A NADPH-Dependent Aldo/Keto Reductase Is Responsible for Detoxifying 3-Keto-Deoxynivalenol to 3-epi-Deoxynivalenol in Pelagibacterium halotolerans ANSP101
Abstract
:1. Introduction
2. Materials and Methods
2.1. Chemiclas and Reagents
2.2. 3-Keto-DON Detection by HPLC
2.3. 3-Keto-DON and 3-epi-DON Identification by HPLC-MS/MS
2.4. Sequencing and Annotation of P. halotolerans ANSP101
2.5. Cloning and Heterologous Expression of Recombinant Protein in E. coli
2.6. Testing the Candidates for 3-Keto-DON Degradation Activity
2.7. Degradation Characteristics of AKR4 on 3-Keto-DON
2.7.1. Cofactor Specificity
2.7.2. Effects of Mycotoxin and Enzyme Concentration on the Removal Rate of 3-Keto-DON by AKR4
2.7.3. Effects of pH and Temperature on the Activity of AKR4
2.7.4. pH Stability and Thermostability of AKR4
2.8. Bioinformatics Analysis
3. Results
3.1. Identification of Aldo/Keto Reductase Genes by Microbial Genomic Sequence Analysis
3.2. Expression and Purification of Candidate Aldo/Keto Reductases
3.3. Degradation of 3-Keto-DON by Candidate Aldo/Keto Reductases
3.4. Characteristic of AKR4
3.5. Cofactor Specificity of AKR4
3.6. Effects of Mycotoxin and Enzyme Concentration on the Removal Rate of 3-Keto-DON by AKR4
3.7. Effects of pH and Temperature on the Removal Rate of 3-Keto-DON by AKR4
3.8. Degradation Products of 3-Keto-DON
3.9. Binding Model of 3-Keto-DON to AKR4 by Molecular Docking
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Zhao, Z.T.; Zhang, Z.Z.; Zhang, H.X.; Liang, Z.H. Small peptides in the detection of mycotoxins and their potential applications in mycotoxin removal. Toxins 2022, 14, 795. [Google Scholar] [CrossRef] [PubMed]
- Eskola, M.; Kos, G.; Elliott, C.T.; Hajslova, J.; Mayar, S.; Krska, R. Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited ‘FAO estimate’ of 25%. Crit. Rev. Food Sci. 2020, 60, 2773–2789. [Google Scholar] [CrossRef] [PubMed]
- Adegoke, T.V.; Yang, B.L.; Tian, X.Y.; Yang, S.; Gao, Y.; Ma, J.N.; Wang, G.; Si, P.D.; Li, R.Y.; Xing, F.G. Simultaneous degradation of aflatoxin B1 and zearalenone by Porin and Peroxiredoxin enzymes cloned from Acinetobacter nosocomialis Y1. J. Hazard. Mater. 2023, 459, 132105. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.P.; Zhang, X.N.; Nie, J.Y.; Bacha, S.A.S.; Yan, Z.; Gao, G.M. Occurrence and co-occurrence of mycotoxins in apple and apple products from China. Food Control 2020, 118, 107354. [Google Scholar] [CrossRef]
- Summerell, B.A.; Leslie, J.F. Fifty years of Fusarium: How could nine species have ever been enough? Fungal Divers. 2011, 50, 135–144. [Google Scholar] [CrossRef]
- Riahi, I.; Pérez-Vendrell, A.M.; Ramos, A.J.; Brufau, J.; Esteve-Garcia, E.; Schulthess, J.; Marquis, V. Biomarkers of deoxynivalenol toxicity in chickens with special emphasis on metabolic and welfare parameters. Toxins 2021, 13, 217. [Google Scholar] [CrossRef] [PubMed]
- Payros, D.; Alassane-Kpembi, I.; Pierron, A.; Loiseau, N.; Pinton, P.; Oswald, I.P. Toxicology of deoxynivalenol and its acetylated and modified forms. Arch Toxicol. 2016, 90, 2931–2957. [Google Scholar] [CrossRef] [PubMed]
- Toutounchi, N.S.; Braber, S.; van’t Land, B.; Thijssen, S.; Garssen, J.; Folkerts, G.; Hogenkamp, A. Deoxynivalenol exposure during pregnancy has adverse effects on placental structure and immunity in mice model. Reprod. Toxicol. 2022, 112, 109–118. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.J.; Ryu, D. Advances in mycotoxin research: Public health perspectives. J. Food Sci. 2015, 80, T2970–T2983. [Google Scholar] [CrossRef]
- Galvano, F.; Piva, A.; Ritieni, A.; Galvano, G. Dietary strategies to counteract the effects of mycotoxins: A review. J. Food Prot. 2001, 64, 120–131. [Google Scholar] [CrossRef]
- Gao, X.J.; Mu, P.Q.; Wen, J.K.; Sun, Y.; Chen, Q.M.; Deng, Y.Q. Detoxification of trichothecene mycotoxins by a novel bacterium, Eggerthella sp DⅡ-9. Food Chem. Toxicol. 2018, 112, 310–319. [Google Scholar] [CrossRef]
- Gao, X.J.; Mu, P.Q.; Zhu, X.H.; Chen, X.X.; Tang, S.L.; Wu, Y.T.; Miao, X.; Wang, X.H.; Wen, J.K.; Deng, Y.Q. Dual function of a novel bacterium, Slackia sp. D-G6: Detoxifying deoxynivalenol and producing the natural estrogen analogue, equol. Toxins 2020, 12, 85. [Google Scholar] [CrossRef] [PubMed]
- He, W.J.; Shi, M.M.; Yang, P.; Huang, T.; Yuan, Q.S.; Yi, S.Y.; Wu, A.B.; Li, H.P.; Gao, C.B.; Zhang, J.B.; et al. Novel soil bacterium strain Desulfitobacterium sp. PGC-3-9 detoxifies trichothecene mycotoxins in wheat via de-epoxidation under aerobic and anaerobic conditions. Toxins 2020, 12, 363. [Google Scholar] [CrossRef] [PubMed]
- Ito, M.; Sato, I.; Ishizaka, M.; Yoshida, S.; Koitabashi, M.; Yoshida, S.; Tsushima, S. Bacterial cytochrome P450 system catabolizing the Fusarium toxin deoxynivalenol. Appl. Environ. Microb. 2013, 79, 1619–1628. [Google Scholar] [CrossRef] [PubMed]
- Kimura, M.; Tokai, T.; Matsumoto, G.; Fujimura, M.; Hamamoto, H.; Yoneyama, K.; Shibata, T.; Yamaguchi, I. Trichothecene nonproducer Gibberella species have both functional and nonfunctional 3-O-acetyltransferase genes. Genetics 2003, 163, 677–684. [Google Scholar] [CrossRef] [PubMed]
- Michlmayr, H.; Malachov, A.; Varga, E. Biochemical characterization of a recombinant UDP-glucosyltransferase from rice and enzymatic production of deoxynivalenol-3-O-β-D-glucoside. Toxins 2015, 7, 2685–2700. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.W.; Sun, S.L.; Ge, W.Y.; Zhao, L.F.; Hou, B.Q.; Wang, K.; Lyu, Z.F.; Chen, L.Y.; Xu, S.S.; Guo, J.; et al. Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. Science 2020, 368, eaba5435. [Google Scholar] [CrossRef] [PubMed]
- Pierron, A.; Mimoun, S.; Murate, L.S.; Loiseau, N.; Lippi, Y.; Bracarense, A.P.F.L.; Schatzmayr, G.; He, J.W.; Zhou, T.; Moll, W.D.; et al. Microbial biotransformation of DON: Molecular basis for reduced toxicity. Sci. Rep. 2016, 6, 29105. [Google Scholar] [CrossRef] [PubMed]
- Hassan, Y.I.; He, J.W.; Perilla, N.; Tang, K.J.; Karlovsky, P.; Zhou, T. The enzymatic epimerization of deoxynivalenol by Devosia mutans proceeds through the formation of 3-keto-DON intermediate. Sci. Rep. 2017, 7, 6929. [Google Scholar] [CrossRef] [PubMed]
- He, W.J.; Zhang, L.M.; Yi, S.Y.; Tang, X.L.; Yuan, Q.S.; Guo, M.W.; Wu, A.B.; Qu, B.; Li, H.P.; Liao, Y.C. An aldo-keto reductase is responsible for Fusarium toxin-degrading activity in a soil Sphingomonas strain. Sci. Rep. 2017, 7, 9549. [Google Scholar] [CrossRef] [PubMed]
- He, W.J.; Shi, M.M.; Yang, P.; Huang, T.; Zhao, Y.; Wu, A.B.; Dong, W.B.; Li, H.P.; Zhang, J.B.; Liao, Y.C. A quinone-dependent dehydrogenase and two NADPH-dependent aldo/keto reductases detoxify deoxynivalenol in wheat via epimerization in a Devosia strain. Food Chem. 2020, 321, 126703. [Google Scholar] [CrossRef] [PubMed]
- Carere, J.; Hassan, Y.I.; Lepp, D.; Zhou, T. The enzymatic detoxification of the mycotoxin deoxynivalenol: Identification of DepA from the DON epimerization pathway. Microb. Biotechnol. 2018, 11, 1106–1111. [Google Scholar] [CrossRef] [PubMed]
- Carere, J.; Hassan, Y.I.; Lepp, D.; Zhou, T. The identification of DepB: An enzyme responsible for the final detoxification step in the deoxynivalenol epimerization pathway in Devosia mutans 17-2-E-8. Front. Microbiol. 2018, 9, 1573. [Google Scholar] [CrossRef] [PubMed]
- Zhang, J.; Qin, X.J.; Guo, Y.P.; Zhang, Q.Q.; Ma, Q.G.; Ji, C.; Zhao, L.H. Enzymatic degradation of deoxynivalenol by a novel bacterium, Pelagibacterium halotolerans ANSP101. Food Chem. Toxicol. 2020, 140, 111276. [Google Scholar] [CrossRef]
- Qin, X.J.; Zhang, J.; Liu, Y.R.; Guo, Y.P.; Tang, Y.; Zhang, Q.Q.; Ma, Q.G.; Ji, C.; Zhao, L.H. A quinoprotein dehydrogenase from Pelagibacterium halotolerans ANSP101 oxidizes deoxynivalenol to 3-keto-deoxynivalenol. Food Control. 2022, 136, 108834. [Google Scholar] [CrossRef]
- Altschul, S.F.; Gish, W.; Miller, W.; Myers, E.W.; Lipman, D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215, 403–410. [Google Scholar] [CrossRef] [PubMed]
- Penning, T.M. The aldo-keto reductases (AKRs): Overview. Chem-Biol. Interact. 2015, 234, 236–246. [Google Scholar] [CrossRef] [PubMed]
- Ikunaga, Y.; Sato, I.; Grond, S.; Numaziri, N.; Yoshida, S.; Yamaya, H.; Hiradate, S.; Hasegawa, M.; Toshima, H.; Koitabashi, M.; et al. Nocardioides sp. strain WSN05-2, isolated from a wheat field, degrades deoxynivalenol, producing the novel intermediate 3-epi-deoxynivalenol. Appl. Microbiol. Biotechnol. 2011, 89, 419–427. [Google Scholar] [CrossRef]
- Wang, Y.; Zhang, H.H.; Zhao, C.; Han, Y.T.; Liu, Y.C.; Zhang, X.L. Isolation and characterization of a novel deoxynivalenol-transforming strain Paradevosia shaoguanensis DDB001 from wheat field soil. Lett. Appl. Microbiol. 2017, 65, 414–422. [Google Scholar] [CrossRef] [PubMed]
- Qu, R.; Jiang, C.M.; Wu, W.Q.; Pang, B.; Lei, S.Z.; Lian, Z.Y.; Shao, D.Y.; Jin, M.L.; Shi, J.L. Conversion of DON to 3-epi-DON in vitro and toxicity reduction of DON in vivo by Lactobacillus rhamnosus. Food Funct. 2019, 10, 2785–2796. [Google Scholar] [CrossRef]
- He, J.W.; Bondy, G.S.; Zhou, T.; Caldwell, D.; Boland, G.J.; Scott, P.M. Toxicology of 3-epi-deoxynivalenol, a deoxynivalenol-transformation product by Devosia mutans 17-2-E-8. Food Chem. Toxicol. 2015, 84, 250–259. [Google Scholar] [CrossRef] [PubMed]
- Sengupta, D.; Naik, D.; Reddy, A.R. Plant aldo-keto reductases (AKRs) as multi-tasking soldiers involved in diverse plant metabolic processes and stress defense: A structure-function update. J. Plant Physiol. 2015, 179, 40–55. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Liu, Y.; Ma, M.; Tang, Y.; Huang, Z.; Guo, Y.; Ma, Q.; Zhao, L. A NADPH-Dependent Aldo/Keto Reductase Is Responsible for Detoxifying 3-Keto-Deoxynivalenol to 3-epi-Deoxynivalenol in Pelagibacterium halotolerans ANSP101. Foods 2024, 13, 1064. https://doi.org/10.3390/foods13071064
Liu Y, Ma M, Tang Y, Huang Z, Guo Y, Ma Q, Zhao L. A NADPH-Dependent Aldo/Keto Reductase Is Responsible for Detoxifying 3-Keto-Deoxynivalenol to 3-epi-Deoxynivalenol in Pelagibacterium halotolerans ANSP101. Foods. 2024; 13(7):1064. https://doi.org/10.3390/foods13071064
Chicago/Turabian StyleLiu, Yanrong, Mingxin Ma, Yu Tang, Zhenqian Huang, Yongpeng Guo, Qiugang Ma, and Lihong Zhao. 2024. "A NADPH-Dependent Aldo/Keto Reductase Is Responsible for Detoxifying 3-Keto-Deoxynivalenol to 3-epi-Deoxynivalenol in Pelagibacterium halotolerans ANSP101" Foods 13, no. 7: 1064. https://doi.org/10.3390/foods13071064