Abstract
Deoxynivalenol (DON) is a widely distributed mycotoxin that frequently occurs in various foodstuffs, and poses a health risk to human and animals. Biodegradation of DON to less- or non-toxic substances using naturally existing microorganisms is considered the best approach for DON detoxification. Although various microorganisms capable of detoxifying DON have been reported; however, such studies on probiotic strains are scarce. In this study, a bacterial strain (ASAG 216) showed to possess the capability of detoxifying 100 μg/mL DON by 81.1% within 8 h was isolated from the intestine of a donkey. After morphological observation and 16S rDNA sequence analysis, the strain was identified as Bacillus subtilis. The DON-degradation potential of B. subtilis ASAG 216 was predominantly attributed to the culture supernatant, which turned to be sensitive to heat, sodium dodecyl sulfate, and proteinase K treatment, indicating the possible presence of extracellular proteins or enzymes in the supernatant which were responsible for DON degradation. Moreover, B. subtilis ASAG 216 has a broad temperature (35–50 °C) and pH (6.5–9.0) tolerance on DON degradation, apart from its ability to withstand conditions which generally prevail during the intestinal transit. In addition, the tested strain showed antimicrobial activity against Escherichia coli, Staphylococcus aureus and Salmonella typhimurium. These results provide satisfactory grounds for the potential use of B. subtilis ASAG 216 as a new feed additive to address DON contamination.
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van der Lee T, Zhang H, van Diepeningen A, Waalwijk C (2015) Biogeography of Fusarium graminearum species complex and chemotypes: a review. Food Addit Contam Part A 32:453–460
Pestka JJ (2007) Deoxynivalenol: toxicity, mechanisms and animal health risks. Anim Feed Sci Technol 137:283–298
Hassan Y, He JW, Perilla N, Tang KJ, Karlovsky P, Zhou T (2017) The enzymatic epimerization of deoxynivalenol by Devosia mutans proceeds through the formation of 3-keto-DON intermediate. Sci Rep 7:1–11
Schoneberg A, Musa T, Voegele RT, Vogelgsang S (2015) The potential of antagonistic fungi for control of Fusarium graminearum and Fusarium crookwellense varies depending on the experimental approach. J Appl Microbiol 118:1165–1179
Mandala G, Tundo S, Francesconi S, Gevi F, Zolla L, Ceoloni C, D’Ovidio R (2019) Deoxynivalenol detoxification in transgenic wheat confers resistance to Fusarium head blight and crown rot diseases. MPMI 32:583–592
Berthiller F, DallAsta C, Schuhmacher R, Lemmens M, Adam G, Krska R (2005) Masked mycotoxins: determination of a deoxynivalenol glucoside in artificially and naturally contaminated wheat by liquid chromatography-tandem mass spectrometry. J Agr Food Chem 53:3421–3425
Shapira R, Paster N, Magan N, Olsen M (2004) Control of mycotoxins in storage and techniques for their decontamination. In: N. Magan, M. (eds.) Olsen Mycotoxins in Food: Detection and Control. Cambridge, Woodhead Publishing, pp 190–223
Wu Q, Kuča K, Humpf HU, Klímová B, Cramer B (2017) Fate of deoxynivalenol and deoxynivalenol-3-glucoside during cereal-based thermal food processing: a review study. Mycotoxin Res 33:79–91
Rempe I, Kersten S, Valenta H, Dänicke S (2013) Hydrothermal treatment of naturally contaminated maize in the presence of sodium metabisulfite, methylamine and calcium hydroxide; effects on the concentration of zearalenone and deoxynivalenol. Mycotoxin Res 29:169–175
Murata H, Mitsumatsu M, Shimada N (2008) Reduction of feed-contaminating mycotoxins by ultraviolet irradiation: an in vitro study. Food Addit Contam A 25:1107–1110
Xu Y, Ji J, Wu H, Pi F, Blaženović I, Zhang Y, Sun X (2019) Untargeted GC-TOFMS-based cellular metabolism analysis to evaluate ozone degradation effect of deoxynivalenol. Toxicon 168:49–57
Savi GD, Cardoso WA, Furtado BG, Bortolotto T, Zanoni ET, Scussel R, Rezende LF, Machado-de-Avila RA, Montedo O, Angioletto E (2018) Antifungal activities against toxigenic Fusarium specie and deoxynivalenol adsorption capacity of ion-exchanged zeolites. J Environ Sci Heal B 53:184–190
Awad WA, Ghareeb K, Böhm J, Zentek J (2010) Decontamination and detoxification strategies for the Fusarium mycotoxin deoxynivalenol in animal feed and the effectiveness of microbial biodegradation. Food Addit Contam 27:510–520
Ahad R, Zhou T, Lepp D, Pauls KP (2017) Microbial detoxification of eleven food and feed contaminating trichothecene mycotoxins. BMC Biotechnol 17:30
He P, Young LG, Forsberg C (1992) Microbial transformation of deoxynivalenol (vomitoxin). Appl Environ Microbiol 58:3857–3863
He JW, Hassan YI, Perilla N, Li XZ, Boland GJ, Zhou T (2016) Bacterial epimerization as a route for deoxynivalenol detoxification: the influence of growth and environmental conditions. Front Microbiol 7:572
Ikunaga Y, Sato I, Grond S, Numaziri N, Yoshida S, Yamaya H et al (2011) Nocardioides sp. strain WSN05-2, isolated from a wheat field, degrades deoxynivalenol, producing the novel intermediate 3-epi-deoxynivalenol. Appl Microbiol Biotechnol 89:419–427
Li XZ, Zhu C, de Lange CFM, Zhou T, He JW, Yu HW, Gong J, Young JC (2011) Efficacy of detoxification of deoxynivalenol-contaminated corn by Bacillus sp. LS100 in reducing the adverse effects of the mycotoxin on swine growth performance. Food Addit Contam Part A 28:894–901
Guo HY, Ji J, Wang JS, Sun XL (2020) Deoxynivalenol: Masked forms, fate during food processing, and potential biological remedies. Compr Rev Food Sci Food Saf 19:895–926
FAO/WHO (2002) Guidelines for the evaluation of probiotics in food. Food and Agriculture Organization of the United Nations and World Health Organization Working Group Report
Chlebicz A, Śliżewska K (2020) In vitro detoxification of aflatoxin B 1, deoxynivalenol, fumonisins, T-2 Toxin and zearalenone by probiotic bacteria from genus lactobacillus and saccharomyces cerevisiae yeast. Probiotics Antimicro Prot 12:289–301
Franco TS, Garcia S, Hirooka EY, Ono YS, dos San-tos JS (2011) Lactic acid bacteria in the inhibition of Fusarium graminearum and deoxynivalenol detoxification. J Appl Microbio 111:739–748
Zou ZY, He ZF, Li HJ, Han PF, Meng X, Zhang Y, Tang J (2012) In vitro removal of deoxynivalenol and T-2 toxin by lactic acid bacteria. Food Sci Biotechnol 21:1677–1683
Niderkorn V, Morgavi DP, Pujos E, Tissandier A, Boudra H (2007) Screening of fermentative bacteria for their ability to bind and biotransform deoxynivalenol, zearalenone and fumonisins in an in vitro simulated corn silage model. Food Addit Contam 24:406–415
Juodeikiene G, Bartkiene E, Cernauskas D, Cizeikiene D, Zadeike D, Lele V, Bartkevics V (2018) Antifungal activity of lactic acid bacteria and their application for Fusarium mycotoxin reduction in malting wheat grains. LWT-Food Sci Technol 89:307–314
Cheng B, Wan CX, Yang SL, Xu HG, Wei H, Liu JS, Tian WH, Zeng M (2010) Dedoxification of deoxynivalenol by Bacillus strains. J Food Safety 30:599–614
Wang SW, Hou QQ, Guo QQ, Zhang J, Sun YM, Wei H, Shen LX (2020) Isolation and characterization of a deoxynivalenol-degrading bacterium Bacillus licheniformis YB9 with the capability of modulating intestinal microbial flora of mice. Toxins 12:184
Dong XZ, Cai MY (2001) Common bacterial identification system manual. Science Press, Beijing
Huang Y, Adams MC (2004) In vitro assessment of the upper gastrointestinal tolerance of potential probiotic dairy propionibacteria. Int J Food Microbio 91:253–260
Raksha Rao K, Vipin AV, Hariprasa P, Anu Appaiah KA, Venkateswaran G (2017) Biological detoxification of aflatoxin B1 by Bacillus licheniformis CFR1. Food Control 71:234–241
Ul Hassan Z, Al Thani R, Balmas V, Migheli Q, Jaoua S (2019) Prevalence of Fusarium fungi and their toxins in marketed feed. Food Control 104:224–230
Pestka JJ (2010) Deoxynivalenol: mechanisms of action, human exposure, and toxicological relevance. Arch Toxicol 84:663–679
Zhang J, Qin XJ, Guo YP, Zhang QQ, Ma QG, Ji C, Zhao LH (2020) Enzymatic degradation of deoxynivalenol by a novel bacterium, Pelagibacterium halotolerans ANSP101. Food Chem Toxicol 140:111276
Fuchs E, Binder E, Heidler D, Krska R (2002) Structural characterization of metabolites after the microbial degradation of type A trichothecenes by the bacterial strain BBSH 797. Food Addit Contam 19:379–386
Gao X, Mu P, Wen J, Sun Y, Chen Q, Deng Y (2018) Detoxification of trichothecene mycotoxins by a novel bacterium, Eggerthella sp. DII-9. Food Chem Toxicol 112:310–319
He JW, Bondy GS, Zhou T, Caldwell D, Boland GJ, Scott PM (2015) Toxicology of 3-epi-deoxynivalenol, a deoxynivalenol-transformation product by Devosia mutans 17-2-E-8. Food Chem Toxicol 84:250–259
Hong HA, Duc LH, Cutting SM (2005) The use of bacterial spore formers as probiotics. Fems Microbio Rev 29:813–835
Jeong JS, Kim IH (2014) Effect of Bacillus subtilis C-3102 spores as a probiotic feed supplement on growth performance, noxious gas emission, and intestinal microflora in broilers. Poult Sci 93:3097–3103
Larsen N, Thorsen L, Kpikpi EN (2014) Characterization of Bacillus spp. strains for use as probiotic additives in pig feed. Appl Microbiol Biot 98:1105–1118
Zokaeifar H, Balcazar JL, Saad CR, Kamarudin MS, Sijam K, Arshad A, Nejat N (2012) Effects of Bacillus subtilis on the growth performance, digestive enzymes, immune gene expression and disease resistance of white shrimp Litopenaeus vannamei. Fish Shellfish Immun 33:683–689
Guan S, He JW, Young JC, Zhu HH, Li XZ, Ji C (2009) Transformation of trichothecene mycotoxins by microorganisms from fish digesta. Aquaculture 290:290–295
Faizan AS, Yan B, Tian FW, Zhao JX, Zhang H, Chen W (2019) Lactic acid bacteria as antifungal and anti-mycotoxigenic agents: a comprehensive review. Compr Rev Food Sci F 18:1403–1436
Carere J, Hassan YI, Lepp D, Zhou T (2018) The enzymatic detoxification of the mycotoxin deoxynivalenol: identification of DepA from the DON epimerization pathway. Microb Biotechnol 11:1106–1111
Carere J, Hassan YI, Lepp D, Zhou T (2018) The identification of DepB: an Enzyme 462 responsible for the final detoxification step in the deoxynivalenol epimerization pathway in Devosia mutans 17–2-E-8. Front Microbiol 9
Acknowledgements
We would like to thank the National Natural Science Foundation of China and Natural Science Foundation of Shanxi for the financial support of this paper. And we thank for Beijing Century Honbon Bio. Co., to provided fermentation tank.
Funding
This study was supported by the National Natural Science Foundation of China (Grant No. 31902198) and Natural Science Foundation of Shanxi (201901D211183).
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Jia, R., Cao, L., Liu, W. et al. Detoxification of deoxynivalenol by Bacillus subtilis ASAG 216 and characterization the degradation process. Eur Food Res Technol 247, 67–76 (2021). https://doi.org/10.1007/s00217-020-03607-8
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DOI: https://doi.org/10.1007/s00217-020-03607-8