Research Advance on Biotransformation of Deoxynivalenol by Microbes and Biological Enzymes

  • ZHANG Jing ,
  • ZHANG Qiongqiong ,
  • JI Cheng ,
  • ZHAO Lihong
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  • State Key Laboratory of Animal Nutrition, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China

Received date: 2020-08-18

  Online published: 2020-10-22

Abstract

Deoxynivalenol (DON), a toxic secondary metabolite produced by Fusarium species that mainly infests cereals such as wheat and corn, seriously threatens human and livestock health. Biotransformation of DON by microbes or biological enzymes has high catalytic efficiency, strong specificity and no pollution to the environment, and has great effect on eliminating DON of substrate. This review systematically outlined the research in the biotransformation of DON, including the action type, microbes, biological enzymes, product toxicity, and the application in animal production, in order to provide theoretical basis for the biodegradation of DON in feed and food.

Cite this article

ZHANG Jing , ZHANG Qiongqiong , JI Cheng , ZHAO Lihong . Research Advance on Biotransformation of Deoxynivalenol by Microbes and Biological Enzymes[J]. Chinese Journal of Animal Nutrition, 2020 , 32(10) : 4807 -4820 . DOI: 10.3969/j.issn.1006-267x.2020.10.032

References

[1] HUSSEIN H S,BRASEL J M.Toxicity,metabolism,and impact of mycotoxins on humans and animals[J].Toxicology,2001,167(2):101-134.  
[2] MARESCA M,YAHI N,YOUNÈS-SAKR L,et al.Both direct and indirect effects account for the pro-inflammatory activity of enteropathogenic mycotoxins on the human intestinal epithelium:stimulation of interleukin-8 secretion,potentiation of interleukin-1β effect and increase in the transepithelial passage of commensal bacteria[J].Toxicology and Applied Pharmacology,2008,228(1):84-92.  
[3] PESTKA J J.Deoxynivalenol:mechanisms of action,human exposure,and toxicological relevance[J].Archives of Toxicology,2010,84(9):663-679.  
[4] BAI G H,SHANER G.Management and resistance in wheat and barley to Fusarium head blight[J].Annual Review of Phytopathology,2004,42:135-161.
[5] 雷元培,周建川,王利通,等.2018年中国饲料原料及配合饲料中霉菌毒素污染调查报告[J].饲料工业,2020,41(10):60-64.
[6] MISHRA S,SRIVASTAVA S,DEWANGAN J,et al.Global occurrence of deoxynivalenol in food commodities and exposure risk assessment in humans in the last decade:a survey[J].Critical Reviews in Food Science and Nutrition,2020,60(8):1346-1374.  
[7] 中华人民共和国国家质量监督检验检疫总局,中国国家标准化管理委员会.GB13078-2017饲料卫生标准[S].北京:中国标准出版社,2017.
[8] 国家卫生和计划生育委员会,国家食品药品监督管理总局.GB2761-2017食品安全国家标准食品中真菌毒素限量[S].北京:中国标准出版社,2017.
[9] USFDA.Guidance for industry and FDA:Advisory levels for deoxynivalenol (DON) in finished wheat products for human consumption and grains and grain by-products used for animal feed[S].Rockville,MD:USFDA,2010.
[10] European Communities.Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting maximum levels for certain contaminants in foodstuffs[S].[s.l.]:[s.n.],2006.
[11] LEE J Y,LIM W,PARK S,et al.Deoxynivalenol induces apoptosis and disrupts cellular homeostasis through MAPK signaling pathways in bovine mammary epithelial cells[J].Environmental Pollution,2019,252:879-887.
[12] WANG X C,FAN M X,CHU X Y,et al.Deoxynivalenol induces toxicity and apoptosis in piglet hippocampal nerve cells via the MAPK signaling pathway[J].Toxicon,2018,155:1-8.
[13] ZHANG H,DENG X W,ZHOU C,et al.Deoxynivalenol induces inflammation in IPEC-J2 cells by activating P38 MAPK and Erk1/2[J].Toxins,2020,12(3):180.
[14] LIU D D,WANG Q,HE W M,et al.Two-way immune effects of deoxynivalenol in weaned piglets and porcine alveolar macrophages:due mainly to its exposure dosage[J].Chemosphere,2020,249:126464.
[15] LI X G,ZHU M,CHEN M X,et al.Acute exposure to deoxynivalenol inhibits porcine enteroid activity via suppression of the Wnt/β-catenin pathway[J].Toxicology Letters,2019,305:19-31.
[16] GRAZIANI F,PINTON P,OLLEIK H,et al.Deoxynivalenol inhibits the expression of trefoil factors (TFF) by intestinal human and porcine goblet cells[J].Archives of Toxicology,2019,93(4):1039-1049.  
[17] WANG X C,CHEN X F,CAO L,et al.Mechanism of deoxynivalenol-induced neurotoxicity in weaned piglets is linked to lipid peroxidation,dampened neurotransmitter levels,and interference with calcium signaling[J].Ecotoxicology and Environmental Safety,2020,194:110382.
[18] SALAHIPOUR M H,HASANZADEH S,MALEKINEJAD H,et al.Deoxynivalenol reduces quality parameters and increases DNA damage in mice spermatozoa[J].Andrologia,2019,51(5):e13238.
[19] WACHÉ Y J,HBABI-HADDIOUI L,GUZYLACK-PIRIOU L,et al.The mycotoxin deoxynivalenol inhibits the cell surface expression of activation markers in human macrophages[J].Toxicology,2009,262(3):239-244.  
[20] YOUNG L G,MCGIRR L,VALLI V E,et al.Vomitoxin in corn fed to young pigs[J].Journal of Animal Science,1983,57(3):655-664.  
[21] SAVI G D,CARDOSO W A,FURTADO B G,et al.Antifungal activities against toxigenic Fusarium specie and deoxynivalenol adsorption capacity of ion-exchanged zeolites[J].Journal of Environmental Science and Health,2018,53(3):184-190.  
[22] LI M M,GUAN E Q,BIAN K.Detoxification of deoxynivalenol by 60Co γ-ray irradiation and toxicity analyses of radiolysis products[J].Journal of AOAC International,2019,102(6):1749-1755.  
[23] BAI X J,SUN C P,LIU D,et al.Photocatalytic degradation of deoxynivalenol using graphene/ZnO hybrids in aqueous suspension[J].Applied Catalysis B-Environmental,2017,204:11-20.
[24] WANG L,WANG Y,SHAO H L,et al.In vivo toxicity assessment of deoxynivalenol-contaminated wheat after ozone degradation[J].Food Additives & Contaminants:Part A,2017,34(1):103-112.  
[25] XU Y,JI J,WU H,et al.Untargeted GC-TOFMS-based cellular metabolism analysis to evaluate ozone degradation effect of deoxynivalenol[J].Toxicon,2019,168:49-57.
[26] REMPE I,KERSTEN S,VALENTA H,et al.Hydrothermal treatment of naturally contaminated maize in the presence of sodium metabisulfite,methylamine and calcium hydroxide;effects on the concentration of zearalenone and deoxynivalenol[J].Mycotoxin Research,2013,29(3):169-175.  
[27] HE J W,ZHOU T,YOUNG J C,et al.Chemical and biological transformations for detoxification of trichothecene mycotoxins in human and animal food chains:a review[J].Trends in Food Science & Technology,2010,21(2):67-76.  
[28] ERIKSEN G S,PETTERSSON H,LUNDH T.Comparative cytotoxicity of deoxynivalenol,nivalenol,their acetylated derivatives and de-epoxy metabolites[J].Food and Chemical Toxicology,2004,42(4):619-624.  
[29] DESJARDINS A E,HOHN T M,MCCORMICK S P.Trichothecene biosynthesis in Fusarium species:chemistry,genetics,and significance[J].Microbiological Reviews,1993,57(3):595-604.  
[30] IKUNAGA Y,SATO I,GROND S,et al.Nocardioides sp. strain WSN05-2,isolated from a wheat field,degrades deoxynivalenol,producing the novel intermediate 3-epi-deoxynivalenol[J].Applied Microbiology and Biotechnology,2011,89(2):419-427.  
[31] SHIMA J,TAKASE S,TAKAHASHI Y,et al.Novel detoxification of the trichothecene mycotoxin deoxynivalenol by a soil bacterium isolated by enrichment culture[J].Applied and Environmental Microbiology,1997,63(10):3825-3830.  
[32] SATO I,ITO M,ISHIZAKA M,et al.Thirteen novel deoxynivalenol-degrading bacteria are classified within two genera with distinct degradation mechanisms[J].FEMS Microbiology Letters,2012,327(2):110-117.  
[33] ROTTER B A.Invited review:toxicology of deoxynivalenol (vomitoxin)[J].Journal of Toxicology and Environmental Health,1996,48(1):1-34.  
[34] DÄNICKE S,VALENTA H,DÖLL S.On the toxicokinetics and the metabolism of deoxynivalenol (don) in the pig[J].Archives of Animal Nutrition,2004,58(2):169-180.  
[35] SEELING K,DÄNICKE S,VALENTA H,et al.Effects of Fusarium toxin-contaminated wheat and feed intake level on the biotransformation and carry-over of deoxynivalenol in dairy cows[J].Food Additives & Contaminants,2006,23(10):1008-1020.  
[36] PRELUSKY D B,VEIRA D M,TRENHOLM H L,et al.Metabolic fate and elimination in milk,urine and bile of deoxynivalenol following administration to lactating sheep[J].Journal of Environmental Science and Health (Part B),1987,22(2):125-148.  
[37] HE P,YOUNG L G,FORSBERG C.Microbially detoxified vomitoxin-contaminated corn for young pigs[J].Journal of Animal Science,1993,71(4):963-967.  
[38] BINDER J,HORVATH E M,SCHATZMAYR G,et al.Screening for deoxynivalenol-detoxifying anaerobic rumen microorganisms[J].Cereal Research Communications,1997,25(31):343-346.
[39] FUCHS E,BINDER E M,HEIDLER D,et al.Structural characterization of metabolites after the microbial degradation of type A trichothecenes by the bacterial strain BBSH 797[J].Food Additives & Contaminants,2002,19(4):379-386.  
[40] GAO X J,MU P Q,WEN J K,et al.Detoxification of trichothecene mycotoxins by a novel bacterium,Eggerthella sp. DⅡ-9[J].Food and Chemical Toxicology,2018,112:310-319.
[41] LI X Z,ZHU C,DE LANGE C F M,et al.Efficacy of detoxification of deoxynivalenol-contaminated corn by Bacillus sp. LS100 in reducing the adverse effects of the mycotoxin on swine growth performance[J].Food Additives & Contaminants,2011,28(7):894-901.  
[42] LI F C,WANG J Q,HUANG L B,et al.Effects of adding Clostridium sp. WJ06 on intestinal morphology and microbial diversity of growing pigs fed with natural deoxynivalenol contaminated wheat[J].Toxins,2017,9(12):383.
[43] GAO X J,MU P Q,ZHU X H,et al.Dual function of a novel bacterium,Slackia sp. D-G6:detoxifying deoxynivalenol and producing the natural estrogen analogue,equol[J].Toxins,2020,12(2):85.
[44] HE W J,YUAN Q S,ZHANG Y B,et al.Aerobic de-epoxydation of trichothecene mycotoxins by a soil bacterial consortium isolated using in situ soil enrichment[J].Toxins,2016,8(10):277.
[45] HE W J,SHI M M,YANG P,et al.Novel soil bacterium strain Desulfitobacterium sp. PGC-3-9 detoxifies trichothecene mycotoxins in wheat via de-epoxidation under aerobic and anaerobic conditions[J].Toxins,2020,12(6):363.
[46] MAYER E,NOVAK B,SPRINGLER A,et al.Effects of deoxynivalenol (DON) and its microbial biotransformation product deepoxy-deoxynivalenol (DOM-1) on a trout,pig,mouse,and human cell line[J].Mycotoxin Research,2017,33(4):297-308.  
[47] BRACARENSE A P F L,PIERRON A,PINTON P,et al.Reduced toxicity of 3-epi-deoxynivalenol and de-epoxy-deoxynivalenol through deoxynivalenol bacterial biotransformation:in vivo analysis in piglets[J].Food and Chemical Toxicology,2020,140:111241.
[48] WANG G,WANG Y X,JI F,et al.Biodegradation of deoxynivalenol and its derivatives by Devosia insulae A16[J].Food Chemistry,2019,276:436-442.
[49] 李笑樱.降解呕吐毒素德沃斯氏菌的饲用安全性和有效性评价[D].博士学位论文.北京:中国农业大学,2015:39-44.
[50] ZHANG J,QIN X J,GUO Y P,et al.Enzymatic degradation of deoxynivalenol by a novel bacterium,Pelagibacterium halotolerans ANSP101[J].Food and Chemical Toxicology,2020,140:111276.
[51] HE W J,ZHANG L M,Yi S Y,et al.An aldo-keto reductase is responsible for Fusarium toxin-degrading activity in a soil Sphingomonas strain[J].Scientific Reports,2017,7:9549.
[52] CARERE J,HASSAN Y I,LEPP D,et al.The enzymatic detoxification of the mycotoxin deoxynivalenol:identification of DepA from the DON epimerization pathway[J].Microbial Biotechnology,2018,11(6):1106-1111.  
[53] HE W J,SHI M M,YANG P,et al.A quinone-dependent dehydrogenase and two NADPH-dependent aldo/keto reductases detoxify deoxynivalenol in wheat via epimerization in a Devosia strain[J].Food Chemistry,2020,321:126703.
[54] HE J W,BONDY G S,ZHOU T,et al.Toxicology of 3-epi-deoxynivalenol,a deoxynivalenol-transformation product by Devosia mutans 17-2-E-8[J].Food and Chemical Toxicology,2015,84:250-259.
[55] WANG Y,ZHANG H H,ZHAO C,et al.Isolation and characterization of a novel deoxynivalenol-transforming strain Paradevosia shaoguanensis DDB001 from wheat field soil[J].Letters in Applied Microbiology,2017,65(5):414-422.  
[56] QU R,JIANG C M,WU W Q,et al.Conversion of DON to 3-epi-DON in vitro and toxicity reduction of DON in vivo by Lactobacillus rhamnosus[J].Food & Function,2019,10(5):2785-2796.  
[57] HASSAN Y I,HE J W,PERILLA N,et al.The enzymatic epimerization of deoxynivalenol by Devosia mutans proceeds through the formation of 3-keto-DON intermediate[J].Scientific Reports,2017,7:6929.
[58] CARERE J,HASSAN Y I,LEPP D,et al.The identification of DepB:an enzyme responsible for the final detoxification step in the deoxynivalenol epimerization pathway in Devosia mutans 17-2-E-8[J].Frontiers in Microbiology,2018,9:1573.
[59] PIERRON A,MIMOUN S,MURATE L S,et al.Microbial biotransformation of DON:molecular basis for reduced toxicity[J].Scientific Reports,2016,6:29105.
[60] ITO M,SATO I,ISHIZAKA M,et al.Bacterial cytochrome P450 system catabolizing the Fusarium toxin deoxynivalenol[J].Applied and Environmental Microbiology,2013,79(5):1619-1628.  
[61] POPPENBERGER B,BERTHILLER F,LUCYSHYN D,et al.Detoxification of the Fusarium mycotoxin deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana[J].The Journal of Biological Chemistry,2003,278(48):47905-47914.  
[62] TIAN Y,TAN Y L,LIU N,et al.Detoxification of deoxynivalenol via glycosylation represents novel insights on antagonistic activities of Trichoderma when confronted with Fusarium graminearum[J].Toxins,2016,8(11):335.
[63] SCHWEIGER W,BODDU J,SHIN S,et al.Validation of a candidate deoxynivalenol-inactivating UDP-glucosyltransferase from barley by heterologous expression in yeast[J].Molecular Plant-Microbe Interactions,2010,23(7):977-986.  
[64] MICHLMAYR H,MALACHOVÁ A,VARGA E,et al.Biochemical characterization of a recombinant UDP-glucosyltransferase from rice and enzymatic production of deoxynivalenol-3-O-β-D-glucoside[J].Toxins,2015,7(7):2685-2700.  
[65] PIERRON A,MIMOUN S,MURATE L S,et al.Intestinal toxicity of the masked mycotoxin deoxynivalenol-3-β-D-glucoside[J].Archives of Toxicology,2016,90(8):2037-2046.  
[66] NAGL V,WOECHTL B,SCHWARTZ-ZIMMERMANN H E,et al.Metabolism of the masked mycotoxin deoxynivalenol-3-glucoside in pigs[J].Toxicology Letters,2014,229(1):190-197.  
[67] KIMURA M,KANEKO I,KOMIYAMA M,et al.Trichothecene 3-O-acetyltransferase protects both the producing organism and transformed yeast from related mycotoxins:cloning and characterization of Tri101[J].Journal of Biological Chemistry,1998,273(3):1654-1661.  
[68] KIMURA M,TOKAI T,MATSUMOTO G,et al.Trichothecene nonproducer Gibberella species have both functional and nonfunctional 3-O-acetyltransferase genes[J].Genetics,2003,163(2):677-684.
[69] KHATIBI P A,NEWMISTER S A,RAYMENT I,et al.Bioprospecting for Trichothecene 3-O-acetyltransferases in the fungal genus Fusarium yields functional enzymes with different abilities to modify the mycotoxin deoxynivalenol[J].Applied and Environmental Microbiology,2011,77(4):1162-1170.  
[70] BROEKAERT N,DEVREESE M,DEMEYERE K,et al.Comparative in vitro cytotoxicity of modified deoxynivalenol on porcine intestinal epithelial cells[J].Food and Chemical Toxicology,2016,95:103-109.
[71] BROEKAERT N,DEVREESE M,DE MIL T,et al.Oral bioavailability,hydrolysis,and comparative toxicokinetics of 3-acetyldeoxynivalenol and 15-acetyldeoxynivalenol in broiler chickens and pigs[J].Journal of Agricultural and Food Chemistry,2015,63(39):8734-8742.  
[72] PINTON P,TSYBULSKYY D,LUCIOLI J,et al.Toxicity of deoxynivalenol and its acetylated derivatives on the intestine:differential effects on morphology,barrier function,tight junction proteins,and mitogen-activated protein kinases[J].Toxicological Sciences,2012,130(1):180-190.  
[73] KADOTA T,FURUSAWA H,HIRANO S,et al.Comparative study of deoxynivalenol,3-acetyldeoxynivalenol,and 15-acetyldeoxynivalenol on intestinal transport and IL-8 secretion in the human cell line Caco-2[J].Toxicology in Vitro,2013,27(6):1888-1895.  
[74] KLUGER B,BUESCHL C,LEMMENS M,et al.Biotransformation of the mycotoxin deoxynivalenol in Fusarium resistant and susceptible near isogenic wheat lines[J].PLoS One,2015,10(3):e0119656.
[75] GARDINER S A,BODDU J,BERTHILLER F,et al.Transcriptome analysis of the barley-deoxynivalenol interaction:evidence for a role of glutathione in deoxynivalenol detoxification[J].Molecular Plant-Microbe Interactions,2010,23(7):962-976.  
[76] WANG H W,SUN S L,GE W Y,et al.Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat[J].Science,2020,368(6493):eaba5435.
[77] WARTH B,FRUHMANN P,WIESENBERGER G,et al.Deoxynivalenol-sulfates:identification and quantification of novel conjugated (masked) mycotoxins in wheat[J].Analytical and Bioanalytical Chemistry,2015,407(4):1033-1039.  
[78] GUAN S,HE J W,YOUNG J C,et al.Transformation of trichothecene mycotoxins by microorganisms from fish digesta[J].Aquaculture,2009,290(3/4):290-295.
[79] ISLAM R,ZHOU T,YOUNG J C,et al.Aerobic and anaerobic de-epoxydation of mycotoxin deoxynivalenol by bacteria originating from agricultural soil[J].World Journal of Microbiology and Biotechnology,2012,28(1):7-13.  
[80] ZHAO L H,LI X Y,JI C,et al.Protective effect of Devosia sp. ANSB714 on growth performance,serum chemistry,immunity function and residues in kidneys of mice exposed to deoxynivalenol[J].Food and Chemical Toxicology,2016,92:143-149.
[81] LI X Y,GUO Y P,ZHAO L H,et al.Protective effects of Devosia sp. ANSB714 on growth performance,immunity function,antioxidant capacity and tissue residues in growing-finishing pigs fed with deoxynivalenol contaminated diets[J].Food and Chemical Toxicology,2018,121:246-251.
[82] SHI D H,ZHOU J C,ZHAO L H,et al.Alleviation of mycotoxin biodegradation agent on zearalenone and deoxynivalenol toxicosis in immature gilts[J].Journal of Animal Science and Biotechnology,2018,9:42.
[83] GUO Y P,HUO X T,ZHAO L H,et al.Protective effects of Bacillus subtilis ANSB060,Bacillus subtilis ANSB01G,and Devosia sp. ANSB714-based mycotoxin biodegradation agent on mice fed with naturally moldy diets[J].Probiotics and Antimicrobial Proteins,2019,12(3):994-1001.
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