Abstract
Deoxynivalenol (DON), one of the most widespread mycotoxins in food and feed, poses a persistent health threat to humans and farm animals, and is difficult to eliminate. The utilization of the biotransformation mechanism by microorganisms to detoxify DON is a promising strategy. Although individual strains are capable of DON degradation, their isolation and purification are challenging and time-consuming. Recently, the microbial consortia concept has been proposed, owing to their ability to perform more complex tasks and are more tolerant to environmental changes than individual strains or species. In this study, the novel microbial consortia C1 that could efficiently convert DON to de-epoxy DON (DOM-1) was screened from the cecum contents of ducks. After 24 h anaerobic incubation, 100 μg/ml DON was completely degraded by C1. In vitro, C1 can effectively degrade DON in corn steep liquor (CSL) with an efficiency of 49.44% within 14 days. Furthermore, C1 effectively alleviated the DON poisoning in mice. After C1 treatment, the serum DON level decreased by 40.39%, and the reduction in serum total protein and albumin levels were mitigated. Additionally, C1 is effective in protecting the mouse liver against 5 mg/kg DON. These findings suggest that C1 could be a promising DON biological detoxifier and provide novel microbial resources for preventing DON contamination.
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Achal V, Mukherjee A, Reddy MS (2010) Biocalcification by Sporosarcina pasteurii using corn steep liquor as the nutrient source. Ind Biotechnol 6:170–174
Ahad R, Zhou T, Lepp D, Pauls KP (2017) Microbial detoxification of eleven food and feed contaminating trichothecene mycotoxins. BMC Biotechnol 17:30
Amézqueta S, Gonzalez-Penas E, Lizarraga T, Murillo-Arbizu M, De Cerain AL (2008) A simple chemical method reduces ochratoxin A in contaminated cocoa shells. J Food Prot 71:1422–1426
Cai C, Zhao M, Yao F, Zhu R, Cai H, Shao S, Li X-Z, Zhou T (2022) Deoxynivalenol degradation by various microbial communities and its impacts on different bacterial flora. Toxins 14:537
Chaytor AC, See MT, Hansen JA, Souza A, Kim SW (2010) Effects of chronic exposure of diets with low levels of aflatoxin and deoxynivalenol on growth and immune status of pigs. J Anim Sci 89:124–135
Claeys L, Romano C, De Ruyck K, Wilson H, Fervers B, Korenjak M, Zavadil J, Gunter MJ, De Saeger S, De Boevre M (2020) Mycotoxin exposure and human cancer risk: a systematic review of epidemiological studies. Compr Rev Food Sci Food Saf 19:1449–1464
Eskola M, Kos G, Elliott CT, Hajšlová J, Mayar S, Krska R (2020) Worldwide contamination of food-crops with mycotoxins: validity of the widely cited ‘FAO estimate’ of 25. Crit Rev Food Sci Nutr 60:2773–2789
Feizollahi E, Roopesh MS (2021) Mechanisms of deoxynivalenol (DON) degradation during different treatments: a review. Crit Rev Food Sci Nutr 62:5903–5924
Freire L, Sant’Ana A S, (2018) Modified mycotoxins: an updated review on their formation, detection, occurrence, and toxic effects. Food Chem Toxicol 111:189–205
Frobose HL, Erceg JA, Fowler SQ, Tokach M, Derouchey JM, Woodworth JC, Dritz SS, Goodband RD (2016) The progression of deoxynivalenol-induced growth suppression in nursery pigs and the potential of an algae-modified montmorillonite clay to mitigate these effects. J Anim Sci 94:3746–3759
Fuchs E, Binder EM, 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, Zhu X, Chen X, Tang S, Wu Y, Miao X, Wang X, Wen J, Deng Y (2020) Dual function of a novel bacterium, Slackia sp. D-G6: detoxifying deoxynivalenol and producing the Natural Estrogen Analogue, Equol. Toxins 12:85
Hassan YI, He JW, Lepp D, Zhou T (2019) Understanding the bacterial response to mycotoxins: the transcriptomic analysis of deoxynivalenol-induced changes in Devosia mutans 17-2-E-8. Front Pharmacol 10:1098
He P, Young L, Forsberg C (1992) Microbial transformation of deoxynivalenol (vomitoxin). Appl Environ Microbiol 58:3857–3863
He C, Fan Y, Liu G, Zhang H (2008) Isolation and identification of a strain of Aspergillus tubingensis with deoxynivalenol biotransformation capability. Int J Mol Sci 9:2366–2375
Hedman R, Pettersson H (1997) Transformation of nivalenol by gastrointestinal microbes. Arch Anim Nutr 50:321–329
Ikunaga Y, Sato I, Grond S, Numaziri N, Yoshida S, Yamaya H, Hiradate S, Hasegawa M, Koitabashi TM, Al E (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
Islam R, Zhou T, Young JC, Goodwin PH, Pauls KP (2012) Aerobic and anaerobic de-epoxydation of mycotoxin deoxynivalenol by bacteria originating from agricultural soil. World J Microbiol Biotechnol 28:7–13
Jard G, Liboz T, Mathieu F, Guyonvarc’H A, Lebrihi A (2011) Review of mycotoxin reduction in food and feed: from prevention in the field to detoxification by adsorption or transformation. Food Addit Contam Part A 28:1590–1609
Jin J, Fall M, Liu Q, Rietjens IM, Xing F (2021) Comparative microbial conversion of deoxynivalenol and acetylated deoxynivalenol in different parts of the chicken intestine as detected in vitro and translated to the in vivo situation. J Agric Food Chem 69:15384–15392
Jmh A, Dpba B (2021) Deoxynivalenol: Mechanisms of action and its effects on various terrestrial and aquatic species. Food Chem Toxicol: Int J Publ British Ind Biol Res Assoc 157:112616
Khodaei D, Javanmardi F, Khaneghah AM (2020) The global overview of the occurrence of mycotoxins in Cereals: a three-year survey. Curr Opin Food Sci 39:36–42
Lauren D, Ringrose M (1997) Determination of the fate of three Fusarium mycotoxins through wet-milling of maize using an improved HPLC analytical technique. Food Addit Contam 14:435–443
Li J, Bai Y, Ma K, Ren Z, Li J, Zhang J, Shan A (2022) Dihydroartemisinin alleviates deoxynivalenol induced liver apoptosis and inflammation in piglets. Ecotoxicol Environ Saf 241:113811
Li F, Wang J, Huang L, Chen H, Wang C (2017) Effects of adding Clostridium sp. WJ06 on intestinal morphology and microbial diversity of growing pigs fed with natural deoxynivalenol contaminated wheat. Toxins 9:383
Liggett RW, Koffler H (1948) Corn steep liquor in microbiology. Bacteriol Rev 12:297–311
Liu L, Xie M, Wei D (2022) Biological detoxification of mycotoxins: current status and future advances. Int J Mol Sci 23:1064
Luo Y, Liu X, Li J (2018) Updating techniques on controlling mycotoxins—a review. Food Control 89:123–132
Mishra S, Srivastava S, Dewangan J, Divakar A, Kumar Rath S (2022) Global occurrence of deoxynivalenol in food commodities and exposure risk assessment in humans in the last decade: a survey. Crit Rev Food Sci Nutr 60:1346–1374
Moon Y, Kim HK, Suh H, Chung DH (2007) Toxic alterations in chick embryonic liver and spleen by acute exposure to Fusarium-producing mycotoxin deoxynivalenol. Biol Pharm Bull 30:1808–1812
Park J, Kim D-H, Moon J-Y, An J-A, Kim Y-W, Chung S-H, Lee C (2018) Distribution analysis of twelve mycotoxins in corn and corn-derived products by LC-MS/MS to evaluate the carry-over ratio during wet-milling. Toxins 10:319
Patil A, Munot N, Patwekar M, Patwekar F, Ahmad I, Alraey Y, Alghamdi S, Kabrah A, Dablool AS, Islam F (2022) Encapsulation of lactic acid bacteria by lyophilisation with its effects on viability and adhesion properties. Evidence-Based Complementary and Alternative Medicine: Ecam 2022:4651194
Pestka JJ (2010) Deoxynivalenol-induced proinflammatory gene expression: mechanisms and pathological sequelae. Toxins 2:1300–1317
Qu R, Jiang C, Wu W, Pang B, Lei S, Lian Z, Shao D, Jin M, Shi J (2019) Conversion of DON to 3-epi -DON in vitro and toxicity reduction of DON in vivo by Lactobacillus rhamnosus. Food Funct 10:2785–2796
Ruan H, Lu Q, Wu J, Qin J, Sui M, Sun X, Shi Y, Luo J, Yang M (2022) Hepatotoxicity of food-borne mycotoxins: molecular mechanism, anti-hepatotoxic medicines and target prediction. Crit Rev Food Sci Nutr 62:2281–2308
Ruhnau D, Hess C, Doupovec B, Grenier B, Schatzmayr D, Hess M, Awad W (2021) Deepoxy-deoxynivalenol (DOM-1), a derivate of deoxynivalenol (DON), exhibits less toxicity on intestinal barrier function, Campylobacter jejuni colonization and translocation in broiler chickens. Gut Pathogens 13:44
Shalapy A, Zhao S, Zhang C, Li Y, Geng H, Ullah S, Wang G, Huang S, Liu Y (2020) Adsorption of deoxynivalenol (DON) from corn steep liquor (CSL) by the microsphere adsorbent SA/CMC loaded with calcium. Toxins 12:208
Sun Y, Jiang J, Mu P, Lin R, Wen J, Deng Y (2022) Toxicokinetics and metabolism of deoxynivalenol in animals and humans. Arch Toxicol 96:2639–2654
Ullah Z, Yousaf M, Shami M, Sharif M, Mahrose K (2018) Effect of graded levels of dietary corn steep liquor on growth performance, nutrient digestibility, haematology and histopathology of broilers. J Anim Physiol Anim Nutr 102:e395–e402
Vainio H, Heseltine E, Wilbourn J (1993) Report on an IARC working group meeting on some naturally occurring substances. Int J Cancer 53:535–537
Völkl A, Vogler B, Schollenberger M, Karlovsky P (2004) Microbial detoxification of mycotoxin deoxynivalenol. Journal of Basic Microbiology: an International Journal on Biochemistry, Physiology, Genetics, Morphology, and Ecology of Microorganisms 44:147–156
Wang G, Wang Y, Ji F, Xu L, Yu M, Shi J, Xu J (2019) Biodegradation of deoxynivalenol and its derivatives by Devosia insulae A16. Food Chem 276:436–442
Wang C, Huang L, Wang P, Liu Q, Wang J (2020) The effects of deoxynivalenol on the ultrastructure of the sacculus rotundus and vermiform appendix, as well as the intestinal microbiota of weaned rabbits. Toxins 12:569
Wang R, Cui N, Yiannikouris A, Huang Y, Zhao W, Su X, Lin G, Zhu R, Song Z, Wang P (2022) New insights into the deposition of zearalenone in minipigs: a suitable bioindicator for internal exposure. J Agric Food Chem 70(43):14032–14042
Wu Y, Ye J, Wang S, Han X, Li L, Zhu L, Li S, Liu H, Wang Y, Shao Y (2023) An accurate and efficient method for simultaneous determination of 16 trichothecenes in maize and wheat by UHPLC-Q-Orbitrap-HRMS combined one-step pretreatment with a novel isotope multipoint calibration strategy. Food Control 149:109708
Yu H, Zhou T, Gong J, Young C, Su X, Li XZ, Zhu H, Rong T, Yang R (2010) Isolation of deoxynivalenol-transforming bacteria from the chicken intestines using the approach of PCR-DGGE guided microbial selection. BMC Microbiol 10:182
Zhao L, Zhang L, Xu Z, Liu X, Sun L (2021) Occurrence of Aflatoxin B 1, deoxynivalenol and zearalenone in feeds in China during 2018–2020. J Animal Sci Biotechnol 12:74
Acknowledgements
We appreciate the help of Yu Wu from the Academy of National Food and Strategic Reserves Administration for valuable analysis with the mass spectrometry.
Funding
This work was supported by the National Key Research and Development Program of China: No.2016YFE0113300; Central Public-interest Scientific Institution Basal Research Fund (No. 1610382022007); European Union’s Horizon 2020 research and innovation program under grant agreement: No. 678012.
Author information
Authors and Affiliations
Contributions
J. Q. W. and Z. L. W. conceived and designed the experiments; Y. D. Z., Z. L. W., B. Q. G., and J. W. W. conducted the experiments; H. T., B. H., X. M. W., and J. L. supervised the work, provided some data analysis, and revised the final version of the manuscript; Z. L. W., and J. Q. W. wrote the manuscript.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Zheng, Y., Gao, B., Wu, J. et al. Degradation of deoxynivalenol by a microbial consortia C1 from duck intestine. Mycotoxin Res 40, 147–158 (2024). https://doi.org/10.1007/s12550-023-00511-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12550-023-00511-4