Microbial and enzymatic battle with food contaminant zearalenone (ZEN).
Bacteria
Biochemical mechanism
Biodegradation
Detoxification
Enzymes
Fungi
Yeast
Zearalenone (ZEN)
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
Jun 2022
Jun 2022
Historique:
received:
19
04
2022
accepted:
01
06
2022
revised:
31
05
2022
pubmed:
16
6
2022
medline:
9
7
2022
entrez:
15
6
2022
Statut:
ppublish
Résumé
Zearalenone (ZEN) contamination of various foods and feeds is an important global problem. In some animals and humans, ZEN causes significant health issues in addition to massive economic losses, annually. Therefore, removal or degradation of the ZEN in foods and feeds is required to be done. The conventional physical and chemical methods have some serious issues including poor efficiency, decrease in nutritional value, palatability of feed, and use of costly equipment. Research examined microbes from diverse media for their ability to degrade zearalenone and other toxins, and the findings of several investigations revealed that enzymes produced from microbes play a significant role in the degradation of mycotoxins. In established bacterial hosts, genetically engineered technique was used to enhance heterologously produced degrading enzymes. Then, the bio-degradation of ZEN by the use of micro-organisms or their enzymes is much more advantageous and is close to nature and ecofriendly. Furthermore, an effort is made to put forward the work done by different scientists on the biodegradation of ZEN by the use of fungi, yeast, bacteria, and/or their enzymes to degrade the ZEN to non-toxic products. KEY POINTS: •Evolved microbial strains degraded ZEA more quickly •Different degrading properties were studied.
Identifiants
pubmed: 35705747
doi: 10.1007/s00253-022-12009-7
pii: 10.1007/s00253-022-12009-7
doi:
Substances chimiques
Mycotoxins
0
Zearalenone
5W827M159J
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
4353-4365Subventions
Organisme : Innovative Research Group Project of the National Natural Science Foundation of China
ID : 41861124004
Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abbès S, Ben Salah-Abbès J, Sharafi H, Oueslati R, Noghabi KA (2013) Lactobacillus paracasei BEJ01 prevents immunotoxic effects during chronic zearalenone exposure in Balb/c mice. Immunopharmacol Immunotoxicol 35:341–348. https://doi.org/10.3109/08923973.2013.772194
doi: 10.3109/08923973.2013.772194
pubmed: 23464632
Adebo OA, Njobeh PB, Gbashi S, Nwinyi OC, Mavumengwana V (2017) Review on microbial degradation of aflatoxins. Crit Rev Food Sci Nutr 57:3208–3217. https://doi.org/10.1080/10408398.2015.1106440
doi: 10.1080/10408398.2015.1106440
pubmed: 26517507
Adibnia E, Razi M, Malekinejad H (2016) Zearalenone and 17 β-estradiol induced damages in male rats reproduction potential; evidence for ERα and ERβ receptors expression and steroidogenesis. Toxicon 120:133–146. https://doi.org/10.1016/j.toxicon.2016.08.009
doi: 10.1016/j.toxicon.2016.08.009
pubmed: 27527272
Alshannaq A, Yu JH (2017) Occurrence, toxicity, and analysis of major mycotoxins in food. Int J Environ Res Public Health 14:632. https://doi.org/10.3390/ijerph14060632
Altalhi AD, El-Deeb B (2009) Localization of zearalenone detoxification gene(s) in pZEA-1 plasmid of Pseudomonas putida ZEA-1 and expressed in Escherichia coli. J Hazard Mater 161:1166–1172. https://doi.org/10.1016/j.jhazmat.2008.04.068
doi: 10.1016/j.jhazmat.2008.04.068
pubmed: 18513857
Azam MS, Yu D, Liu N, Wu A (2019) Degrading ochratoxin A and zearalenone mycotoxins using a multifunctional recombinant enzyme. Toxins (Basel) 11:301. https://doi.org/10.3390/toxins11050301
Bakos K, Kovács R, Staszny Á, Sipos DK, Urbányi B, Müller F, Csenki Z, Kovács B (2013) Developmental toxicity and estrogenic potency of zearalenone in zebrafish (Danio rerio). Aquat Toxicol 136–137:13–21. https://doi.org/10.1016/j.aquatox.2013.03.004
doi: 10.1016/j.aquatox.2013.03.004
pubmed: 23624394
Ben TF, Fedhila K, Chaieb K, Kouidhi B, Bakhrouf A, Abrunhosa L (2017) Adsorption of aflatoxin B1, zearalenone and ochratoxin A by microorganisms isolated from Kefir grains. Int J Food Microbiol 251:1–7. https://doi.org/10.1016/j.ijfoodmicro.2017.03.021
doi: 10.1016/j.ijfoodmicro.2017.03.021
Bergman A, Wenning L, Siewers V, Nielsen J (2018) Investigation of putative regulatory acetylation sites in Fas2p of Saccharomyces cerevisiae. BiO RXiV 46:1–44. https://doi.org/10.1101/430918
doi: 10.1101/430918
Bhat R, Rai RV, Karim AA (2010) Mycotoxins in food and feed: present status and future concerns. Compr Rev Food Sci Food Saf 9:57–81. https://doi.org/10.1111/j.1541-4337.2009.00094.x
doi: 10.1111/j.1541-4337.2009.00094.x
pubmed: 33467806
Bhatti SA, Khan MZ, Saleemi MK, Hassan ZU (2019) Impact of dietary Trichosporon mycotoxinivorans on ochratoxin A induced immunotoxicity. In Vivo Study Food Chem Toxicol 132:110696. https://doi.org/10.1016/j.fct.2019.110696
doi: 10.1016/j.fct.2019.110696
pubmed: 31344370
Bi K, Zhang W, Xiao Z, Zhang D (2018) Characterization, expression and application of a zearalenone degrading enzyme from Neurospora crassa. AMB Express 8:194. https://doi.org/10.1186/s13568-018-0723-z
Bin YS, Zheng HC, Xu JY, Zhao XY, Shu WJ, Li XM, Song H, Ma YH (2021) New biotransformation mode of zearalenone identified in Bacillus subtilis Y816 revealing a novel ZEN conjugate. J Agric Food Chem 69:7409–7419. https://doi.org/10.1021/acs.jafc.1c01817
doi: 10.1021/acs.jafc.1c01817
Bullerman LB, Bianchini A (2007) Stability of mycotoxins during food processing. Int J Food Microbiol 119:140–146. https://doi.org/10.1016/j.ijfoodmicro.2007.07.035
doi: 10.1016/j.ijfoodmicro.2007.07.035
pubmed: 17804104
Castells M, Marín S, Sanchis V, Ramos AJ (2005) Fate of mycotoxins in cereals during extrusion cooking: a review. Food Addit Contam 22:150–157. https://doi.org/10.1080/02652030500037969
doi: 10.1080/02652030500037969
pubmed: 15824005
Chang H, Kim W, Park JH, Kim D, Kim CR, Chung S, Lee C (2017) The occurrence of zearalenone in south korean feedstuffs between 2009 and 2016. Toxins (basel) 9:1–15. https://doi.org/10.3390/toxins9070223
doi: 10.3390/toxins9070223
Chang X, Liu H, Sun J, Wang J, Zhao C, Zhang W, Zhang J, Sun C (2020) Zearalenone removal from corn oil by an enzymatic strategy. Toxins (basel) 12:1–14. https://doi.org/10.3390/toxins12020117
doi: 10.3390/toxins12020117
Cheli F, Pinotti L, Rossi L, Dell’Orto V (2013) Effect of milling procedures on mycotoxin distribution in wheat fractions: a review. LWT - Food Sci Technol 54:307–314. https://doi.org/10.1016/j.lwt.2013.05.040
doi: 10.1016/j.lwt.2013.05.040
Chen Q, Lu Z, Hou W, Shi B, Shan A (2015) Effects of modified maifanite on zearalenone toxicity in female weaner pigs. Ital J Anim Sci 14:143–149. https://doi.org/10.4081/ijas.2015.3597
doi: 10.4081/ijas.2015.3597
Chen SW, Hsu JT, Chou YA, Wang HT (2018) The application of digestive tract lactic acid bacteria with high esterase activity for zearalenone detoxification. J Sci Food Agric 98:3870–3879. https://doi.org/10.1002/jsfa.8904
doi: 10.1002/jsfa.8904
pubmed: 29364505
Chen S, Pan L, Liu S, Pan L, Li X, Wang B (2021) Recombinant expression and surface display of a zearalenone lactonohydrolase from Trichoderma aggressivum in Escherichia coli. Protein Expr Purif 187:105933. https://doi.org/10.1016/j.pep.2021.105933
doi: 10.1016/j.pep.2021.105933
pubmed: 34273541
Chlebicz A (2019) 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 Antimicrob Proteins. https://doi.org/10.1007/s12602-018-9512-x
Cho KJ, Kang JS, Cho WT, Lee CH, Ha JK, Bin SK (2010) In vitro degradation of zearalenone by Bacillus subtilis. Biotechnol Lett 32:1921–1924. https://doi.org/10.1007/s10529-010-0373-y
doi: 10.1007/s10529-010-0373-y
pubmed: 20697929
Colombiana R, Pecuarias DC (2017) Efficacy of a yeast additive to mitigate the effects of zearalenone- contaminated feed in gilts. Rev Colomb Ciencias Pecu 30:299–307. https://doi.org/10.17533/udea.rccp.v30n4a05
Cserháti M, Kriszt B, Krifaton C, Szoboszlay S, Háhn J, Tóth S, Nagy I, Kukolya J (2013) Mycotoxin-degradation profile of Rhodococcus strains. Int J Food Microbiol 166:176–185. https://doi.org/10.1016/j.ijfoodmicro.2013.06.002
doi: 10.1016/j.ijfoodmicro.2013.06.002
pubmed: 23891865
Dänicke S, Winkler J (2015) Invited review: Diagnosis of zearalenone (ZEN) exposure of farm animals and transfer of its residues into edible tissues (carry over). Food Chem Toxicol 84:225–249. https://doi.org/10.1016/j.fct.2015.08.009
doi: 10.1016/j.fct.2015.08.009
pubmed: 26277628
Dänicke S, Swiech E, Buraczewska L, Ueberschär KH (2005) Kinetics and metabolism of zearalenone in young female pigs. J Anim Physiol Anim Nutr (berl) 89:268–276. https://doi.org/10.1111/j.1439-0396.2005.00516.x
doi: 10.1111/j.1439-0396.2005.00516.x
De MT, Devreese M, De BS, Van Ranst E, Eeckhout M, De BP, Croubels S (2015) Characterization of 27 mycotoxin binders and the relation with in vitro zearalenone adsorption at a single concentration. Toxins (basel) 7:21–33. https://doi.org/10.3390/toxins7010021
doi: 10.3390/toxins7010021
Demissie ZA, Foote SJ, Tan Y, Loewen MC (2018) Profiling of the transcriptomic responses of Clonostachys rosea upon treatment with Fusarium graminearum secretome. Front Microbiol 9:1–15. https://doi.org/10.3389/fmicb.2018.01061
doi: 10.3389/fmicb.2018.01061
Devreese M (2013) Development of in vitro and in vivo models for testing the efficacy of mycotoxin detoxifying agents and their possible interaction with oral absorption of veterinary drugs. Food Addit Contam 1:10–1080. https://doi.org/19440049.2012.671788
Deng T, Yuan QS, Zhou T, Guo LP, Jiang WK, Zhou SH, Yang CG, Kang CZ (2021) [Screening of zearalenonedegrading bacteria and analysis of degradation conditions]. Zhongguo Zhong Yao Za Zhi 46:5240–5246. https://doi.org/10.19540/j.cnki.cjcmm.20210716.101
Elaheh J (2016) Mycotoxin-induced toxicity; an updated mini-review on the current concepts. Immunopathol Persa 2:e11
El-nezami H, Polychronaki N, Salminen S, Mykka H (2002) Binding rather than metabolism may explain the interaction of two food-grade. Microbiology 68:3545–3549. https://doi.org/10.1128/AEM.68.7.3545
doi: 10.1128/AEM.68.7.3545
Eskola M, Kos G, Elliott CT, Hajšlová J, Mayar S, Krska R (2019) Worldwide contamination of food-crops with mycotoxins: validity of the widely cited ‘FAO estimate’ of 25%. Crit Rev Food Sci Nutr 0:1–17. https://doi.org/10.1080/10408398.2019.1658570
Fandohan P, Zoumenou D, Hounhouigan DJ, Marasas WFO, Wingfield MJ, Hell K (2005) Fate of aflatoxins and fumonisins during the processing of maize into food products in Benin. Int J Food Microbiol 98:249–259. https://doi.org/10.1016/j.ijfoodmicro.2004.07.007
doi: 10.1016/j.ijfoodmicro.2004.07.007
pubmed: 15698686
Fandohan P, Ahouansou R, Houssou P, Hell K, Marasas WFO, Wingfield MJ (2006) Impact of mechanical shelling and dehulling on Fusarium infection and fumonisin contamination in maize. Food Addit Contam 23:415–421. https://doi.org/10.1080/02652030500442516
doi: 10.1080/02652030500442516
pubmed: 16546888
Fleck SC, Churchwell MI, Doerge DR (2017) Metabolism and pharmacokinetics of zearalenone following oral and intravenous administration in juvenile female pigs. Food Chem Toxicol 106:193–201. https://doi.org/10.1016/j.fct.2017.05.048
doi: 10.1016/j.fct.2017.05.048
pubmed: 28552786
Frizzell C, Uhlig S, Miles CO, Verhaegen S, Elliott CT, Eriksen GS, Sørlie M, Ropstad E, Connolly L (2015) Biotransformation of zearalenone and zearalenols to their major glucuronide metabolites reduces estrogenic activity. Toxicol Vitr 29:575–581. https://doi.org/10.1016/j.tiv.2015.01.006
doi: 10.1016/j.tiv.2015.01.006
Fu G, Ma J, Wang L, Yang X, Liu J, Zhao X (2016) Effect of degradation of zearalenone-contaminated feed by Bacillus licheniformis CK1 on postweaning female piglets. Toxins (basel) 8:1–11. https://doi.org/10.3390/toxins8100300
doi: 10.3390/toxins8100300
Gaje M, Da M, Mróz M (2013) The effect of low doses of zearalenone and its metabolites on progesterone and 17 b -estradiol concentrations in peripheral blood and body weights of pre-pubertal female Beagle dogs. Toxicon 76:260–269. https://doi.org/10.1016/j.toxicon.2013.08.060
doi: 10.1016/j.toxicon.2013.08.060
Gao X, Sun L, Zhang N, Li C, Zhang J, Xiao Z, Qi D (2017) Gestational zearalenone exposure causes reproductive and developmental toxicity in pregnant rats and female offspring. Toxins (Basel) 9:21. https://doi.org/10.3390/toxins9010021
Garcia SO, Feltrin ACP, Garda-Buffon J (2018) Zearalenone reduction by commercial peroxidase enzyme and peroxidases from soybean bran and rice bran. Food Addit Contam - Part A Chem Anal Control Expo Risk Assess 35:1819–1831. https://doi.org/10.1080/19440049.2018.1486044
doi: 10.1080/19440049.2018.1486044
pubmed: 29889651
Giordano A, Denzoin L, Soraci AL, Tapia MO, Ross R, Apás A, González SN (2017) Zearalenone adsorption capacity of lactic acid bacteria isolated from pigs. Brazilian J Microbiol 48:715–723. https://doi.org/10.1016/j.bjm.2017.05.001
doi: 10.1016/j.bjm.2017.05.001
Gonçalves A, Gkrillas A, Dorne JL, Dall’Asta C, Palumbo R, Lima N, Battilani P, Venâncio A, Giorni P (2019) Pre- and postharvest strategies to minimize mycotoxin contamination in the rice food chain. Compr Rev Food Sci Food Saf 18:441–454. https://doi.org/10.1111/1541-4337.12420
doi: 10.1111/1541-4337.12420
pubmed: 33336939
González Pereyra ML, Di Giacomo AL, Lara AL, Martínez MP, Cavaglieri L (2020) Aflatoxin-degrading Bacillus sp. strains degrade zearalenone and produce proteases, amylases and cellulases of agro-industrial interest. Toxicon 180:43–48. https://doi.org/10.1016/j.toxicon.2020.04.006
doi: 10.1016/j.toxicon.2020.04.006
pubmed: 32298663
Greco MV, Franchi ML, Rico Golba SL, Pardo AG, Pose GN (2014) Mycotoxins and mycotoxigenic fungi in poultry feed for food-producing animals. Sci World J 2014:9. https://doi.org/10.1155/2014/968215
Harkai P, Szabó I, Cserháti M, Krifaton C, Risa A, Radó J, Balázs A, Berta K, Kriszt B (2016) Biodegradation of aflatoxin-B1 and zearalenone by Streptomyces sp. collection. Int Biodeterior Biodegrad 108:48–56. https://doi.org/10.1016/j.ibiod.2015.12.007
doi: 10.1016/j.ibiod.2015.12.007
Hathout AS, Aly SE (2014) Biological detoxification of mycotoxins: a review. Ann Microbiol 64:905–919. https://doi.org/10.1007/s13213-014-0899-7
doi: 10.1007/s13213-014-0899-7
He X, Gu W, Sun Y, Li Y, Sun X (2015) Evaluation of reduced toxicity of zearalenone as measured by the Hep G2 cell assay on degradation enzymes. Food Control 57:161–168. https://doi.org/10.1016/j.foodcont.2015.03.031
Hennig-Pauka I, Koch FJ, Schaumberger S, Woechtl B, Novak J, Sulyok M, Nagl V (2018) Current challenges in the diagnosis of zearalenone toxicosis as illustrated by a field case of hyperestrogenism in suckling piglets. Porc Heal Manag 4:1–9. https://doi.org/10.1186/s40813-018-0095-4
doi: 10.1186/s40813-018-0095-4
Hojnik N, Cvelbar U, Tavčar-Kalcher G, Walsh JL, Križaj I (2017) Mycotoxin decontamination of food: cold atmospheric pressure plasma versus “classic” decontamination. Toxins (Basel) 9:151. https://doi.org/10.3390/toxins9050151
Hsu TC, Yi PJ, Lee TY, Liu JR (2018) Probiotic characteristics and zearalenone-removal ability of a Bacillus licheniformis strain. PLoS ONE 13:1–18. https://doi.org/10.1371/journal.pone.0194866
doi: 10.1371/journal.pone.0194866
Hu J, Chen F, Kan T, Zhuang H, Zhang J, Han X (2017) Inhibition of fusarium solani infection in murine keratocytes by Lactobacillus salivarius ssp. salivarius JCM1231 Culture Filtrate In Vitro. Curr Eye Res 42:1339–1347. https://doi.org/10.1080/02713683.2017.1317816
doi: 10.1080/02713683.2017.1317816
pubmed: 28636459
Huang W, Chang J, Wang P, Liu C, Yin Q, Zhu Q, Lu F, Gao T (2018) Effect of the combined compound probiotics with mycotoxin–degradation enzyme on detoxifying aflatoxin B1 and zearalenone. J Toxicol Sci 43:377–385. https://doi.org/10.2131/jts.43.377
doi: 10.2131/jts.43.377
pubmed: 29877214
Huang W, Chang J, Wang P, Liu C, Yin Q, Song A, Gao T, Dang X, Lu F (2019) Effect of compound probiotics and mycotoxin degradation enzymes on alleviating cytotoxicity of swine jejunal epithelial cells induced by aflatoxin b 1 and zearalenone. Toxins 11:1–13. https://doi.org/10.3390/toxins11010012
doi: 10.3390/toxins11010012
Hui R, Hu X, Liu W, Liu W, Zheng Y, Chen Y, Guo RT, Jin J, Chen CC (2017) Characterization and crystal structure of a novel zearalenone hydrolase from Cladophialophora bantiana. Acta Crystallogr Sect Struct Biol Commun 73:515–519. https://doi.org/10.1107/S2053230X17011840
doi: 10.1107/S2053230X17011840
Jard G, Liboz T, Mathieu F, Guyonvarc’ HA, André F, Delaforge M, Lebrihi A (2010) Transformation of zearalenone to zearalenone-sulfate by Aspergillus spp. World Mycotoxin J 3:183–191. https://doi.org/10.3920/WMJ2009.1184
doi: 10.3920/WMJ2009.1184
Jebali R, Abbès S, Ben S-A, Ben YR, Haous Z, Oueslati R (2015) Ability of Lactobacillus plantarum MON03 to mitigate aflatoxins (B1 and M1) immunotoxicities in mice. J Immunotoxicol 12:290–299. https://doi.org/10.3109/1547691X.2014.973622
doi: 10.3109/1547691X.2014.973622
pubmed: 25441623
Ji C, Fan Y, Zhao L (2016) Review on biological degradation of aflatoxin, zearalenone and deoxynivalenol. Anim Nutr J 2:127–133. https://doi.org/10.1016/j.aninu.2016.07.003
Jones DP (2008) Radical-free biology of oxidative stress. Am J Physiol - Cell Physiol 295:849–68. https://doi.org/10.1152/ajpcell.00283.2008
Kaushik G (2015) Effect of processing on mycotoxin content in grains. Crit Rev Food Sci Nutr 55:1672–1683. https://doi.org/10.1080/10408398.2012.701254
doi: 10.1080/10408398.2012.701254
pubmed: 24915313
Keller L, Abrunhosa L, Keller K, Rosa CA, Cavaglieri L, Venâncio A (2015) Zearalenone and its derivatives α-zearalenol and β-zearalenol decontamination by Saccharomyces cerevisiae strains isolated from bovine forage. Toxins (Basel) 7:3297–308. https://doi.org/10.3390/toxins7083297
Khatibi PA, Berger G, Wilson J, Brooks WS, McMaster N, Griffey CA, Hicks KB, Nghiem NP, Schmale DG (2014) A comparison of two milling strategies to reduce the mycotoxin deoxynivalenol in barley. J Agric Food Chem 62:4204–4213. https://doi.org/10.1021/jf501208x
doi: 10.1021/jf501208x
pubmed: 24735088
Kim SH, Vujanovic V (2017) Biodegradation and biodetoxification of Fusarium mycotoxins by Sphaerodes mycoparasitica. sAMB Expres 7:1–9. https://doi.org/10.1186/s13568-017-0446-6
doi: 10.1186/s13568-017-0446-6
Kosawang C, Karlsson M, Jensen DF, Dilokpimol A, Collinge DB (2014) Transcriptomic profiling to identify genes involved in Fusarium mycotoxin Deoxynivalenol and Zearalenone tolerance in the mycoparasitic fungus Clonostachys rosea. BMC Genomics 15:55. http://www.biomedcentral.com/1471-2164/15/55
Kouadio JH, Mobio A, Baudrimont I, Moukha S (2005) Comparative study of cytotoxicity and oxidative stress induced by deoxynivalenol, zearalenone or fumonisin B1 in human intestinal cell line Caco-2. Toxicology 213:56–65. https://doi.org/10.1016/j.tox.2005.05.010
doi: 10.1016/j.tox.2005.05.010
pubmed: 16019124
Kouadio KN, Ouattara A, Coast I (2008) Taxonomic diversity and structure of benthic macroinvertebrates in aby lagoon (Ivory Coast, West Africa). Pakistan J Biol Sci 11:2224–30. https://doi.org/10.3923/pjbs.2008.2224.2230
Krifaton C, Kriszt B, Risa A, Szoboszlay S, Cserháti M, Harkai P, Eldridge M, Wang J, Kukolya J (2013) Application of a yeast estrogen reporter system for screening zearalenone degrading microbes. J Hazard Mater 244–245:429–435. https://doi.org/10.1016/j.jhazmat.2012.11.063
doi: 10.1016/j.jhazmat.2012.11.063
pubmed: 23274943
Kriszt R, Krifaton C, Szoboszlay S, Cserhati M, Kriszt B, Kukolya J, Czeh A, Feher-Toth S, Torok L, Szoke Z, Kovacs KJ, Terez Barna SF (2012) A new zearalenone biodegradation strategy using non- pathogenic Rhodococcus pyridinivorans K408 Strain. PLoS ONE 7:1–9. https://doi.org/10.1371/journal.pone.0043608
doi: 10.1371/journal.pone.0043608
Lee A, Cheng K, Liu J (2017) Isolation and characterization of a Bacillus amyloliquefaciens strain with zearalenone removal ability and its probiotic potential. PLoS One 12:e0182220. https://doi.org/10.1371/journal.pone.0182220
Lei YP, Zhao LH, Ma QG, Zhang JY, Zhou T, Gao CQ, Ji C (2014) Degradation of zearalenone in swine feed and feed ingredients by Bacillus subtilis. World Mycotoxin J 7:3920. https://doi.org/10.3920/WMJ2013.1623
doi: 10.3920/WMJ2013.1623
Liu RJ, Ping JY, Cheng KP (2011) Isolation and characterization of a Bacillus licheniformis strain capable of degrading zearalenone. World J Microbiol Biotechnol 27:1035–1043. https://doi.org/10.1007/s11274-010-0548-7
Liu K, Sun X, Feng Y, Cheng S, Li B, Li Y, Shen W, Li L (2017) The impact of Zearalenone on the meiotic progression and primordial follicle assembly during early oogenesis. Toxicol Appl Pharmacol 329:9–17. https://doi.org/10.1016/j.taap.2017.05.024
doi: 10.1016/j.taap.2017.05.024
pubmed: 28552778
Liu XL, Wu RY, Sun XF, Cheng SF, Zhang RQ, Zhang TY, Zhang XF, Zhao Y, Shen W, Li L (2018) Mycotoxin zearalenone exposure impairs genomic stability of swine follicular granulosa cells in vitro. Int J Biol Sci 14:294–305. https://doi.org/10.7150/ijbs.23898
doi: 10.7150/ijbs.23898
pubmed: 29559847
pmcid: 5859475
Liu P, Li J, Deng Z (2013) Bio-transformation of agri-food wastes by newly isolated Neurospora crassa and Lactobacillus plantarum for egg production. Poult Sci Assoc Inc 95:684–693. https://doi.org/10.3382/ps/pev357
Loi M, Fanelli F, Teresa M, Mirabelli V, Haidukowski M, Logrieco AF, Caliandro R, Mule G (2018) In vitro single and combined mycotoxins degradation by Ery4 laccase from Pleurotus eryngii and redox mediators. Food Control 90:401–406. https://doi.org/10.1016/j.foodcont.2018.02.032
doi: 10.1016/j.foodcont.2018.02.032
Loi M, Fanelli F, Liuzzi VC, Logrieco AF, Mulè G (2017) Mycotoxin biotransformation by native and commercial enzymes: present and future perspectives. Toxins (Basel) 9:111. https://doi.org/10.3390/toxins9040111
Long C, Long C, Amoasii L, Mireault AA, Mcanally JR, Li H, Sanchez- E, Bhattacharyya S, Shelton JM, Bassel-duby R, Olson EN (2015) Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351:400–403. https://doi.org/10.1126/science.aad5725
Lyagin I, Efremenko E (2019) Enzymes for detoxification of various mycotoxins: origins and mechanisms of catalytic action. Molecules 24:1–39. https://doi.org/10.3390/molecules24132362
doi: 10.3390/molecules24132362
Malekinejad H (2005) Bioactivation of zearalenone by porcine hepatic biotransformation Original article Bioactivation of zearalenone by porcine hepatic biotransformation. Vet Res 6:799–810. https://doi.org/10.1051/vetres
Matumba L, Van Poucke C, Njumbe Ediage E, Jacobs B, De Saeger S (2015) Effectiveness of hand sorting, flotation/washing, dehulling and combinations thereof on the decontamination of mycotoxin-contaminated white maize. Food Addit Contam - Part A Chem Anal Control Expo Risk Assess 32:960–969. https://doi.org/10.1080/19440049.2015.1029535
doi: 10.1080/19440049.2015.1029535
pubmed: 25785488
McCormick SP (2013) Microbial detoxification of mycotoxins. J Chem Ecol 39:907–918. https://doi.org/10.1007/s10886-013-0321-0
doi: 10.1007/s10886-013-0321-0
pubmed: 23846184
Metzler M, Pfeiffer E, Hildebrand AA (2010) Zearalenone and its metabolites as endocrine disrupting chemicals. World Mycotoxin Journal 3:385–401. https://doi.org/10.3920/WMJ2010.1244
Minervini F, Aquila MED (2008) Zearalenone and reproductive function in farm animals. Int J Mol Sci 9:2570–2584. https://doi.org/10.3390/ijms9122570
doi: 10.3390/ijms9122570
pubmed: 19330093
pmcid: 2635636
Minervini F, Giannoccaro A, Fornelli F, Dell’Aquila ME, Minoia P, Visconti A (2006) Influence of mycotoxin zearalenone and its derivatives (alpha and beta zearalenol) on apoptosis and proliferation of cultured granulosa cells from equine ovaries. Reprod Biol Endocrinol 4:1–9. https://doi.org/10.1186/1477-7827-4-62
doi: 10.1186/1477-7827-4-62
Nygren K, Dubey M, Zapparata A, Iqbal M, Tzelepis GD, Durling MB, Jensen DF, Karlsson M (2018) The mycoparasitic fungus Clonostachys rosea responds with both common and specific gene expression during interspecific interactions with fungal prey. Evol Appl 11:931–949. https://doi.org/10.1111/eva.12609
doi: 10.1111/eva.12609
pubmed: 29928301
pmcid: 5999205
Pan Y, Liu C, Yang J, Tang Y (2022) Conversion of zearalenone to β-zearalenol and zearalenone-14,16-diglucoside by Candida parapsilosis ATCC 7330. Food Control 131:108429. https://doi.org/10.1016/j.foodcont.2021.108429
doi: 10.1016/j.foodcont.2021.108429
Pang J, Zhou Q, Sun X, Li L, Zhou B, Zeng F, Zhao Y, Shen W, Sun Z (2017) Effect of low-dose zearalenone exposure on reproductive capacity of male mice. Toxicol Appl Pharmacol 333:60–67. https://doi.org/10.1016/j.taap.2017.08.011
doi: 10.1016/j.taap.2017.08.011
pubmed: 28837831
Peng WX, Marchal JLM, van der Poel AFB (2018) Strategies to prevent and reduce mycotoxins for compound feed manufacturing. Anim Feed Sci Technol 237:129–153. https://doi.org/10.1016/j.anifeedsci.2018.01.017
doi: 10.1016/j.anifeedsci.2018.01.017
Pierides M, El-Nezami H, Peltonen K, Salminen S, Ahokas J (2000) Ability of dairy strains of lactic acid bacteria to bind aflatoxin M1 in a food model. J Food Prot 63:645–650. https://doi.org/10.4315/0362-028X-63.5.645
doi: 10.4315/0362-028X-63.5.645
pubmed: 10826723
Pistol GC, Braicu C, Motiu M, Gras MA, Marin E, Stancu M, Calin L, Israel-roming F (2015) Zearalenone mycotoxin affects immune mediators, MAPK signalling molecules, nuclear receptors and genome-wide gene expression in pig spleen. Plos One 10:1–23. https://doi.org/10.1371/journal.pone.0127503
Qin X, Xin Y, Su X, Wang X, Wang Y, Zhang J, Tu T, Yao B, Luo H, Huang H (2021) Efficient degradation of zearalenone by dye-decolorizing peroxidase from streptomyces thermocarboxydus combining catalytic properties of manganese peroxidase and laccase. Toxins (Basel) 13:602. https://doi.org/10.3390/toxins13090602
Ratnaseelan AM, Tsilioni I, Theoharides TC (2018) Effects of mycotoxins on neuropsychiatric symptoms and immune processes. Clin Ther 40:903–917. https://doi.org/10.1016/j.clinthera.2018.05.004
doi: 10.1016/j.clinthera.2018.05.004
pubmed: 29880330
Ren ZH, Deng HD, Wang YC, Deng JL, Zuo ZC, Wang Y, Peng X, Cui HM, Fang J, Yu SM, Shen LH, Hu YC (2016) The Fusarium toxin zearalenone and deoxynivalenol affect murine splenic antioxidant functions, interferon levels , and T-cell subsets 41:195–200. https://doi.org/10.1016/j.etap.2015.12.007
Risa A, Krifaton C, Kukolya J, Kriszt B, Cserháti M, Táncsics A (2018) Aflatoxin B1 and zearalenone-detoxifying profile of Rhodococcus type strains. Curr Microbiol 75:907–917. https://doi.org/10.1007/s00284-018-1465-5
doi: 10.1007/s00284-018-1465-5
pubmed: 29511873
Saleemi MK, Khan MZ, Khan A, Javed I, Ul Hasan Z, Hameed MR, Hameed S, Mehmood MA (2012) Occurrence of toxigenic fungi in maize and maize-gluten meal from Pakistan. Phytopathol Mediterr 51:219–224. https://doi.org/10.14601/Phytopathol_Mediterr-9858
doi: 10.14601/Phytopathol_Mediterr-9858
Saleemi MK, Ashraf K, Gul ST, Naseem MN, Sajid MS, Mohsin M, He C, Zubair M, Khan A (2020) Toxicopathological effects of feeding aflatoxins B1 in broilers and its ameliosration with indigenous mycotoxin binder. Ecotoxicol Environ Saf 187:109712. https://doi.org/10.1016/j.ecoenv.2019.109712
doi: 10.1016/j.ecoenv.2019.109712
pubmed: 31654867
Salem IB, Boussabbeh M, Neffati F, Najjar MF, Bacha H (2016) Zearalenone-induced changes in biochemical parameters, oxidative stress and apoptosis in cardiac tissue : protective role of crocin. Toxicol 35: 623–634. https://doi.org/10.1177/0960327115597467
Keith Scudamore, Harry Baillie, Sue Patel SGE (2007) The occurrence and fate of fusarium mycotoxins during the commercial processing of oats in the UK. Food Addit Contam 24:1374–1385. https://doi.org/10.1080/02652030701509972
Shuping DSS, Eloff JN (2017) The use of plants to protect plants and food against fungal pathogens: a review. African J Tradit Complement Altern Med AJTCAM 14:120–127. https://doi.org/10.21010/ajtcam.v14i4.14
doi: 10.21010/ajtcam.v14i4.14
Song Y, Wang Y, Guo Y, Qiao Y, Ma Q, Ji C, Zhao L (2021) Degradation of zearalenone and aflatoxin B1 by Lac2 from Pleurotus pulmonarius in the presence of mediators. Toxicon 201:1–8. https://doi.org/10.1016/j.toxicon.2021.08.003
doi: 10.1016/j.toxicon.2021.08.003
pubmed: 34391788
Sun X, He X, Li Y, Xu D, Qian H (2014) Biological detoxification of zearalenone by Aspergillus niger strain FS10. FOOD Chem Toxicol 72:76–82. https://doi.org/10.1016/j.fct.2014.06.021
doi: 10.1016/j.fct.2014.06.021
pubmed: 25007785
Sun J, Xia Y, Ming D (2020) Whole-genome sequencing and bioinformatics analysis of apiotrichum mycotoxinivorans: predicting putative zearalenone-degradation enzymes. Front Microbiol 11:1–12. https://doi.org/10.3389/fmicb.2020.01866
doi: 10.3389/fmicb.2020.01866
Szente L, Milkos P, Sandor KM, Nikolett S, Tamas K, Beata PL (2015) Interactions of zearalenone with native and chemically modified cyclodextrins and their potential utilization. J Photochem Photobiol B Biol 151:63–68. https://doi.org/10.1016/j.jphotobiol.2015.07.009
Takahashi-Ando N, Ohsato S, Shibata T, Hamamoto H, Yamaguchi I, Kimura M (2004) Metabolism of zearalenone by genetically modified organisms expressing the detoxification gene from Clonostachys rosea. Appl Environ Microbiol 70:3239–3245. https://doi.org/10.1128/AEM.70.6.3239-3245.2004
doi: 10.1128/AEM.70.6.3239-3245.2004
pubmed: 15184117
pmcid: 427733
Tan H, Hu Y, He J, Wu L, Liao F (2014) Zearalenone degradation by two Pseudomonas strains from soil. Mycotoxin Res. https://doi.org/10.1007/s12550-014-0199-x
doi: 10.1007/s12550-014-0199-x
pubmed: 25488508
Tang Y, Xiao J, Chen Y, Yu Y, Xiao X, Yu Y, Wu H (2013) Secretory expression and characterization of a novel peroxiredoxin for zearalenone detoxification in Saccharomyces cerevisiae. Microbiol Res 168:6–11. https://doi.org/10.1016/j.micres.2012.08.002
doi: 10.1016/j.micres.2012.08.002
pubmed: 23036477
Tang Y, Liu C, Yang J, Peng X (2022) A novel enzyme synthesized by Acinetobacter sp. SM04 is responsible for zearalenone biodegradation. Biosci Biotechnol Biochem 86:209–216. https://doi.org/10.1093/bbb/zbab204
doi: 10.1093/bbb/zbab204
pubmed: 34864831
Taylor P, Yiannikouris A, Kettunen H, Apajalahti J, Pennala E, Moran CA (2013) Comparison of the sequestering properties of yeast cell wall extract and hydrated sodium calcium aluminosilicate in three in vitro models accounting for the animal physiological bioavailability of zearalenone. Food Addit Contam 30:1641–1650. https://doi.org/10.1080/19440049.2013.809625
Turcotte JC, Hunt PJB, Blaustein JD (2005) Estrogenic effects of zearalenone on the expression of progestin receptors and sexual behavior in female rats. Horm Behav 47:178–184. https://doi.org/10.1016/j.yhbeh.2004.09.005
Van Der Westhuizen L, Shephard GS, Burger HM, Rheeder JP, Gelderblom WCA, Wild CP, Gong YY (2011) Fumonisin B1 as a urinary biomarker of exposure in a Maize intervention study among South African subsistence farmers. Cancer Epidemiol Biomarkers Prev 20:483–489. https://doi.org/10.1158/1055-9965.EPI-10-1002
doi: 10.1158/1055-9965.EPI-10-1002
pubmed: 21266524
Vekiru E, Hametner C, Mitterbauer R, Rechthaler J, Adam G, Schatzmayr G, Krska R, Schuhmacher R (2010) Cleavage of zearalenone by trichosporon mycotoxinivorans to a novel nonestrogenic metabolite7. Appl Environ Microbiol 76:2353–2359. https://doi.org/10.1128/AEM.01438-09
doi: 10.1128/AEM.01438-09
pubmed: 20118365
pmcid: 2849244
Wan MLY, Turner PC, Allen KJ, El-nezami H (2016) Lactobacillus rhamnosus GG modulates intestinal mucosal barrier and inflammation in mice following combined dietary exposure to deoxynivalenol and zearalenone Lactobacillus rhamnosus GG modulates intestinal mucosal barrier and inflammation in mice followi. J Funct Foods 22:34–43. https://doi.org/10.1016/j.jff.2016.01.014
Wang M, Yin L, Hu H, Selvaraj JN, Zhou Y, Zhang G (2018) Expression, functional analysis and mutation of a novel neutral zearalenone-degrading enzyme. Int J Biol Macromol 118:1284–1292. https://doi.org/10.1016/j.ijbiomac.2018.06.111
doi: 10.1016/j.ijbiomac.2018.06.111
pubmed: 29949749
Wang N, Li P, Pan J, Wang M, Long M, Zang J, Yang S (2018) Bacillus velezensis A2 fermentation exerts a protective effect on renal injury induced by Zearalenone in mice. Sci Rep 8:1–14. https://doi.org/10.1038/s41598-018-32006-z
doi: 10.1038/s41598-018-32006-z
Wang Y, Zhang J, Wang Y, Wang K, Wei H, Shen L (2018) Isolation and characterization of the Bacillus cereus BC7 strain, which is capable of zearalenone removal and intestinal flora modulation in mice. Toxicon 155:9–20. https://doi.org/10.1016/j.toxicon.2018.09.005
doi: 10.1016/j.toxicon.2018.09.005
pubmed: 30267721
Wang Y, Zhao C, Zhang D, Zhao M, Zheng D, Peng M, Cheng W, Guo P, Cui Z (2018) Simultaneous degradation of aflatoxin B1 and zearalenone by a microbial consortium. Toxicon 146:69–76. https://doi.org/10.1016/j.toxicon.2018.04.007
doi: 10.1016/j.toxicon.2018.04.007
pubmed: 29621525
Wang Z, Bu Y, Zhao Y, Zhang Z, Liu L, Zhou H (2018e) Morphology-tunable tellurium nanomaterials produced by the tellurite-reducing bacterium Lysinibacillus sp. ZYM-1. Environ Sci Pollut Res 25:20756–20768. https://doi.org/10.1007/s11356-018-2257-y
Wang Y, Wang G, Dai Y, Wang Y, Lee YW, Shi J, Xu J (2020) Biodegradation of deoxynivalenol by a novel microbial consortium. Front Microbiol 10:2964. https://doi.org/10.3389/fmicb.2019.02964
Xia Y, Wu Z, He R, Gao Y, Qiu Y, Cheng Q, Ma X, Wang Z (2021) Simultaneous degradation of two mycotoxins enabled by a fusion enzyme in food-grade recombinant Kluyveromyces lactis. Bioresour Bioprocess 8:1–11. https://doi.org/10.1186/s40643-021-00395-1
doi: 10.1186/s40643-021-00395-1
Xiang L, Wang Q, Zhou Y, Yin L, Zhang G, Ma Y (2016) High-level expression of a ZEN-detoxifying gene by codon optimization and biobrick in Pichia pastoris. Microbiol Res 193:48–56. https://doi.org/10.1016/j.micres.2016.09.004
doi: 10.1016/j.micres.2016.09.004
pubmed: 27825486
Xu J, Wang H, Zhu Z, Ji F, Yin X, Hong Q, Shi J (2016) Isolation and characterization of Bacillus amyloliquefaciens ZDS-1: exploring the degradation of zearalenone by Bacillus spp. Food Control 68:244–250. https://doi.org/10.1016/j.foodcont.2016.03.030
doi: 10.1016/j.foodcont.2016.03.030
Xu L, Sun X, Wan X, Li H, Yan F, Han R, Li H, Li Z, Tian Y, Liu X, Kang X, Wang Y (2020) Identification of a Bacillus amyloliquefaciens H6 thioesterase involved in zearalenone detoxification by transcriptomic analysis. J Agric Food Chem 68:10071–10080. https://doi.org/10.1021/acs.jafc.0c03954
doi: 10.1021/acs.jafc.0c03954
pubmed: 32815728
Yang WC, Hsu TC, Cheng KC, Liu JR (2017) Expression of the Clonostachys rosea lactonohydrolase gene by Lactobacillus reuteri to increase its zearalenone ‑ removing ability. Microb Cell Fact 16:69. https://doi.org/10.1186/s12934-017-0687-8
Yu Y, Wu H, Tang Y, Qiu L (2012) Cloning, expression of a peroxiredoxin gene from Acinetobacter sp. SM04 and characterization of its recombinant protein for zearalenone detoxification. Microbiol Res 167:121–126. https://doi.org/10.1016/j.micres.2011.07.004
doi: 10.1016/j.micres.2011.07.004
pubmed: 21885267
Yu Y, Qiu L, Wu H (2011a) Degradation of zearalenone by the extracellular extracts of Acinetobacter sp . SM04 liquid cultures. Biodegradation 22:613–622. https://doi.org/10.1007/s10532-010-9435-z
Yu Y, Qiu L, Wu H (2011b) Oxidation of zearalenone by extracellular enzymes from Acinetobacter sp . SM04 into smaller estrogenic products. World J Microbiol Biotechnol 27:2675–2681. https://doi.org/10.1007/s11274-011-0741-3
Zada S, Alam S, Al Ayoubi S, Shakeela Q, Nisa S, Niaz Z, Khan I, Ahmed W, Bibi Y, Ahmed S, Qayyum A (2021) Biological transformation of zearalenone by some bacterial isolates associated with ruminant and food samples. Toxins (Basel) 13. https://doi.org/10.3390/toxins13100712
Zatecka E, Ded L, Elzeinova F, Kubatova A, Dorosh A, Margaryan H, Dostalova P, Korenkova V, Hoskova K, Peknicova J (2014) Effect of zearalenone on reproductive parameters and expression of selected testicular genes in mice. Reprod Toxicol 45:20–30. https://doi.org/10.1016/j.reprotox.2014.01.003
doi: 10.1016/j.reprotox.2014.01.003
pubmed: 24412631
Zhang H, Dong M, Yang Q, Tibiru AM, Li J, Zhang X (2016) Biodegradation of zearalenone by Saccharomyces cerevisiae: possible involvement of ZEN responsive proteins of the yeast. J Proteomics 143: 416–423. https://doi.org/10.1016/j.jprot.2016.04.017
Zhang Z, Xu W, Wu H, Zhang W, Mu W (2019) Identification of a potent enzyme for the detoxification of zearalenone. J Agric Food Chem 68:376–383. https://doi.org/10.1021/acs.jafc.9b06223
Zhao L, Jin H, Lan J, Zhang R, Ren H, Zhang X, Yu G (2015) Detoxification of zearalenone by three strains of lactobacillus plantarum from fermented food invitro. Food Control 54:158–164. https://doi.org/10.1016/j.foodcont.2015.02.003
doi: 10.1016/j.foodcont.2015.02.003
Zheng W, Pan S, Wang G, Jun Y, Liu Q, Gu J, Yuan Y, Zhong X, Ping Z, Chun J (2016) Zearalenone impairs the male reproductive system functions via inducing structural and functional alterations of sertoli cells. Environ Toxicol Pharmacol 42:146–155. https://doi.org/10.1016/j.etap.2016.01.013
doi: 10.1016/j.etap.2016.01.013
pubmed: 26851377
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. Sci Total Environ 709:135897. https://doi.org/10.1016/J.SCITOTENV.2019.135897
doi: 10.1016/J.SCITOTENV.2019.135897
pubmed: 31887512
Zhu L, Yuan H, Guo C, Lu Y, Deng S, Yang Y, Wei Q, Wen L, He Z (2012) Zearalenone induces apoptosis and necrosis in porcine granulosa cells via a caspase-3- and caspase-9-dependent mitochondrial signaling pathway. J Cell Physiol 227:1814–1820. https://doi.org/10.1002/jcp.22906
doi: 10.1002/jcp.22906
pubmed: 21732350
Zhu C, Hou Y, Han J, Cui X, Kim N, Sun S (2014) Zearalenone exposure affects epigenetic modifications of mouse eggs. Mutagenesis 29:489–495. https://doi.org/10.1093/mutage/geu033
Zinedine A, Soriano JM, Man J, Molto JC (2007) Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone : an oestrogenic mycotoxin. Food Chem Toxicol 45:1–18. https://doi.org/10.1016/j.fct.2006.07.030
doi: 10.1016/j.fct.2006.07.030
pubmed: 17045381