Comparison of the aflatoxin B1 production pattern in fungal biomass and growth medium in toxigenic Aspergillus species of northern isolates of Iran

Document Type : Research Paper

Authors

1 PhD Graduated of Microbiology, Faculty of Basic Sciences, Lahijan Branch, Islamic Azad University, Lahijan, Iran

2 Assistant Professor, Department of Microbiology, Faculty of Basic Sciences, Lahijan Branch, Islamic Azad University, Lahijan, Iran

3 Associated Professor, Department of Basic Sciences, Faculty of Veterinary Medicine, Shahid Chamran University of Ahvaz, Ahvaz, Iran

4 Associated Professor, Department of Microbiology, Faculty of Basic Sciences, Lahijan Branch, Islamic Azad University, Lahija, Iran

5 Assistant Professor, Department of Statistics, Faculty of Basic Sciences, Lahijan Branch, Islamic Azad University, Lahijan, Iran

Abstract

Aflatoxin is the most economically important mycotoxin in the world. The most toxic form of aflatoxin is aflatoxin B1. It is one of the few fungal toxins that is regulated by the US food and drug administration; moreover, compared with other mycotoxins, more is known about its biology and biosynthesis. In the present study, we aimed at detecting the ability of producing aflatoxin B1 in different Aspergillus species that have been isolated from agro-ecological zones and processing plants in the North of Iran. Also, through using the ELISA method, the aflatoxin B1 production pattern was compared between fungal biomass and growth medium in toxicogenic isolates. The results showed that all of the studied Aspergillus species isolates tended to produce aflatoxin B1. Although there was a statically significant difference in the mean of aflatoxin B1 in growth medium and cell extract in several species, in A. flavus, A. parasiticus, A. sojae, A. terreus, A. ostianus, A. carbonarius, A. wentii storing, the toxin in fungal cell was more than that of releasing toxin in matrix culture medium. In the other isolates including A. niger, A. foetidus, and A. ocraceus, export of toxin was more than that of cell storage. We concluded that toxicogenic isolates of Aspergillus spp can be found in all studied geographic areas of Northern Iran. Although the behavior of species in releasing of aflatoxin into the growth environment was different, we hypothesized that it depends on different mechanisms that effect on export toxin into the external environment.

Keywords


Adhikari, B.N.; Bandyopadhyay, R. and Cotty, P.J. (2016). Degeneration of aflatoxin gene clusters in Aspergillus flavus from Africa and North America. AMB Express, 6(1): 62.
Afsah‐Hejri, L.; Jinap, S.; Hajeb, P.; Radu, S. and Shakibazadeh, S. (2013). A review on mycotoxins in food and feed: Malaysia case study. Comprehensive Reviews in Food Science and Food Safety, 12(6): 629-651.
Alshannaq, A. and Yu, J.H. (2017). Occurrence, toxicity, and analysis of major mycotoxins in food. International Journal of Environmental Research and Public Health, 14(6): 632.
Ardic, M.; Karakaya, Y.; Atasever, M. and Durmaz, H. (2008). Determination of aflatoxin B1 levels in deep-red ground pepper (isot) using immunoaffinity column combined with ELISA. Food and Chemical Toxicology, 46(5): 1596-1599.
Atasever, M.A.; Atasever, M.; ÖZTURAN, K. and Urcar, S. (2010). Determination of aflatoxin M1 level in butter samples consumed in Erzurum, Turkey. Kafkas Universitesi Veteriner Fakultesi Dergisi, 16: 159-162.
Aycicek, H.; Aksoy, A. and Saygi, S. (2005). Determination of aflatoxin levels in some dairy and food products which consumed in Ankara, Turkey. Food Control, 16(3): 263-266.
Bandyopadhyay, R.; Ortega-Beltran, A.; Akande, A.; Mutegi, C.; Atehnkeng, J.; Kaptoge, L. and Cotty, P. (2016). Biological control of aflatoxins in Africa: current status and potential challenges in the face of climate change. World Mycotoxin Journal, 9(5):771-789.
Caceres, I., Khoury, A. A., Khoury, R. E., Lorber, S., Oswald, I. P., Khoury, A. E., . . . Bailly, J.-D. (2020). Aflatoxin Biosynthesis and Genetic Regulation : A Review. Toxins, 12(3), 150.
Chanda, A.; Roze, L.V. and Linz, J.E. (2010). A possible role for exocytosis in aflatoxin export in Aspergillus parasiticus. Eukaryotic Cell, 9(11): 1724-1727.
Chang, P.K.; Yu, J. and Yu, J.H. (2004). aflT, a MFS transporter-encoding gene located in the aflatoxin gene cluster, does not have a significant role in aflatoxin secretion. Fungal Genetics and Biology, 41(10): 911-920.
Cotty, P. (1994). Influence of field application of an atoxigenic strain of Aspergillus flavus on the populations of A. flavus infecting cotton bolls and on the aflatoxin content of cottonseed. Phytopathology, 84(11): 1270-1277.
Cotty, P.J. and Jaime-Garcia, R. (2007). Influences of climate on aflatoxin producing fungi and aflatoxin contamination. International Journal of Food Microbiology, 119(1-2): 109-115.
Fox, E.M. and Howlett, B.J. (2008). Secondary metabolism: regulation and role in fungal biology. Current Opinion in Microbiology, 11(6): 481-487.
Frisvad, J.C.; Andersen, B. and Thrane, U. (2008). The use of secondary metabolite profiling in chemotaxonomy of filamentous fungi. Mycological Research, 112(2): 231-240.
Frisvad, J.C.; Larsen, T.O.; De Vries, R.; Meijer, M.; Houbraken, J.; Cabañes, F. and Samson, R. (2007). Secondary metabolite profiling, growth profiles and other tools for species recognition and important Aspergillus mycotoxins. Studies in Mycology, 59: 31-37.
Islam, M.S.; Callicott, K.A.; Mutegi, C.; Bandyopadhyay, R. and Cotty, P.J. (2018). Aspergillus flavus resident in Kenya: High genetic diversity in an ancient population primarily shaped by clonal reproduction and mutation-driven evolution. Fungal Ecology, 35: 20-33.
Klich, M.A. (2002). Biogeography of Aspergillus species in soil and litter. Mycologia, 94(1): 21-27.
Klich, M.A. (2007). Aspergillus flavus: the major producer of aflatoxin. Molecular Plant Pathology, 8(6): 713-722.
Lai, X.; Zhang, H.; Liu, R. and Liu, C. (2015). Potential for aflatoxin B1 and B2 production by Aspergillus flavus strains isolated from rice samples. Saudi Journal of Biological Sciences, 22(2): 176-180.
Levin, R.E. (2012). PCR detection of aflatoxin producing fungi and its limitations. International Journal of Food Microbiology, 156(1): 1-6.
Lin, Y.; Ayres, J. and Koehler, P. (1980). Influence of temperature cycling on the production of aflatoxins B1 and G1 by Aspergillus parasiticus. Applied and Environmental Microbiology, 40(2): 333-336.
Ma, H.; Zhang, N.;Sun, L. and Qi, D. (2015). Effects of different substrates and oils on aflatoxin B 1 production by Aspergillus parasiticus. European Food Research and Technology, 240(3): 627-634.
McKean, C.; Tang, L.; Billam, M.; Tang, M.; Theodorakis, C.W.; Kendall, R.J. and Wang, J.S. (2006). Comparative acute and combinative toxicity of aflatoxin B1 and T‐2 toxin in animals and immortalized human cell lines. Journal of Applied Toxicology: An International Journal, 26(2): 139-147.
Pitt, J. and Samson, R. (2007). Nomenclatural considerations in naming species of Aspergillus and its teleomorphs. Studies in Mycology, 59: 67-70.
Rosi, P.; Borsari, A.;  Lasi, G.; Lodi, S.; Galanti, A.; Fava, A. and Ferri, E. (2007). Aflatoxin M1 in milk: Reliability of the immunoenzymatic assay. International Dairy Journal, 17(5), 429-435.
Roze, L.V.; Chanda, A.; Laivenieks, M.; Beaudry, R.M.; Artymovich, K.A.; Koptina, A.V. and Linz, J.E. (2010). Volatile profiling reveals intracellular metabolic changes in Aspergillus parasiticus: veA regulates branched chain amino acid and ethanol metabolism. BMC Biochemistry, 11(1): 33.
Shoji, J.Y.; Arioka, M. and Kitamoto, K. (2008). Dissecting cellular components of the secretory pathway in filamentous fungi: insights into their application for protein production. Biotechnology Letters, 30(1): 7-14.
Shuaib, F.M.; Ehiri, J.; Abdullahi, A.; Williams, J.H. and Jolly, P.E. (2010). Reproductive health effects of aflatoxins: a review of the literature. Reproductive Toxicology, 29(3):262-270.
Sirikantaramas, S.; Yamazaki, M. and Saito, K. (2008). Mechanisms of resistance to self-produced toxic secondary metabolites in plants. Phytochemistry Reviews, 7(3): 467.
Tanaka, Y.; Sasaki, N. and Ohmiya, A. (2008). Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. The Plant Journal, 54(4): 733-749.
Varga, J.; Frisvad, J.C. and Samson, R. (2011). Two new aflatoxin producing species, and an overview of Aspergillus section Flavi. Studies in Mycology, 69: 57-80.
Yin, Y.N.; Yan, L.Y.; Jiang, J.H. and Ma, Z.H. (2008). Biological control of aflatoxin contamination of crops. Journal of Zhejiang University Science B, 9(10):787-792.