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Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications

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A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Mycotoxins".

Deadline for manuscript submissions: closed (30 June 2022) | Viewed by 39375

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Dr. Ting Zhou

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Guest Editor

Guelph Research and Development Center, Agriculture and Agri-Food Canada, Guelph, ON N1G 5C9, Canada
Interests: mycotoxin detoxification; microbial detoxification; trichothecene mycotoxins; deoxynivalenol; patulin
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Special Issue Information

Dear Colleagues,

Although great achievements have been made in controlling crop diseases caused by mycotoxigenic fungi, the fact is that mycotoxin contamination still cannot be avoided under the current agricultural practices. Moreover, the genetic alterations in some mycotoxigenic fungal populations have escalated the levels of mycotoxin contamination, and climate changes have already shown in certain geographic areas to possibly increase both the prevalence and severity of major mycotoxins. Globally, more than six hundred million metric tons of grains alone may be contaminated with various mycotoxins annually based on the FAO estimate of 25% mycotoxin contamination and the data of grain production worldwide. The contaminated grains and other food commodities present an ongoing safety burden in food supply chains, intensify food insecurity, add more challenges in environment protection, and cause substantial economic losses directly or indirectly. Therefore, postharvest strategies to mitigate mycotoxin contamination are truly essential and extremely critical. One such strategy is detoxification, which has shown very promising results in many studies and is attracting more and more researchers and industrial developers.

This Special Issue aims to provide an effective platform for 1) reporting discoveries of innovative mycotoxin detoxifications, including scientific concepts, novel technologies, and new organisms and agents, etc.; 2) illustrating understandings of detoxification mechanisms; and 3) demonstrating application possibilities and technologies. Both research (in particular) and review articles are welcome. We expect that the Special Issue will turn out to be a comprehensive and systematic compendium in the field of mycotoxin detoxification.

Dr. Ting Zhou
Guest Editor

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Keywords

mycotoxin
detoxification
transformation
degradation
metabolite
toxicology
pathway
modeling
microorganisms
enzyme
food safety
feed safety

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Published Papers (11 papers)

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Research

Jump to: Review

12 pages, 2870 KiB

Open AccessArticle

Possible Reaction Mechanisms Involved in Degradation of Patulin by Heat-Assisted Cysteine under Highly Acidic Conditions

by Enjie Diao, Kun Ma, Minghua Li, Hui Zhang, Peng Xie, Shiquan Qian, Huwei Song, Ruifeng Mao and Liming Zhang

Toxins 2022, 14(10), 695; https://doi.org/10.3390/toxins14100695 - 10 Oct 2022

Cited by 2 | Viewed by 2092

Abstract

Patulin (PAT) is one of mycotoxins that usually contaminates apple juice, and it is not easily detoxified by cysteine (CYS) at room temperature due to the highly acidic conditions based on the Michael addition reaction. However, it could be effectively degraded by a heating treatment at 120 °C for 30 min in the presence of cysteine. In our study, a total of eight degradation products (DP A–H) were characterized and identified via liquid chromatography quadrupole time-of-flight mass spectrometry (LC-Q-TOF-MS) in a negative ion mode, and their structures and formulas were proposed based on their accurate mass data. The fragmentation patterns of PAT and its degradation products were obtained from the MS/MS analysis. Meanwhile, the possible reaction mechanisms involved in the degradation of PAT were established and explained for the first time. According to the relation between the structure and toxicity of PAT, it could be deduced that the toxic effects of PAT degradation products were potentially much less than those of PAT-self. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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16 pages, 2729 KiB

Open AccessEditor’s ChoiceArticle

Modification of Deoxynivalenol by a Fungal Laccase Paired with Redox Mediator TEMPO

by Hina Shanakhat, Susan P. McCormick, Mark Busman, Joseph O. Rich and Matthew G. Bakker

Toxins 2022, 14(8), 548; https://doi.org/10.3390/toxins14080548 - 11 Aug 2022

Cited by 4 | Viewed by 2750

Abstract

Mycotoxins such as deoxynivalenol introduce a health risk to the food supply and are costly to manage or avoid. Technologies for reducing or eliminating the toxicity of deoxynivalenol could be useful in a variety of processes, such as in preserving the value as animal feed of byproducts of ethanol production. We characterized transformation products of deoxynivalenol that were formed by the combination of a fungal laccase paired with the chemical mediator 2,2,6,6-tetramethylpiperidine-N-oxyl (TEMPO), using chromatography, mass spectrometry, and nuclear magnetic resonance spectroscopy. Alcohol groups at the C3 and C15 positions of deoxynivalenol were oxidized to ketones, and the chemical mediator became covalently linked to the C4 position. Conditions experienced during gas chromatography led to the dissociation of TEMPO, forming 3,15-diketodeoxynivalenol. Understanding the range of possible modifications to deoxynivalenol and other trichothecenes is a necessary step toward effective remediation of contaminated grain. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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12 pages, 2186 KiB

Open AccessEditor’s ChoiceArticle

Application of Aspergillus niger Fumonisin Amine Oxidase (AnFAO) to Detoxify Fumonisin-Contaminated Maize

by Patrick G. Telmer, Megan J. Kelman, Justin B. Renaud, Mark W. Sumarah and Christopher P. Garnham

Toxins 2022, 14(8), 544; https://doi.org/10.3390/toxins14080544 - 9 Aug 2022

Cited by 6 | Viewed by 2424

Abstract

Fumonisin mycotoxins are a family of secondary metabolites produced by Fusarium verticillioides and related species, as well as some strains of Aspergillus niger. Fumonisin contamination of maize is a concern when grown under hot, dry conditions. When present above regulatory levels, there can be effects on animal health. New tools to reduce the toxicity of maize and maize products with high concentrations of fumonisin are needed. Recently, we reported an amine oxidase (AnFAO) from a fumonisin-producing Aspergillus niger strain capable of oxidatively deaminating intact fumonisins. In this study, AnFAO was used to reduce intact fumonisin concentrations in milled maize flour, whole kernel maize inoculated with fumonisin-producing Fusarium verticillioides, and dried distillers’ grains with solubles (DDGS). The data showed that milled maize flour incubated with 1 µM AnFAO for 1 h resulted in complete deamination of FB₁ and FB₂. A greater than 90% reduction in FB_1–3 concentrations was observed following a simple washing procedure of whole kernel maize in the presence of 1 µM AnFAO for 1 h. Similarly, a ≥86% reduction in FB_1–3 concentrations was observed in DDGS after 4 h incubation with 1 µM AnFAO. Finally, we engineered the methylotrophic yeast Pichia pastoris to produce functional AnFAO in both a secreted and intracellular form. These results support the further development and application of AnFAO as a promising tool to remediate fumonisin-contaminated maize and maize products. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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17 pages, 6560 KiB

Open AccessArticle

Deoxynivalenol Degradation by Various Microbial Communities and Its Impacts on Different Bacterial Flora

by Chenggang Cai, Miaomiao Zhao, Feng Yao, Ruiyu Zhu, Haiying Cai, Suqin Shao, Xiu-Zhen Li and Ting Zhou

Toxins 2022, 14(8), 537; https://doi.org/10.3390/toxins14080537 - 5 Aug 2022

Cited by 8 | Viewed by 2297

Abstract

Deoxynivalenol, a mycotoxin that may present in almost all cereal products, can cause huge economic losses in the agriculture industry and seriously endanger food safety and human health. Microbial detoxifications using microbial consortia may provide a safe and effective strategy for DON mitigation. In order to study the interactions involving DON degradation and change in microbial flora, four samples from different natural niches, including a chicken stable (expJ), a sheep stable (expY), a wheat field (expT) and a horse stable (expM) were collected and reacted with purified DON. After being co-incubated at 30 °C with 130 rpm shaking for 96 h, DON was reduced by 74.5%, 43.0%, 46.7%, and 86.0% by expJ, expY, expT, and expM, respectively. After DON (0.8 mL of 100 μg/mL) was co-cultivated with 0.2 mL of the supernatant of each sample (i.e., suspensions of microbial communities) at 30 °C for 96 h, DON was reduced by 98.9%, 99.8%, 79.5%, and 78.9% in expJ, expY, expT, and expM, respectively, and was completely degraded after 8 days by all samples except of expM. DON was confirmed being transformed into de-epoxy DON (DOM-1) by the microbial community of expM. The bacterial flora of the samples was compared through 16S rDNA flux sequencing pre- and post the addition of DON. The results indicated that the diversities of bacterial flora were affected by DON. After DON treatment, the most abundant bacteria belong to Galbibacter (16.1%) and Pedobacter (8.2%) in expJ; Flavobacterium (5.9%) and Pedobacter (5.5%) in expY; f_Microscillaceae (13.5%), B1-7BS (13.4%), and RB41 (10.5%) in expT; and Acinetobacter (24.1%), Massilia (8.8%), and Arthrobacter (7.6%) in expM. This first study on the interactions between DON and natural microbial flora provides useful information and a methodology for further development of microbial consortia for mycotoxin detoxifications. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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15 pages, 3016 KiB

Open AccessArticle

Characterization of Two Dehydrogenases from Gluconobacter oxydans Involved in the Transformation of Patulin to Ascladiol

by Edicon T. S. Chan, Yan Zhu, Xiu-Zhen Li, Ting Zhou and Stephen Y. K. Seah

Toxins 2022, 14(7), 423; https://doi.org/10.3390/toxins14070423 - 21 Jun 2022

Cited by 10 | Viewed by 2463

Abstract

Patulin is a mycotoxin that primarily contaminate apples and apple products. Whole cell or cell-free extracts of Gluconobacter oxydans ATCC 621 were able to transform patulin to E-ascladiol. Proteins from cell-free extracts were separated by anion exchange chromatography and fractions with patulin transformation activity were subjected to peptide mass fingerprinting, enabling the identification of two NADPH dependent short chain dehydrogenases, GOX0525 and GOX1899, with the requisite activity. The genes encoding these enzymes were expressed in E. coli and purified. Kinetic parameters for patulin reduction, as well as pH profiles and thermostability were established to provide further insight on the potential application of these enzymes for patulin detoxification. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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10 pages, 507 KiB

Open AccessCommunication

Decrease in Aflatoxin M₁ Concentration in Milk during Cholesterol Removal by Application of β-Cyclodextrin

by Peter Šimko and Lukáš Kolarič

Toxins 2022, 14(6), 379; https://doi.org/10.3390/toxins14060379 - 29 May 2022

Cited by 5 | Viewed by 2245

Abstract

Approximately one-third of humankind is chronically exposed to the carcinogenic aflatoxin M₁ contained in milk. As β-cyclodextrin is frequently used in the food industry, its effect on aflatoxin M₁ concentration was investigated during cholesterol removal from milk due to the similarity among the physicochemical properties of aflatoxin M₁ and cholesterol. Moreover, the elimination of cholesterol using β-cyclodextrin has been successfully applied in many studies without any substantial effect on the quality of the treated milk. Therefore, milk samples were spiked with aflatoxin M₁ within the range from 0.20 to 2.00 µg/kg, and cholesterol removal was carried out by 2.0% (w/w) β-cyclodextrin addition, as this concentration is enough for the sufficient removal of cholesterol. It was found that the mean cholesterol concentration decreased by 92.3%, while the aflatoxin M₁ concentration decreased to 0.53 ± 0.04 µg/kg, i.e., by 39.1% after treatment (n = 2). This mitigation procedure itself is easy and inexpensive and thus is fully applicable with a high potential for complete decontamination of aflatoxin M₁ milk. This method will therefore considerably improve the food safety issues associated with aflatoxin M₁ presence in milk and dairy products. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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14 pages, 1332 KiB

Open AccessArticle

Spent Coffee Grounds Valorization as Bioactive Phenolic Source Acquired Antifungal, Anti-Mycotoxigenic, and Anti-Cytotoxic Activities

by Ahmed Noah Badr, Marwa M. El-Attar, Hatem S. Ali, Manal F. Elkhadragy, Hany M. Yehia and Amr Farouk

Toxins 2022, 14(2), 109; https://doi.org/10.3390/toxins14020109 - 31 Jan 2022

Cited by 16 | Viewed by 4309

Abstract

Spent coffee grounds (SCGs), which constitute 75% of original coffee beans, represent an integral part of sustainability. Contamination by toxigenic fungi and their mycotoxins is a hazard that threatens food production. This investigation aimed to examine SCGs extract as antimycotic and anti-ochratoxigenic material. The SCGs were extracted in an eco-friendly way using isopropanol. Bioactive molecules of the extract were determined using the UPLC apparatus. The cytotoxicity on liver cancer cells (Hep-G2) showed moderate activity with selectivity compared with human healthy oral epithelial (OEC) cell lines but still lower than the positive control (Cisplatin). The antibacterial properties were examined against pathogenic strains, and the antifungal was examined against toxigenic fungi using two diffusion assays. Extract potency was investigated by two simulated models, a liquid medium and a food model. The results of the extract showed 15 phenolic acids and 8 flavonoids. Rosmarinic and syringic acids were the most abundant phenolic acids, while apigenin-7-glucoside, naringin, epicatechin, and catechin were the predominant flavonoids in the SCGs extract. The results reflected the degradation efficiency of the extract against the growth of Aspergillus strains. The SCGs recorded detoxification in liquid media for aflatoxins (AFs) and ochratoxin A (OCA). The incubation time of the extract within dough spiked with OCA was affected up to 2 h, where cooking was not affected. Therefore, SCGs in food products could be applied to reduce the mycotoxin contamination of raw materials to the acceptable regulated limits. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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21 pages, 2749 KiB

Open AccessEditor’s ChoiceArticle

A Novel Microbial Zearalenone Transformation through Phosphorylation

by Yan Zhu, Pascal Drouin, Dion Lepp, Xiu-Zhen Li, Honghui Zhu, Mathieu Castex and Ting Zhou

Toxins 2021, 13(5), 294; https://doi.org/10.3390/toxins13050294 - 21 Apr 2021

Cited by 15 | Viewed by 2672

Abstract

Zearalenone (ZEA) is a mycotoxin widely occurring in many agricultural commodities. In this study, a purified bacterial isolate, Bacillus sp. S62-W, obtained from one of 104 corn silage samples from various silos located in the United States, exhibited activity to transform the mycotoxin ZEA. A novel microbial transformation product, ZEA-14-phosphate, was detected, purified, and identified by HPLC, LC-MS, and NMR analyses. The isolate has been identified as belonging to the genus Bacillus according to phylogenetic analysis of the 16S rRNA gene and whole genome alignments. The isolate showed high efficacy in transforming ZEA to ZEA-14-phosphate (100% transformation within 24 h) and possessed advantages of acid tolerance (work at pH = 4.0), working under a broad range of temperatures (22–42 °C), and a capability of transforming ZEA at high concentrations (up to 200 µg/mL). In addition, 23 Bacillus strains of various species were tested for their ZEA phosphorylation activity. Thirteen of the Bacillus strains showed phosphorylation functionality at an efficacy of between 20.3% and 99.4% after 24 h incubation, suggesting the metabolism pathway is widely conserved in Bacillus spp. This study established a new transformation system for potential application of controlling ZEA although the metabolism and toxicity of ZEA-14-phosphate requires further investigation. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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Review

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22 pages, 446 KiB

Open AccessReview

Crosstalk between Mycotoxins and Intestinal Microbiota and the Alleviation Approach via Microorganisms

by Daiyang Xia, Qianyuan Mo, Lin Yang and Wence Wang

Toxins 2022, 14(12), 859; https://doi.org/10.3390/toxins14120859 - 6 Dec 2022

Cited by 8 | Viewed by 2741

Abstract

Mycotoxins are secondary metabolites produced by fungus. Due to their widespread distribution, difficulty in removal, and complicated subsequent harmful by-products, mycotoxins pose a threat to the health of humans and animals worldwide. Increasing studies in recent years have highlighted the impact of mycotoxins on the gut microbiota. Numerous researchers have sought to illustrate novel toxicological mechanisms of mycotoxins by examining alterations in the gut microbiota caused by mycotoxins. However, few efficient techniques have been found to ameliorate the toxicity of mycotoxins via microbial pathways in terms of animal husbandry, human health management, and the prognosis of mycotoxin poisoning. This review seeks to examine the crosstalk between five typical mycotoxins and gut microbes, summarize the functions of mycotoxins-induced alterations in gut microbes in toxicological processes and investigate the application prospects of microbes in mycotoxins prevention and therapy from a variety of perspectives. The work is intended to provide support for future research on the interaction between mycotoxins and gut microbes, and to advance the technology for preventing and controlling mycotoxins. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

11 pages, 309 KiB

Open AccessReview

Mycotoxin Metabolism by Edible Insects

by Natasha Marie Evans and Suqin Shao

Toxins 2022, 14(3), 217; https://doi.org/10.3390/toxins14030217 - 17 Mar 2022

Cited by 18 | Viewed by 4222

Abstract

Mycotoxins are a group of toxic secondary metabolites produced in the food chain by fungi through the infection of crops both before and after harvest. Mycotoxins are one of the most important food safety concerns due to their severe poisonous and carcinogenic effects on humans and animals upon ingestion. In the last decade, insects have received wide attention as a highly nutritious, efficient and sustainable source of animal-derived protein and caloric energy for feed and food purposes. Many insects have been used to convert food waste into animal feed. As food waste might contain mycotoxins, research has been conducted on the metabolism and detoxification of mycotoxins by edible insects. The mycotoxins that have been studied include aflatoxins, fumonisins, zearalenone (ZEN), vomitoxin or deoxynivalenol (DON), and ochratoxins (OTAs). Aflatoxin metabolism is proved through the production of hydroxylated metabolites by NADPH-dependent reductases and hydroxylases by different insects. ZEN can be metabolized into α- and β-zearalenol. Three DON metabolites, 3-, 15-acetyl-DON, and DON-3-glucoside, have been identified in the insect DON metabolites. Unfortunately, the resulting metabolites, involved enzymes, and detoxification mechanisms of OTAs and fumonisins within insects have yet to be identified. Previous studies have been focused on the insect tolerance to mycotoxins and the produced metabolites; further research needs to be conducted to understand the exact enzymes and pathways that are involved. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

19 pages, 1391 KiB

Open AccessReview

Deoxynivalenol: Toxicology, Degradation by Bacteria, and Phylogenetic Analysis

by Anne Caroline Schoch Marques Pinto, Camilla Reginatto De Pierri, Alberto Gonçalves Evangelista, Ana Silvia de Lara Pires Batista Gomes and Fernando Bittencourt Luciano

Toxins 2022, 14(2), 90; https://doi.org/10.3390/toxins14020090 - 25 Jan 2022

Cited by 42 | Viewed by 9562

Abstract

Deoxynivalenol (DON) is a toxic secondary metabolite produced by fungi that contaminates many crops, mainly wheat, maize, and barley. It affects animal health, causing intestinal barrier impairment and immunostimulatory effect in low doses and emesis, reduction in feed conversion rate, and immunosuppression in high doses. As it is very hard to completely avoid DON’s production in the field, mitigatory methods have been developed. Biodegradation has become a promising method as new microorganisms are studied and new enzymatic routes are described. Understanding the common root of bacteria with DON degradation capability and the relationship with their place of isolation may bring insights for more effective ways to find DON-degrading microorganisms. The purpose of this review is to bring an overview of the occurrence, regulation, metabolism, and toxicology of DON as addressed in recent publications focusing on animal production, as well as to explore the enzymatic routes described for DON’s degradation by microorganisms and the phylogenetic relationship among them. Full article

(This article belongs to the Special Issue Innovative Mycotoxin Detoxification: Discoveries, Mechanisms and Applications)

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