Abstract
Zearalenone (ZEN) is a fungal toxin produced by Fusarium that widely occurs in various types of grains and feed. It has strong reproductive toxicity and a wide range of distribution, which will impact food and feed safety. In this study, Bacillus subtilis ZENL09, which is capable of transforming ZEN was investigated. By optimizing the fermentation conditions, the supernatant of Bacillus subtilis ZENL09 fermentation can achieve about 88% degradation rate of ZEN after reacting with ZEN for 12 h. The degradation product was collected by high-performance liquid chromatography, followed by LC-Q-TOF and MS/MS analysis to identify the changes in molecular mass and compound structure. The possible structure of the degradation product was also tentatively determined. Further evaluation of the degradation products’ cytotoxicity was conducted using HepG2 cells, and the results indicated a significant reduction in toxicity compared to ZEN. Detoxification experiments on corn steep liquor showed that the fermentation supernatant of Bacillus subtilis degraded 87% of ZEN within 12 h, which further validates its potential application for detoxification in food and agricultural products.
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References
Calado, T., Abrunhosa, L., Cabo Verde, S., Alté, L., Venâncio, A., & Fernández-Cruz, M. L. (2020). Effect of gamma-radiation on zearalenone-degradation, cytotoxicity and estrogenicity. Foods, 9(11), 1687. https://doi.org/10.3390/foods9111687
Cetin, Y., & Bullerman, L. B. (2005). Cytotoxicity of Fusarium mycotoxins to mammalian cell cultures as determined by the MTT bioassay. Food and Chemical Toxicology, 43(5), 755–764. https://doi.org/10.1016/j.fct.2005.01.016
Cho, K., Kang, J., Cho, W., Lee, C., Ha, J., & Song, K. B. (2010). In vitro degradation of zearalenone by Bacillus subtilis. Biotechnology Letters, 32, 1921–1924. https://doi.org/10.1007/s10529-010-0373-y
Darwesh, O. M., & Elshahawy, I. E. (2021). Silver nanoparticles inactivate sclerotial formation in controlling white rot disease in onion and garlic caused by the soil borne fungus Stromatinia cepivora. European Journal of Plant Pathology, 160(4), 917–934. https://doi.org/10.1007/s10658-021-02296-7
De Boer, S. A., & Diderichsen, B. (1991). On the safety of Bacillus subtilis and B. amyloliquefaciens: A review. Applied Microbiology and Biotechnology, 36, 1–4.
Dubey, P., Singh, A., & Yousuf, O. (2022). Ozonation: An evolving disinfectant technology for the food industry. Food and Bioprocess Technology, 15(9), 2102–2113. https://doi.org/10.1007/s11947-022-02876-3
El Golli, B. E., Bouaziz, C., Ladjimi, M., Renaud, F., & Bacha, H. (2009). Comparative mechanisms of zearalenone and ochratoxin A toxicities on cultured HepG2 cells: Is oxidative stress a common process? Environmental Toxicology: An International Journal, 24(6), 538–548. https://doi.org/10.1002/tox.20449
Feizollahi, E., & Roopesh, M. S. (2021). Degradation of zearalenone by atmospheric cold plasma: Effect of selected process and product factors. Food and Bioprocess Technology, 14(11), 2107–2119. https://doi.org/10.1007/s11947-021-02692-1
Guo, Y., Zhou, J., Tang, Y., Ma, Q., Zhang, J., Ji, C., & Zhao, L. (2020). Characterization and genome analysis of a zearalenone-degrading Bacillus velezensis strain ANSB01E. Current Microbiology, 77, 273–278. https://doi.org/10.1007/s00284-019-01811-8
He, X., Li, S., Li, Y., Gu, W., Sun, Y., & Sun, X. (2015). Evaluation of reduced toxicity of zearalenone as measured by the HepG2 cell assay on degradation enzymes. Food Control, 57, 161–168. https://doi.org/10.1016/j.foodcont.2015.03.031
Hussein, H.-A.A., Darwesh, O. M., Mekki, B. B., & El-Hallouty, S. M. (2019). Evaluation of cytotoxicity, biochemical profile and yield components of groundnut plants treated with nano-selenium. Biotechnology Reports, 24, e00377. https://doi.org/10.1016/j.btre.2019.e00377
Igawa, T., Takahashi-Ando, N., Ochiai, N., Ohsato, S., Shimizu, T., Kudo, T., Yamaguchi, I., & Kimura, M. (2007). Reduced contamination by the Fusarium mycotoxin zearalenone in maize kernels through genetic modification with a detoxification gene. Applied and Environmental Microbiology, 73(5), 1622–1629. https://doi.org/10.1128/AEM.01077-06
Ji, C., Fan, Y., & Zhao, L. (2016). Review on biological degradation of mycotoxins. Animal Nutrition, 2(03), 127–133. https://doi.org/10.1016/j.aninu.2016.07.003
Kurup, A. H., Patras, A., Pendyala, B., Vergne, M. J., & Bansode, R. R. (2022). Evaluation of ultraviolet-light (UV-A) emitting diodes technology on the reduction of spiked aflatoxin B-1 and aflatoxin M-1 in whole milk. Food and Bioprocess Technology, 15(1), 165–176. https://doi.org/10.1007/s11947-021-02731-x
Lei, Y., Zhao, L., Ma, Q., Zhang, J., Zhou, T., Gao, C., & Ji, C. (2014). Degradation of zearalenone in swine feed and feed ingredients by Bacillus subtilis ANSB01G. World Mycotoxin Journal, 7(2), 143–151. https://doi.org/10.3920/WMJ2013.1623
Li, K., Jia, J., Xu, Q., & Wu, N. (2023a). Whole-genome sequencing and phylogenomic analyses of a novel zearalenone-degrading Bacillus subtilis B72. 3. Biotech, 13(3), 103. https://doi.org/10.1007/s13205-023-03517-y
Li, Y., Cai, R., Fu, C., Qi, L., Yuan, Y., Yue, T., Ge, Q., Zhao, Z., & Wang, Z. (2023b). Degradation of patulin in apple juice by pulsed light and its effect on the quality. Food and Bioprocess Technology, 16(4), 870–880. https://doi.org/10.1007/s11947-022-02978-y
Luiz, K., Luís, A., Kelly, K., Carlos, R., Lilia, C., & Armando, V. (2015). Zearalenone and its derivatives α-Zearalenol and β-Zearalenol decontamination by Saccharomyces cerevisiae strains isolated from bovine forage. Toxins, 7(8), 3297–3308. https://doi.org/10.3390/toxins7083297
Rasch, C., Kumke, M., & Loehmannsroeben, H.-G. (2010). Sensing of mycotoxin producing fungi in the processing of grains. Food and Bioprocess Technology, 3(6), 908–916. https://doi.org/10.1007/s11947-010-0364-y
Richard, J. L. (2007). Some major mycotoxins and their mycotoxicoses—An overview. International Journal of Food Microbiology, 119(1–2), 3–10. https://doi.org/10.1016/j.ijfoodmicro.2007.07.019
Rogowska, A., Pomastowski, P., Sagandykova, G., & Buszewski, B. (2019). Zearalenone and its metabolites: Effect on human health, metabolism and neutralisation methods. Toxicon, 162, 46–56. https://doi.org/10.1016/j.toxicon.2019.03.004
Ropejko, K., & Twaruek, M. (2021). Zearalenone and Its metabolites-general overview, occurrence, and toxicity. Toxins, 13(1), 35. https://doi.org/10.3390/toxins13010035
Saccon, F. A. M., Parcey, D., Paliwal, J., & Sherif, S. S. (2017). Assessment of fusarium and deoxynivalenol using optical methods. Food and Bioprocess Technology, 10(1), 34–50. https://doi.org/10.1007/s11947-016-1788-9
Shen, M.-H., & Singh, R. K. (2022). Decomposing aflatoxins in peanuts using advanced oxidation processes by UV and H2O2. Food and Bioprocess Technology, 15(7), 1647–1657. https://doi.org/10.1007/s11947-022-02844-x
Sorensen, J., & L., Sondergaard, T. & E. (2014). The effects of different yeast extracts on secondary metabolite production in Fusarium. International Journal of Food Microbiology, 170, 55–60. https://doi.org/10.1016/j.ijfoodmicro.2013.10.024
Tatay, E., Font, G., & Ruiz, M.-J. (2016). Cytotoxic effects of zearalenone and its metabolites and antioxidant cell defense in CHO-K1 cells. Food and Chemical Toxicology, 96, 43–49. https://doi.org/10.1016/j.fct.2016.07.027
Tinyiro, S. E., Wokadala, C., Xu, D., & Yao, W. (2011). Adsorption and degradation of zearalenone by bacillus strains. Folia Microbiologica, 56, 321–327.
Wang, J., & Xie, Y. (2020). Review on microbial degradation of zearalenone and aflatoxins. Grain & Oil Science and Technology, 3(3), 117–125. https://doi.org/10.1016/j.gaost.2020.05.002
Wang, N., Wu, W., Pan, J., & Long, M. (2019). Detoxification strategies for zearalenone using microorganisms: A review. Microorganisms, 7(7), 208. https://doi.org/10.3390/microorganisms7070208
Yang, K., Li, K., Pan, L., Luo, X., Xing, J., Wang, J., Wang, L., Wang, R., Zhai, Y., & Chen, Z. (2020). Effect of ozone and electron beam irradiation on degradation of zearalenone and ochratoxin A. Toxins, 12(2), 138. https://doi.org/10.3390/toxins12020138
Yang, S. B., ChenXu, H., YongZhao, J., YaShu, X., JuLi, W., MingSong, X., & HuiMa, Y. H. (2021). New biotransformation mode of Zearalenone identified in Bacillus subtilis Y816 revealing a novel ZEN conjugate. Journal of Agricultural and Food Chemistry, 69(26), 7409–7419. https://doi.org/10.1021/acs.jafc.1c01817
Yang, X., Li, F., Ning, H., Zhang, W., Niu, D., Shi, Z., Chai, S., & Shan, A. (2022). Screening of pig-derived zearalenone-degrading bacteria through the zearalenone challenge model, and their degradation characteristics. Toxins, 14(3), 224. https://doi.org/10.3390/toxins14030224
Yu, Y., Qiu, L., Wu, H., Tang, Y., Yu, Y., Li, X., & Liu, D. (2011) Degradation of zearalenone by the extracellular extracts of Acinetobacter sp. SM04 liquid cultures. Biodegradation, 22(3), 613–622. https://doi.org/10.1007/s10532-010-9435-z
Yue, W., Jian, Z., Yulu, K., Hong, W., & Lixin & Shen,. (2018). Isolation and characterization of the Bacillus cereus BC7 strain, which is capable of zearalenone removal and intestinal flora modulation in mice. Toxicon Official Journal of the International Society on Toxinology, 1(155), 9–20. https://doi.org/10.1016/j.toxicon.2018.09.005
Zhou, J., Zhu, L., Chen, J., Wang, W., Zhang, R., Li, Y., Zhang, Q., & Wang, W. (2020). Degradation mechanism for Zearalenone ring-cleavage by Zearalenone hydrolase RmZHD: A QM/MM study. Science of the Total Environment, 709, 135897. https://doi.org/10.1016/j.scitotenv.2019.135897
Zinedine, A., Soriano, J. M., Molto, J. C., & Manes, J. (2007). Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: An oestrogenic mycotoxin. Food and Chemical Toxicology, 45(1), 1–18. https://doi.org/10.1016/j.fct.2006.07.030
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This work was supported by key research and development program of Hubei Province (No. 2022BBA0053).
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MX: conceptualization, methodology, investigation, writing - original draft. JC: conceptualization. PL: validation, investigation, resources. HZ: formal analysis. ML: formal analysis, resources. QD: formal analysis, resources.
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Xiang, M., Liu, P., Zhang, H. et al. In Vitro Degradation of Zearalenone by Culture Supernatant of Bacillus subtilis. Food Bioprocess Technol (2023). https://doi.org/10.1007/s11947-023-03254-3
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DOI: https://doi.org/10.1007/s11947-023-03254-3