Novel Soil Bacterium Strain Desulfitobacterium sp. PGC-3-9 Detoxifies Trichothecene Mycotoxins in Wheat via De-Epoxidation under Aerobic and Anaerobic Conditions

Abstract

Trichothecenes are the most common mycotoxins contaminating small grain cereals worldwide. The C12,13 epoxide group in the trichothecenes was identified as a toxic group posing harm to humans, farm animals, and plants. Aerobic biological de-epoxidation is considered the ideal method of controlling these types of mycotoxins. In this study, we isolated a novel trichothecene mycotoxin-de-epoxidating bacterium, Desulfitobacterium sp. PGC-3-9, from a consortium obtained from the soil of a wheat field known for the occurrence of frequent Fusarium head blight epidemics under aerobic conditions. Along with MMYPF media, a combination of two antibiotics (sulfadiazine and trimethoprim) substantially increased the relative abundance of Desulfitobacterium species from 1.55% (aerobic) to 29.11% (aerobic) and 28.63% (anaerobic). A single colony purified strain, PGC-3-9, was isolated and a 16S rRNA sequencing analysis determined that it was Desulfitobacterium. The PGC-3-9 strain completely de-epoxidated HT-2, deoxynivalenol (DON), nivalenol and 15-acetyl deoxynivalenol, and efficiently eliminated DON in wheat grains under aerobic and anaerobic conditions. The strain PGC-3-9 exhibited high DON de-epoxidation activity at a wide range of pH (6–10) and temperature (15–50 °C) values under both conditions. This strain may be used for the development of detoxification agents in the agriculture and feed industries and the isolation of de-epoxidation enzymes.

The Ribosome-Binding Mode of Trichothecene Mycotoxins Rationalizes Their Structure—Activity Relationships

“…The 3- epi -DON, intermediate 3-keto-DON, and deepoxy-DON (DOM-1) all displayed reduced toxicity relative to DON [ 24 , 39 ]. Microbes responsible for de-epoxidation have been isolated from animal gut microflora and soil environments [ 4 , 44 , 45 , 48 ]. For example, under anaerobic conditions, bacterial consortia such as Eubacterium sp.…”

“…As discussed above, the present study explained why and how the key structural elements and substituents of trichothecenes impact their toxic actions through the binding interactions with the eukaryotic ribosome. Interestingly, these key toxicity-contributing structural elements have been targeted to develop detoxification strategies towards trichothecenes [43], such as the reductive de-epoxidation at C 12,13 epoxide ring [44][45][46], and the epimerization at C 3 -OH [10,11,47]. The epimerization and de-epoxidation are two microbial biotransformation pathways reported for DON detoxification with 3-epi-DON and deepoxy-DON (DOM-1) as the metabolized products.…”

Post-Harvest Prevention of Fusariotoxin Contamination of Agricultural Products by Irreversible Microbial Biotransformation: Current Status and Prospects

“…A novel bacterial strain able to de-epoxify DON was recently isolated from a wheat field soil and identified as Desulfitobacterium sp. PGC-3-9 [ 125 ]. After a 24 h incubation under anaerobic or aerobic conditions at 37 °C in the minimum medium containing yeast extract, pyruvate, and fumarate (MMYPE medium) supplemented with 500 μg/mL DON, the level of a DON degradation reached 99 and 95%, respectively.…”

Biodegradation of Deoxynivalenol by Nocardioides sp. ZHH-013: 3-keto-Deoxynivalenol and 3-epi-Deoxynivalenol as Intermediate Products

“…Massive screening techniques using diverse methods have been conducted to identify DON-degrading microbes, several of which have high DON conversion ability. Over the last three decades, DON-degrading strains have been identified among genera including Eubacterium (Fuchs et al, 2002), Eggerthella (Gao et al, 2018), Desulfitobacterium (He et al, 2020), Devosia (He et al, 2016;Wang et al, 2017Wang et al, , 2019, Sphingomonas (Ito et al, 2013;He et al, 2017), Nocardioides (Ikunaga et al, 2011), Marmoricola (Ito et al, 2012, Bacillus (Li et al, 2011), Pelagibacterium (Zhang et al, 2020), and Aspergillus (He et al, 2008;Jaqueline and Eliana, 2010;Jaqueline et al, 2011;Yang et al, 2017).…”

“…In the past, it was thought that the conversion of DON to DOM-1 could only be completed under anaerobic conditions; however, recent studies have shown that Desulfitobacterium sp. PGC-3-9 can transform DON under both anaerobic and aerobic conditions ( He et al, 2020 ). The genus Devosia has been widely studied, and several species in this genus can detoxify DON.…”