Aphids transform and detoxify the mycotoxin deoxynivalenol via a type II biotransformation mechanism yet unknown in animals.

N De Zutter,G Haesaert,C Van Poucke,K Audenaert,N Arroyo-Manzanares,M De Boevre,G Smagghe,S De Saeger

doi:10.1038/srep38640

Abstract

Biotransformation of mycotoxins in animals comprises phase I and phase II metabolisation reactions. For the trichothecene deoxynivalenol (DON), several phase II biotransformation reactions have been described resulting in DON-glutathiones, DON-glucuronides and DON-sulfates made by glutathione-S-transferases, uridine-diphosphoglucuronyl transferases and sulfotransferases, respectively. These metabolites can be easily excreted and are less toxic than their free compounds. Here, we demonstrate for the first time in the animal kingdom the conversion of DON to DON-3-glucoside (DON-3G) via a model system with plant pathogenic aphids. This phase II biotransformation mechanism has only been reported in plants. As the DON-3G metabolite was less toxic for aphids than DON, this conversion is considered a detoxification reaction. Remarkably, English grain aphids (Sitobion avenae) which co-occur with the DON producer Fusarium graminearum on wheat during the development of fusarium symptoms, tolerate DON much better and convert DON to DON-3G more efficiently than pea aphids (Acyrthosiphon pisum), the latter being known to feed on legumes which are no host for F. graminearum. Using a non-targeted high resolution mass spectrometric approach, we detected DON-diglucosides in aphids probably as a result of sequential glucosylation reactions. Data are discussed in the light of an eventual co-evolutionary adaptation of S. avenae to DON.

Highlights

In the yeast Saccharomyces cerevisiae, a spontaneous mutant tolerant to the trichothecene, trichodermin was isolated[7]
At the level of a spikelet, these concentrations can mount to 50 mg kg−1.The survival of S. avenae aphids was not affected by DON up to concentrations of 3 mg l−1 compared to the control when analyzed using a Kruskal-Wallis test (p = 0.337), while survival of A. pisum aphids was significantly reduced
The trichothecene DON is a sesquiterpenoid mycotoxin produced by several Fusarium species and is toxic for most eukaryotic cells

Summary

Introduction

In the yeast Saccharomyces cerevisiae, a spontaneous mutant tolerant to the trichothecene, trichodermin was isolated[7]. The gene responsible for the trichodermin tolerance was called tcm[18] and was suggested to encode for the ribosomal protein L3 (RPL3)[10], which is the target of trichothecenes. Insects often live in close proximity of trichothecene-producing fungi and the toxicity has been reported in a few studies. New insights on detoxification might come from animals that live in close contact with DON-producing fungi. A well-known example is the English grain aphid (Sitobion avenae) which migrates from the leaves to the developing ear upon its appearance. From that moment, it resides on the same niche as the Fusarium fungus and comes in close contact with its toxic secondary metabolites. We used a non-targeted high resolution mass spectrometric approach to get an in depth insight into eventual new derived metabolites of DON in animals

Methods

Results

Conclusion