Cleavage of Zearalenone by Trichosporon mycotoxinivorans to a Novel Nonestrogenic Metabolite

Abstract

Zearalenone (ZON) is a potent estrogenic mycotoxin produced by several Fusarium species most frequently on maize and therefore can be found in food and animal feed. Since animal production performance is negatively affected by the presence of ZON, its detoxification in contaminated plant material or by-products of bioethanol production would be advantageous. Microbial biotransformation into nontoxic metabolites is one promising approach. In this study the main transformation product of ZON formed by the yeast Trichosporon mycotoxinivorans was identified and characterized by liquid chromatography-tandem mass spectrometry (LC-MS/MS) and LC-diode array detector (DAD) analysis. The metabolite, named ZOM-1, was purified, and its molecular formula, Zearalenone (ZON) is the main member of a growing family of biologically important "resorcylic acid lactones" (RALs), which have been found in nature. ZON is produced by several Fusarium species, which colonize maize, barley, oat, wheat, and sorghum and tend to develop ZON during prolonged cool, wet growing and harvest seasons (38). Maize is the most frequently contaminated crop plant, and therefore, ZON can be found frequently in animal feeding stuff. Occurrence, toxicity, and metabolism data of ZON were summarized by the European Food Safety Authority (EFSA) (5) and in recent reviews (12,38).The potent xenohormone ZON leads to hyperestrogenism symptoms and in extreme cases to infertility problems, especially in pigs (15). Ovarian changes in pigs have been noted with toxin levels as low as of 50 g/kg in the diet (1). Ruminants are more tolerant to ZON ingestion; however, hyperestrogenic syndrome, including restlessness, diarrhea, infertility, decreased milk yields, and abortion, have been well documented with cattle and sheep (4, 29).Because widespread ZON contamination in feed can occur in problematic years, efficient ways to detoxify are desirable. The transformation of mycotoxins to nontoxic metabolites by pure cultures of microorganisms or by cell-free enzyme preparations (3) is an attractive possibility. Microbial metabolization of ZON to alpha-ZOL and beta-ZOL cannot be regarded as detoxification, because both ZOL products are still estrogenic (14). Also, formation of ZON-glucosides and -diglucosides (8, 17) and ZON-sulfate (7) cannot be considered true detoxification but rather formation of masked mycotoxins, because the conjugates may be hydrolyzed during digestion (11,23), releasing ZON again (2).As the estrogenic activity of ZON and its derivates can be explained by its chemical structure, which resembles natural estrogens (20), it can be expected that cleavage of the lactone undecyl ring system of ZON results in permanent detoxification.El-Sharkawy and Abul-Hajj (9) were the first to report inactivation of ZON after opening of the lactone ring by Gliocladium roseum. This filamentous fungus was capable of metabolizing ZON in yields of 80 to 90%. Also Takahashi-Ando et al. (31) described the degradation reaction of ZON with Clonostachys rosea (synonym of G. roseum...

Biological control of mycotoxin-producing molds

“…For instance, the yeast Trichosporon mycotoxinivorans can detoxify the zearalenone (VEKIRU et al, 2010) and ochratoxin. The latter is detoxified by the cleavage of the phenylalanine moiety to form the derivate ochratoxinα , a virtually nontoxic metabolite compared to the parent compound (SCHATZMAYR et al, 2006).…”

Baeyer−Villiger Monooxygenases: More Than Just Green Chemistry

“…Although the Trichosporon genome sequence is not yet available, a potential BVMO was postulated to be responsible for the lactonization of a macrocyclic compound, zearalenone, a potent estrogenic mycotoxin produced by several Fusarium species that colonize agricultural crops such as maize. 309 Zearalenone is subsequently hydrolyzed by another unknown lactonase/esterase to a nonestrogenic metabolite. Which BVMO and corresponding ring-opening enzyme that will recognize these macrocyclic compounds are exciting prospects.…”

Scientific Opinion on the maintenance of the list of QPS biological agents intentionally added to food and feed (2011 update)

“…Some strains of this species were shown to detoxify ochratoxin A by cleavage of the phenylalanine moiety from the isocumarin derivate to ochratoxin α, a metabolite that has been described to be non-toxic or at least 500 times less toxic than ochratoxin A (Schatmayr et al, 2006). Trichosporon mycotoxinivorans is also able to metabolize Zearalenone in a metabolite (ZOM-1) that apparently shows no estrogenic activity anymore (Vekiru et al, 2010). Some recent results also support the potential of cell walls from Trichosporon mycotoxinivorans to bind enteropathogenic bacteria (E. coli spp and Salmonella spp) while having no adverse effect against beneficial or commensal bacteria (Ganner et al, 2010).…”