Elimination of Fusarium mycotoxin deoxynivalenol (DON) via microbial and enzymatic strategies: Current status and future perspectives

Highlights

• DON is a food contaminant with high contamination level and frequency.

• Microbial antagonists exhibit potentials on F. graminearum control.

• Microbes and enzymes are desirable to dispose DON contaminated cereal grains.

• Application of computational strategy towards DON detoxification enzyme screen is highlighted.

Abstract

Background

Deoxynivalenol (DON) is an important Fusarium mycotoxin commonly detected in foods and feeds, which has drawn global attention because of its high contamination level and frequency. Applying microbial antagonists to inhibit fungal DON synthesis and detoxification of DON into low toxic metabolites are biological approaches to eliminate DON via an environment friendly manner. Therefore, it is essential to review the latest research work on Fusarium biocontrol and DON bio-detoxification.

Scope and approach

We summarized recent reported microbial and enzymatic methods for DON elimination. The microbial antagonists on Fusarium control and DON detoxification microbes/enzymes, as well as their control mechanisms were systematically reviewed. In addition, we highlighted the potentials of biological methods for DON elimination and discussed novel approaches for DON detoxification enzymes discovery guided by computational strategy.

Key finding and conclusion

Successful cases of controlling DON producing fungi by microbial antagonists and detoxifying DON by microbes and enzymes were reported in the past several years, which would provide new opportunities to eliminate mycotoxin DON and promote large-scale usage of bio control-based methods. On the other hand, registration and technical difficulties in practical application should be comprehensively considered and solved in future. Additionally, we proposed a conceptual framework of combining the computational tools with multi omics approaches for DON detoxification enzymes discovery, which could provide a new foundation for future mycotoxin detoxification research.

Introduction

Mycotoxins are toxic secondary metabolites produced by fungi on plant-origin products in field or during storage (Yang et al., 2020). The common mycotoxin producers are the fungi of Fusarium, Alternaria, Aspergillus and Penicillium. Mycotoxins are mutagenic, genotoxic, carcinogenic or teratogenic (Claeys et al., 2020) and foods are easily contaminated with mycotoxins, which poses great hazards to health of humans (Yang et al., 2020). Trichothecene mycotoxins are a class of sesquiterpenoid metabolites (Chen et al., 2019) which can be classed into four different types (A, B, C, and D). Deoxynivalenol (DON, also known as vomitoxin) belonging to type B trichothecene, is the mainly detected mycotoxin in cereal related foods and feeds (Mishra et al., 2020; Mousavi Khaneghah et al., 2020). Though DON's toxicity is less than another trichothecene T-2 toxin, it is the most predominant and agriculturally important mycotoxin (Wu et al., 2017). A recent study reported that all the collected wheat samples (579 samples) and 99.8% of maize samples (606 samples) were detected positive for DON contamination (Yan et al., 2020). Moreover, Mishra et al. reviewed the occurrence of DON in foods, finding that DON concentration in most of the positive tested samples exceeded the permissive limit (Mishra et al., 2020).

F. graminearum complex are well known DON producing phytopathogens which could cause serious crop diseases, such as Fusarium head blight (FHB), maize ear rot and stalk rot. Crop diseases caused by F. graminearum significantly reduce the yield of agricultural products, meanwhile the contaminated cereal grains have severe impacts on foods and feed production (Leite et al., 2021). DON is chemically stable and heat resistant, thus it is difficult to eliminate DON contamination during food/feed process period (Guo et al., 2020). Both cereal based products (Bread, pizza, or beer) and animal derived food (Meat, milk, or eggs) could be easily contaminated by DON (Mishra et al., 2020; Mousavi Khaneghah et al., 2020; Wang, Liao, et al., 2019). Mycotoxin DON in food and feed chains seriously threaten the health of human and domesticated animals through dietary exposure (Fig. 1). The toxicities of DON consist of ribosomal stress, oxidative stress, endoplasmic reticulum stress, immunotoxicity, hepatotoxicity, gastrointestinal toxicity and impair normal physiological functions (Lu et al., 2021), and typical toxic symptoms of DON are nausea, emesis, abdominal pain, diarrhea, anorexia, fever, headache and dizziness (Wu et al., 2017). For animals, DON usually causes feed refusal, vomiting, weight loss and organ injuries, which lead to negative effects on livestock and poultry production (Awad et al., 2010).

In consideration of DON's prevalence in cereal grains and its toxic effects on human and animal (Deng et al., 2021), control methods should be developed to eliminate DON pollution in foods and feeds. DON contamination occurs from preharvest period to post food/feed storage and processing period. The available DON de-contamination approaches are prevention of fungal growth, inhibition of mycotoxin production, and detoxify mycotoxin DON at pre-harvest or post-harvest periods. Physical, chemical, and biological methods with different degradation mechanisms have been explored and applied. For example, physical removal strategy includes adsorption, cold plasma, irradiation, light treatment, ultrasound treatment, and thermal treatment (Afsah-Hejri et al., 2020). Chemical control methods include treatment with ozone, chlorine dioxide, alkaline, and other strong chemical agents (Feizollahi & Roopesh, 2021). Traditional physical and chemical treatments have deficiencies in application, like incomplete degradation, nutrition loss after physical treatment, and causing secondary pollution when using chemical reagents. It is urged to seek alternative methods with less negative influences on environment and human's health. Biological control is regarded as a promising strategy for pathogens and mycotoxin control, which has gained great interests in recent years (Nesic et al., 2021). Biological based DON elimination methods include: 1. application of antagonistic microbes to inhibit DON producing fungi, 2. detoxifying DON to get low or non-toxic metabolites by beneficial microbes and detoxification enzymes. 3. increasing the crop resistance to DON-producing pathogens and the ability to detoxify DON via genetic improvement. During pre-harvest stage, fungicide can be replaced by antagonistic microbes. While probiotics/enzymes with DON detoxification ability could be used as potential additives to eliminate DON, which is more environment friendly than traditional methods (Karlovsky, 2011). Recently, significant processes have been achieved on DON producing Fusarium biocontrol and DON bio-detoxification. In this review, we specially focused on the advances of DON elimination by microbial and enzymatic methods and highlight their potentials on DON contamination control. Moreover, the detoxification mechanisms by microbes or enzymes, current challenges, and further trend on detoxification enzymes discovering were well discussed, which would provide a reference for integrated mycotoxin management.