Degradation of aflatoxin B1 from naturally contaminated maize using the edible fungus Pleurotus ostreatus

Lauren W. JacksonIII and Barry M. Pryor

Updated:2017-08-31 10:50:27.0

Aflatoxins are highly carcinogenic secondary metabolites that can contaminate approximately 25% of crops and that cause or exacerbate multiple adverse health conditions, especially in Sub-Saharan Africa and South and Southeast Asia.  Regulation of mycotoxins is lacking in many developing nations where aflatoxin-related health problems are most severe, and approximately 4.5 billion people are chronically exposed . Aflatoxins are tightly regulated in the U.S. and European Union (EU), where the maximum allowable aflatoxin concentration in foods intended for human consumption range from 4 to 20 ng g−1 (Henry et al. 1999). The maximum contamination level of feed intended for non-dairy livestock in the U.S. is 300 ng g−1 (Kensler et al. 2011).

 Biological detoxification methods are promising because they are assumed to be cheaper and more environmentally friendly compared to chemical alternatives. White-rot fungi produce non-specific enzymes that are known to degrade aflatoxin in in situ and ex situ experiments. Motomura et al. (2003) isolated an unidentified enzyme from Pleurotus ostreatus that reduced the fluorescence of AFB1 and attributed this to the disruption of its lactone ring that plays an important role in carcinogenicity. Alberts et al. (2009) later showed that supernatant from P. ostreatusdegraded AFB1 by up to 76% and that degradation efficiency was strongly correlated with the activity level of pure laccase. Wang et al. (2011) and Yehia (2014) used manganese peroxidases fromPhanerochaete sordida and P. ostreatus, respectively, to degrade AFB1 in ex situ experiments. In a microcosm study, Das et al. (2014) demonstrated enhanced degradation of AFB1 in rice straw by P. ostreatus in the presence of certain surfactants and metal salts, and identified several potential breakdown products. Two strains of P. ostreatus were also used to degrade AFB1 in a co-cultivation experiment with Aspergillus flavus on rice straw revealing that one strain demonstrated superior degradation efficiency (Das et al. 2015).

A recent study reported that vegetative growth and yield characteristics of P. ostreatus were not inhibited by the presence of AFB1. AFB1 was degraded by up to 94% by the Blue strain. No aflatoxin could be detected in P. ostreatus mushrooms produced from AFB1-contaminated maize. Moreover, the mutagenicity of breakdown products from the maize substrate, and reversion of breakdown products to the parent compound, were minimal. These results suggest that P. ostreatus significantly degrades AFB1 in naturally contaminated maize under standard cultivation techniques to levels that are acceptable for some livestock fodder, and that using P. ostreatus to bioconvert crops into mushrooms can reduce AFB1-related losses.

Pleurotus ostreatus can be cultivated on a diverse array of lignocellulosic substrates that can be directly consumed as, or are byproducts from, food intended for human or animal consumption, and which are also highly susceptible aflatoxin contamination e.g. maize, groundnuts, tree nuts, etc. This work adds to the growing body of evidence showing that microbes, especially white-rot fungi, can be used to degrade aflatoxin in crops intended for livestock consumption. 

The results here show that even highly contaminated maize can be detoxified to levels that are acceptable for some uses as livestock fodder according to U.S. standards.  P. ostreatus-treated, lignocellulosic materials and edible oyster mushrooms from the genus Pleurotus have been used as a feed supplement for a variety of animals in studies unrelated (e.g. Adamovic et al. 1998) and related to aflatoxin contamination including a in a study by Yogeswari et al. (2012) that reported a hepatoprotective effect of Pleurotus sajor-caju mushrooms on chickens that were simultaneously fed aflatoxin-contaminated feed. Continued research is needed to identify ligninolytic fungal strains that consistently and completely degrade aflatoxin, but the demonstrated degradation capacity of P. ostreatus and its renowned edibility make it a superior candidate for further investigation.