura, O. and Hirooka, E.Y., 2007. A comparison between enzyme immunoassay and HPLC for ochratoxin A detection in green, roasted and instant coffee. Brazilian Archives of Biology and Technology 50: 349-359.
Flaj, D., Domijan, A.-M., Ivic, D., Cvetkovic, B. and Peraica, M., 2009. ELISA and HPLC analysis of ochratoxin A in red wines of Croatia. Food Control 20: 590-592.
Galvano, F., Ritieni, A., Piva, G. and Pietri, A., 2005. Mycotoxins in the human food chain. In: Diaz, D. (ed.) The mycotoxin blue book. Nottingham University Press, Nottingham, UK, 350 pp.
Garcia, D.J. Ramos, J.A., Sanchis, V. and Marin, S., 2009. Predicting mycotoxins in foods: a review. Food Microbiology 26: 757-769.
International Agency for Research on Cancer (IARC), 1993. Aflatoxins. In: Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins. IARC Monographs on the Evaluation of Carcinogenic Risk to Humans, volume 56. IARC, Lyon, France, pp. 245-395.
Jackson, L.S. and Al-Taher, F., 2008. Factors affecting mycotoxin production in fruits. In: Barkai-Golan, R. and Paster, N. (eds.) Mycotoxins in fruits and vegetables. Academic Press, Elsevier, Salt Lake City, UT, USA, 408 pp.
Khoury, A. and Atoui, A., 2010. Ochratoxin A: general overview and actual molecular status. Toxins 2: 461-493.
Kokotkiewicz, A., Jaremicz, Z. and Luczkiewicz, M., 2010. Aronia plants: a review of traditional use, biological activities, and perspectives for modern medicine. Journal of Medicinal Foods 13: 255-269.
Kralova, J., Hajslova, J., Poustka, J., Hochmann, M., Bjelkova, M. and Odstrcilova, L., 2006. Occurrence of Alternaria toxins in fibre flax, linseed, and peas grown in organic and conventional farms: monitoring pilot study. Czech Journal of Food Sciences 24: 288-296.
Kulling, S.E. and Rawel, H.M., 2008. Chokeberry (Aronia melanocarpa) – a review on the characteristic components and potential health effect. Planta Medica 74: 1625-1634.
Lugauskas, A., Raudonien?, V., Varnait?, R. and Dirgin?iute, V., 2006. Ecological and sanitary significance of micromycetes brought from abroad with various foodstuffs of floral origin. Ekologija 3: 28-41.
Magan, N. and Olsen, M. (eds.), 2004. Mycotoxins in food: detection and control. Woodhead Publishing Limited and CRC Press LLC, Cambridge, UK, 471 pp.
Pardo, E., Sanchis, V., Ramos, A.J. and Marin, S., 2006. Non-specificity of nutritional substrate for ochratoxin A production by isolates of Aspergillus ochraceus. Food Microbiology 23: 351-358.
Pfohl-Leszkowicz, A., Petkova-Bocharova, T., Chernozemsky, I.N. and Castegnaro, M., 2002. Balkan endemic nephropathy and associated urinary tract tumours: a review on aetiological causes and the potential role of mycotoxins. Food Additives and Contaminants 19: 282-302.
Pitt, J.I., 1987. Penicillium viridicatum, Penicillium verrucosum, and production of ochratoxin A. Applied and Environmental Microbiology 53: 266-269.
Pitt, J.I. and Hocking, A.D., 2009. Fungi and food spoilage. Springer Science, New York, NY, USA, 520 pp.
Roze, L.V., Calvo, A.M., Gunterus, A., Beaudry, R., Kall, M. and Linz, J.E., 2004. Ethylene modulates development and toxin biosynthesis in Aspergillus possibly via an ethylene sensor-mediated signalling pathway. Journal of Food Protection 67: 438-447
Sage, L., Garon, D. and Seigle-Murandi, F., 2004. Fungal microflora and ochratoxin – a risk in French vineyards. Journal of Agricultural and Food Chemistry 52: 5764-5768.
Sekar, P., Yumnam, N. and Ponmurugan, K., 2008. Screening and characterization of mycotoxin producing fungi from dried fruits and grains. Advanced Biotech 6: 12-15.
Serra, R., Bragab, A. and Venâncio, A., 2005. Mycotoxin-producing and other fungi isolated from grapes for wine production, with particular emphasis on ochratoxin A. Research in Microbiology 156: 515-521.
Snowdon, A.L., 1990. A color atlas of post-harvest diseases and disorders of fruits and vegetables. Volume 1. General introduction and fruits. CRC Press, Boca Raton, FL, USA, 302 pp.
Stefanaki, I., Foufa, E., Tsatsou-Dritsa, A. and Dias, P., 2003. Ochratoxin A in Greek domestic wines and dried vine fruits. Food Additive and Contaminants 20: 74-83.
Teren, J., Hamari, Z., Rinyu, E. and Kevei, F., 1996. Immunochemical detection of ochratoxin A in black Aspergillus strains. Mycopatholgia 134: 171-176.
Torielli, E., Firrao, G., Locci, R. and Gobi, E., 2006. Ochratoxin A-producing of Penicillium spp. isolated from grapes used for the production of ‘passito’ wines. International Journal of Food Microbiology 106: 307-312.
Tournas, V.H. and Katsoudas, ?., 2005. Mould and yeast flora in fresh berries, grapes and citrus fruits. International Journal of Food Microbiology 105: 11-17.
Trinklein, D., 2010. Aronia: a berry good plant. Missouri Environment and Garden 13: 9.
Varga, J. and Kokakiewicz, Z., 2006. Ochratoxin A in grapes and grape-derived products. Trends in Food Science and Technology 17: 72-81.
Varga, J., Koncz, Z., Kocsubé, S., Mátrai, T., Téren, J., Ostry, V., Skarkova, J., Ruprich, J., Kubatova, A. and Kozakiewicz, Z., 2007. Mycobiota of grapes collected in Hungarian and Czech vineyards in 2004. Acta Alimentaria 36: 329-341.
Zheng, M.Z., Richard, J.L. and Binder, J., 2006. A review of rapid methods for the analysis of mycotoxin. Mucopathologia 161: 261-273.
Article Sidebar
Published
Apr 16, 2014
Article Details
Issue
Section
Research Article
