Biocontrol of Occurrence Ochratoxin A in Wine: A Review
Abstract
:1. Introduction
2. OTA in Wine
Country | Type of Wine | OTA Detected/Total Samples | Samples over the EU Limit (2 ng mL−1) | Source |
---|---|---|---|---|
Argentina | Red | 4/47 | 3 | [51] |
Red | 136/136 | 0 | [52] | |
Brazil | Red | 18/26 | 0 | [53] |
White | 7/17 | 0 | ||
Chile | Red | 28/869 | 0 | [54] |
White | 6/319 | 0 | ||
China | Red | 183/183 | 0 | [55] |
White | 40/40 | 0 | ||
Croatia | Red | 7/7 | 0 | [42] |
White | 4/7 | 0 | ||
Red | 6/6 | 0 | [56] | |
White | 8/10 | 0 | ||
France | red grape most | 11/37 | 0 | [57] |
Greece | Red | 58/78 | 0 | [49] |
White | 40/62 | 0 | ||
Sweet | 6/10 | 0 | ||
Red | 33/104 | 1 | [58] | |
White | 55/118 | 0 | ||
Sweet | 7/10 | 0 | ||
Italy | Red | 14/96 | yes * | [46] |
Red | 553/735 | 22 | ||
White | 128/290 | 0 | [43] | |
Rose | 69/75 | 4 | ||
Desert | 18/28 | 0 | ||
Red | 29/20 | 0 | [48] | |
Sweet | 55/55 | 0 | [59] | |
Poland | Red | 49/53 | yes * | [60] |
Portugal | Red | 9/35 | 1 | [61] |
White | 3/25 | 0 | ||
South Africa | Red | 15/15 | 0 | [62] |
White | 9/9 | 0 | ||
Spain | Red | 34/140 | 2 | [50] |
White | 6/60 | 1 | ||
Sweet | 186/188 | 18 | [40] | |
USA | Red | 28/31 | 2 | [63] |
White | 7/10 | 0 |
3. Factors That Influence OTA Presence in Wines
4. In Field Prevention of OTA Contamination in Wine
5. Biocontrol of OTA Occurrence in Wine
5.1. Inhibition of the Fungi Responsible for OTA Biosynthesis
5.2. Effects of OTA on Bacteria and Yeasts
5.2.1. Effect of OTA on Bacteria
5.2.2. Effects of OTA on Yeasts
5.3. Adsorption of OTA
5.4. Degradation of OTA
Enzymatic Degradation of OTA
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Estereicher, S.K. The beginning of wine and viticulture. Phys. Status Solidi C 2017, 14, 1700008. [Google Scholar] [CrossRef]
- Rosso, A.M. Beer and wine in antiquity: Beneficial remedy or punishment imposed by the Gods? Acta Med.-Hist. Adriat. 2012, 10, 237–262. [Google Scholar] [PubMed]
- Chambers, P.J.; Pretorius, I.S. Fermenting knowledge: The history of wine making, science and yeast research. EMBO Rep. 2010, 11, 914–920. [Google Scholar] [CrossRef] [PubMed]
- OVI, International Organisation of Vine and Wine 2023. State of the World Vine and Wine Sector in 2022. Available online: https://www.oiv.int/sites/default/files/documents/2023_SWVWS_report_EN.pdf (accessed on 10 December 2023).
- Battilani, P.; Giorni, P.; Bertuzzi, T.; Formenti, S.; Pietri, A. Black Aspergilli and ochratoxin A in grapes in Italy. Int. J. Food Microbiol. 2006, 111, S53–S60. [Google Scholar] [CrossRef] [PubMed]
- Infantino, A.; Belocchi, A.; Quaranta, F.; Reverberi, M.; Beccaccioli, M.; Lombardi, D.; Vitale, M. Effects of climate change on the distribution of Fusarium spp. in Italy. Sci. Total Environ. 2023, 882, 163640. [Google Scholar] [CrossRef] [PubMed]
- Cervini, C.; Vercheecke Vassen, C.; Ferrara, M.G.; Garcia-Cela, E.; Magista, D.; Medina, A.; Gallo, A.; Perrone, G. Interracting climate change factors (CO2 and temperature cycles) on growth, secondary metabolites gene expression and phenotypic ochratoxin A by Aspergillus carbonarius strains on grape based matrix. Fungal Biol. 2021, 125, 115–122. [Google Scholar] [CrossRef] [PubMed]
- Akbar, A.; Medina, A.; Magan, N. Impact of interacting climate change factors on growth and ochratoxin A production by Aspergillus section Circumdati and Nigri species on coffee. World Mycotoxin J. 2016, 9, 863–874. [Google Scholar] [CrossRef]
- Bui-Klinke, T.R.; Wu, F. Ochratoxin A and human health risk: A review of the evidence. Crit. Rev. Food Sci. Nutr. 2015, 55, 1860–1869. [Google Scholar] [CrossRef] [PubMed]
- La Placa, L.; Tsitsigiannis, D.; Legieri, M.C.; Battilani, P. From grapes to wine: Impact of the vinification process on ochratoxin A contamination. Foods 2023, 12, 260. [Google Scholar] [CrossRef]
- van der Merwe, K.J.; Steyn, P.S.; Fourie, L.; Scott, D.B.; Theron, J.J. Ochratoxin A, a toxic metabolite produced by Aspergillus Ochraceus. Will. Nat. 1965, 205, 1112–1113. [Google Scholar] [CrossRef]
- Otteneder, H.; Majerus, P. Occurrence of ochratoxin A (OTA) in wines: Influence of the type of wine and its geographical origin. Food Addit. Contam. 2000, 17, 793–798. [Google Scholar] [CrossRef] [PubMed]
- Amezqueta, S.; Shorr-Galindo, S.; Murillo-Arbizu, M.; Gonzales-Pena, E.; Lopez de Certain, A.; Giraud, J.P. OTA producing fungi in foodstuff: A review. Food Control 2012, 26, 259–268. [Google Scholar] [CrossRef]
- IARC. Monographs on the Evaluation of Carcinogenic Risks to Humans: Some Naturally Occurring Substances: Food Items and Con-Stituents, Heterocyclic Aromatic Amines and Mycotoxins; IARC: Lyon, France, 1993; pp. 1–599. [Google Scholar]
- O’Brien, E.; Dietrich, D.R. Ochratoxin A: The continuing enigma. Crit. Rev. Toxicol. 2005, 35, 33–60. [Google Scholar] [CrossRef] [PubMed]
- Ding, L.; Han, M.; Wang, X.; Guo, Y. Ochratoxin A: Overview of prevention, removal and detoxification methods. Toxins 2023, 15, 565. [Google Scholar] [CrossRef] [PubMed]
- Stoev, S.D. Balkan Endemic Nephropathy—Still continuing enigma, risk assessment, and understanding the hazard of joint mycotoxin exposure of animals and humans. Chem. Biol. Interact. 2017, 261, 63–79. [Google Scholar] [CrossRef] [PubMed]
- Jelakovic, B.; Dika, Z.; Arlt, V.M.; Striborova, M.; Pavlovic, N.M.; Nikolic, J.; Colet, J.M.; Vanherwegen, J.L.; Nortier, J.L. Balkanic Endemic Nephropathy and Causative Role of Aristolochic Acid. Semin. Nephrol. 2019, 39, 284–296. [Google Scholar] [CrossRef] [PubMed]
- Ponsone, M.L.; Chiotta, M.L.; Combina, M.; Dalcero, A.M.; Chulze, S.N. Fate of ochratoxin A in Argentinean red wine during pilot scale vinification. Rev. Argent. 2009, 41, 245–250. [Google Scholar]
- Abraham, N.; Chan, E.T.S.; Zhou, T.; Seah, S.Y.K. Microbial detoxification of mycotoxins in food. Front. Microbiol. 2022, 13, 957148. [Google Scholar] [CrossRef] [PubMed]
- Petzinger, E.; Zeigler, K. Ochratoxin A from toxicological perspective. J. Vet. Pharmacol. Ther. 2000, 23, 91–98. [Google Scholar] [CrossRef]
- Duarte, S.C.; Lino, C.M.; Pena, A. Ochratoxin A in feed of food producing animals: An undesirable mycotoxin with health a performance effects. Vet. Microbiol. 2011, 1548, 1–13. [Google Scholar] [CrossRef]
- Munoz, K.; Blaskewicz, M.; Campos, V.; Vega, M.; Degen, G.H. Exposure of infants to ochratoxin A with breast milk. Arch. Toxicol. 2014, 88, 837–846. [Google Scholar] [CrossRef] [PubMed]
- Memis, E.Y.; Yalcin, S.S. Human milk mycotoxin contamination: Smoking exposure and breastfeeding problems. J. Matern.-Fetal Neonatal Med. 2021, 34, 31–40. [Google Scholar] [CrossRef] [PubMed]
- European Commission. Commission Regulation (EC) Number 1881/2006 of 19 December 2006 Setting Maximum Levels of Certain. Contaminants in Foodstuff; European Commission: Ispra, Italy, 2006. [Google Scholar]
- European Commission. Directive 2009/128/EC Aims to Achieve a Sustainable Use of Pesticides in the EU by Reducing the Risks and Impacts of Pesticide Use; European Commission: Ispra, Italy, 2009. [Google Scholar]
- Bhat, R.; Rai, R.V.; Karim, A.A. Mycotoxins in food and feed: Present status and future concerns. Compr. Rev. Food Sci. Food Saf. 2010, 9, 57–81. [Google Scholar] [CrossRef] [PubMed]
- Kumar, P.; Mahato, D.K.; Sharma, B.; Borah, R.; Haque, S.; Mahmud, M.M.C.; Shah, A.K.; Rawal, D.; Bora, H.; Bui, S. Ochratoxins in food and feed: Occurrence and its impact on human health and management strategies. Toxicon 2020, 187, 151–162. [Google Scholar] [CrossRef] [PubMed]
- Leblanc, J.C.; Tard, A.; Volatier, J.L.; Verger, P. Estimated dietary exposure to principal food mycotoxins from the first French total diet study. Food Addit. Contam. 2005, 22, 652–672. [Google Scholar] [CrossRef] [PubMed]
- Battilani, P.; Magan, N.; Logrieco, A. European research on ochratoxin A in grapes and wine. Int. J. Food Microbiol. 2006, 111, S2–S4. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization (WHO). Mycotoxins. 2023. Available online: https://www.who.int/news-room/fact-sheets/detail/mycotoxins (accessed on 30 November 2023).
- Barik, S.K.; Behera, M.D.; Shrotriya, S.; Likhovskoi, V. Monitoring climate change impacts on agriculture and forests: Trends and prospects. Environ. Monit. Assess. 2022, 195, 174. [Google Scholar] [CrossRef] [PubMed]
- Singh, B.K.; Delgado-Baquerizo, M.; Egidi, E.; Guirado, E.; Leach, J.E.; Liu, H.; Trivedi, P. Climate change impacts on plant pathogens, food security and paths forward. Nat. Rev. Microbiol. 2023, 21, 640–656. [Google Scholar] [CrossRef] [PubMed]
- Marchand, P.A. EU chemical plant protection products in 2023: Current state and perspectives. Agrochemicals 2023, 2, 106–117. [Google Scholar] [CrossRef]
- Vekemans, M.C.; Marchand, P.A. The fate of biocontrol agents under the European phytopharmaceutical regulation: How this regulation hinders the approval of botanicals as new active substances. Environ. Sci. Pollut. Res. 2020, 27, 39879–39887. [Google Scholar] [CrossRef]
- Loncar, J.; Bellich, B.; Parroni, A.; Reverberi, M.; Rizzo, R.; Zjalić, S.; Cescutti, P. Oligosaccharides Derived from Tramesan: Their Structure and Activity on Mycotoxin Inhibition in Aspergillus flavus and Aspergillus carbonarius. Biomolecules 2021, 11, 243. [Google Scholar] [CrossRef] [PubMed]
- Thomas, G.; Rusman, Q.; Morrison, W.R., 3rd; Magalhães, D.M.; Dowell, J.A.; Ngumbi, E.; Osei-Owusu, J.; Kansman, J.; Gaffke, A.; Pagadala Damodaram, K.J.; et al. Deciphering Plant-Insect-Microorganism Signals for Sustainable Crop Production. Biomolecules 2023, 13, 997. [Google Scholar] [CrossRef] [PubMed]
- Zimmerli, B.; Dick, R. Ochratoxin A in grape wine and grape-juice: Occurrence and risk assessment. Food Addit. Contam. 1996, 13, 665–668. [Google Scholar] [CrossRef] [PubMed]
- Lucchetta, G.; Bazzo, I.; Cortivo, G.D.; Stringher, L.; Bellotto, D.; Borgo, M.; Angelini, E. Occurrence of black Aspergilli and ochratoxin A on grapes in Italy. Toxins 2010, 2, 840–855. [Google Scholar] [CrossRef] [PubMed]
- Burdasal, P.; Legarda, T. Occurrence of ochratoxin A in sweet wines produced in Spain and other countries. Food Addit. Contam. 2007, 24, 976–986. [Google Scholar] [CrossRef] [PubMed]
- Freire, L.; Braga, P.A.C.; Furtado, M.M.; Delafiori, J.; Dias-Audibert, L.; Pereira, G.E.; Reyes, F.G.; Catharino, R.R.; Sant’Ana, A.S. From grape to wine: Fate of ochratoxin A during red, rose and white wine making process and of ochratoxin derivate in the final products. Food Control 2020, 113, 107167. [Google Scholar] [CrossRef]
- Domijan, A.M.; Peraica, M. Ochratoxin A in wine. Arh. Hig. Rada Toksikol. 2005, 56, 17–20. [Google Scholar] [PubMed]
- Brera, C.; Debegnach, F.; Minardi, V.; Prantera, E.; Pannunzi, E.; Faleo, S.; de Santis, B.; Miraglia, M. Ochratoxin A contamination in Italian wine samples and evaluation of the exposure in the Italian population. J. Agric. Food Chem. 2008, 56, 10611–10618. [Google Scholar] [CrossRef] [PubMed]
- Freire, L.; Passamani, F.R.; Thomas, A.B.; Nassur, R.C.; Silva, L.M.; Paschoal, F.N.; Pereira, G.E.; Prado, G.; Batista, L.R. Influence of physical and chemical characteristics of wine grapes on the incidence of Penicillium and Aspergillus fungi in grapes and ochratoxin A in wines. Int. J. Food Microbiol. 2017, 241, 181–190. [Google Scholar] [CrossRef]
- Freire, L.; Guerreiro, T.M.; Carames, E.T.S.; Lopes, L.S.; Orlando, E.A.; Pereira, G.E.; Pallone, J.A.L.; Catharino, R.R.; Sant’Ana, A.S. Influence of maturation stages in different varieties of wine grapes (Vitis vinifera) on the production of ochratoxin A and its modified forms by Aspergillus carbonarius and Aspergillus niger. J. Agric. Food Chem. 2018, 66, 8824–8831. [Google Scholar] [CrossRef]
- Pietri, A.; Bertuzzi, P.; Pallaroni, L.; Piva, G. Occurrence of ochratoxin A in Italian wines. Food Addit. Contam. 2001, 18, 647–654. [Google Scholar] [CrossRef] [PubMed]
- Clouvel, P.; Bonvarlet, L.; Martinez, A.; Lagouarde, P.; Dieng, I.; Martin, P. Wine contamination by ochratoxin A in relation to vine environment. Int. J. Food Microbiol. 2008, 123, 74–80. [Google Scholar] [CrossRef] [PubMed]
- Di Stefano, V.; Avellone, G.; Pintozzo, R.; Capocchiano, V.G.; Mazza, A.; Cicero, N.; Dugo, G. Natural co-occurrence of ochratoxin A, ochratoxin B and aflatoxins in Sicilian red wines. Food Addit. Contam. Part. A 2015, 32, 1343–1351. [Google Scholar] [CrossRef] [PubMed]
- Stefanaki, I.; Foufa, E.; Tsatsou-Dritsa, A.; Photis, D. Ochratoxin A concentration in Greek domestic vines and dried wine fruits. Food Addit. Contam. 2003, 20, 74–83. [Google Scholar] [CrossRef] [PubMed]
- Belli, N.; Marin, S.; Duaigues, A.; Ramos, A.J.; Sanchis, V. Ochratoxin A in wines, musts and grape juices from Spain. J. Sci. Food Agric. 2004, 84, 591–594. [Google Scholar] [CrossRef]
- Ponsone, M.L.; Chiotta, M.L.; Combina, M.; Torres, A.; Knass, P.; Dalcero, A.; Chulze, S. Natural occurrence of ochratoxin A in musts, wines and grape vine fruits from grapes harvested in Argentina. Toxins 2010, 2, 1984–1996. [Google Scholar] [CrossRef] [PubMed]
- Marino-Repizo, L.; Gargantini, R.; Manzano, H.; Raba, J.; Cerutti, S. Assesment of ochratoxin A occurrence in Argentinian red wines using a novel sensitive quichers-solid phase extraction approach prior to ultra high-performance liquid chromatography mass spectrometry methodology. J. Sci. Food Agric. 2017, 97, 2487–2497. [Google Scholar] [CrossRef] [PubMed]
- Kruger, C.D.; Fernandes, A.M.; Rosa, C.A. Ochratoxin A in wines from 2002 to 2008 harvest marketed in Rio de Janeiro, Brazil. Food Addit. Contam. Part B Surveill. 2012, 5, 204–207. [Google Scholar] [CrossRef]
- Vega, M.; Rios, G.; von Baer, D.; Marones, C.; Tessini, C.; Herlitz, E.; Saelzer, R.; Ruiz, M.A. Ochratoxin A occurrence in wines produced in Chile. Food Control 2012, 28, 147–150. [Google Scholar] [CrossRef]
- Zhong, Q.D.; Li, G.H.; Wang, D.B.; Shao, Y.; Li, J.G.; Xiong, Z.H.; Wu, Y.N. Exposure assessment to ochratoxin A in Chinese wine. J. Agric. Food Chem. 2014, 62, 8908–8913. [Google Scholar] [CrossRef]
- Peraica, M.; Flajs, D.; Domijan, A.M.; Ivic, D.; Cvjetkovic, B. Ochratoxin A contamination in food from Croatia. Toxins 2010, 2, 2098–2105. [Google Scholar] [CrossRef]
- Sage, L.; Garon, D.; Seigle-Morandi, F. Fungal microflora and ochratoxin A risk in French vineyards. J. Agric. Food Chem. 2004, 52, 5764–5768. [Google Scholar] [CrossRef]
- Labrinea, E.P.; Natskoulis, P.I.; Spiropoulus, A.E.; Magan, N.; Tassou, C.C. A survey of ochratoxin A occurrence in Greek wines. Food Addit. Contam. Part. B Surveill. 2011, 4, 4–6. [Google Scholar] [CrossRef]
- Di Stefano, V.; Pitonzo, R.; Avellone, G.; Di Fiore, A.; Monte, L.; Ogorka, A.Z.T. Determination of aflatoxin and ochratoxins in Sicilian weet wines by high-perfomance liquid chromatography with fluorometric detection and immunoaffinity clean up. Food Anal. Methods 2015, 8, 569–577. [Google Scholar] [CrossRef]
- Czerwiecki, L.; Wilczynska, G.; Kwiecien, A. Ochratoxin A: An improvement clean-up and HPLC method used to investigate wine and juice on Polish market. Food Addit. Contam. 2005, 22, 158–162. [Google Scholar] [CrossRef] [PubMed]
- Pena, A.; Cerejo, F.; Silva, L.; Lino, C. Ochratoxin A survey in Portuguese wine by LC-FD with direct injection. Talanta 2010, 82, 1556–1561. [Google Scholar] [CrossRef]
- Shephard, G.S.; Fabiani, A.; Stockenstom, S.; Mshicileli, N.; Sewram, V. Quantitation of ochratoxin A in South African wines. J. Agric. Food Chem. 2003, 51, 1102–1106. [Google Scholar] [CrossRef] [PubMed]
- De Jesus, C.L.; Bartley, A.; Welch, A.Z.; Berry, J.P. High incidence and levels of Ochratoxin A in wines sourced from United States. Toxins 2018, 10, 1. [Google Scholar] [CrossRef] [PubMed]
- Barata, A.; Malfeito-Ferreira, M.; Loureiro, V. The microbial ecology of wine grape berries. Int. J. Food Microbiol. 2012, 153, 243–259. [Google Scholar] [CrossRef]
- Mondani, L.; Palumbo, R.; Tsitsigiannis, D.; Perdikis, D.; Mazzoni, E.; Battilani, P. Pest management and ochratoxin A contamination in grapes: A review. Toxins 2020, 12, 303. [Google Scholar] [CrossRef]
- Visconti, F.; López, R.; Olego, M.Á. The Health of Vineyard Soils: Towards a Sustainable Viticulture. Horticulturae 2024, 10, 154. [Google Scholar] [CrossRef]
- Cozzi, G.; Haidukowski, M.; Perrone, G.; Visconti, A.; Logrieco, A. Influence of Lobesia botrana field control on black aspergilli rot and ochratoxin A contamination in grapes. J. Food Prot. 2009, 72, 894–897. [Google Scholar] [CrossRef] [PubMed]
- Cozzi, G.; Somma, S.; Haidukowski, M.; Logrieco, A.F. Ochratoxin A management in vineyards by Lobesia botrana biocontrol. Toxins 2013, 5, 49–59. [Google Scholar] [CrossRef] [PubMed]
- Mitchell, D.; Parra, R.; Alfred, D.; Magan, N. Water and temperature relations of growth and ochratoxin A production by Aspergillus carbonarius strains from grapes in Europe and Israel. J. Appl. Microbiol. 2004, 97, 439–445. [Google Scholar] [CrossRef] [PubMed]
- Passamani, F.R.; Hernandes, T.; Lopes, N.A.; Bastoc, S.C.; Santiago, W.D.; Cardoso, M.; Batista, L.R. Effect of temperature, water activity and pH on growth and production of ochratoxin A by Aspergillus niger and Aspergillus carbonarius from Brazilian grapes. J. Food Prot. 2014, 77, 1947–1952. [Google Scholar] [CrossRef] [PubMed]
- Visconti, A.; Perrone, G.; Cozzi, G.; Solfrizzo, M. Managing ochratoxin A risk in the grape-wine food chain. Food Addit. Contam. 2008, 25, 193–202. [Google Scholar] [CrossRef]
- Reverberi, M.; Gazzetti, K.; Punelli, F.; Scarpari, M.; Zjalic, S.; Ricelli, A.; Fabbri, A.A.; Fanelli, C. Aopyap1 regulates OTA synthesis by controlling cell redox balance in Aspergillus ochraceus. Appl. Microbiol. Biotechnol. 2012, 95, 1293–1304. [Google Scholar] [CrossRef]
- Crespo-Sempere, A.; Selma Lazaro, C.; Palumbo, J.D.; Gonzales-Candelas, L.; Martinez-Culebras, P.V. Effect of oxidants and phenolic antioxidants on the ochratoxigenic fungus Aspergillus carbonarius. J. Sci. Food Agric. 2015, 96, 169–177. [Google Scholar] [CrossRef] [PubMed]
- Ortiz-Villeda, B.; Lobos, O.; Aguilar-Zuniga, K.; Carrasco-Sanchez, V. Ochratoxins in wine: A review of their occurrence in the last decade, toxicity and exposure risk in humans. Toxins 2021, 13, 478. [Google Scholar] [CrossRef]
- Zjalic, S.; Frece, J.; Pavlovic, M.; Jakopovic, Z.; Markov, K. Procjena Rizika Kontaminacije Vina Okratoksinom A. Brošura za Vinare. (Croatian); Markov, K., Zjalic, S., Frece, J., Eds.; Sveučilište u Zadru: Zadar, Croatia, 2017; p. 48. ISBN 978-953-331-173-9. [Google Scholar]
- Tsolakis, H.; Corona, O.; Pulizzi, A.S.; Grippi, F.; Mondello, V. Incidence of grapevine moth Lobesia botrana (Den. & Schif.) on occurrence of ochratoxin A in grapes. In Integrated Protection in Viticulture; IOBC/WPRS Bulletin: Dijon, France, 2008; pp. 363–368. [Google Scholar]
- Wang, L.; Cai, R.; Zhang, J.; Liu, X.; Wang, S.; Ge, Q.; Zhao, Z.; Yue, T.; Yuan, Y.; Wang, Z. Removal of ochratoxin A in wine by Cryptococcus albidus and safety assessment of degradation products. J. Sci. Food Agric. 2023, 104, 2030–2037. [Google Scholar] [CrossRef]
- Farbo, M.G.; Urgeghe, P.P.; Fiori, S.; Marcello, A.; Oggiano, S.; Balmas, V.; Hassan, Z.U.; Jaoua, S.; Migheli, Q. Effect of yeast volatile organic compounds on ochratoxin A-producing Aspergillus carbonarius and A. ochraceus. Int. J. Food Microbiol. 2018, 284, 1–10. [Google Scholar] [CrossRef] [PubMed]
- Commission regulation (EU). No 2023/915 of 25 April 2023 on Maximum Levels of Certain Contaminants in Food and Replacing Regulation 2023. (EC) No 1881/2006. Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/PDF/?uri=CELEX:32023R0915 (accessed on 30 February 2024).
- Bhatnagar, D.E.E.P.A.K.; Ehrlich, K.C.; Cleveland, T.E. Handbook of Applied Mycology, 5th ed.; Marcel Dekker Inc.: New York, NY, USA, 1991; pp. 255–286. [Google Scholar]
- Loi, M.; Fanelli, F.; Liuzzi, V.C.; Logrieco, A.F.; Mulè, G. Mycotoxin Biotransformation by Native and Commercial Enzymes: Present and Future Perspectives. Toxins 2017, 9, 111. [Google Scholar] [CrossRef] [PubMed]
- Shetty, P.H.; Jespersen, L. Saccharomyces cerevisiae and lactic acid bacteria as potential mycotoxin decontamination agents. Trends Food Sci. Technol. 2006, 17, 48–55. [Google Scholar] [CrossRef]
- Petruzzi, L.; Bevilacqua, A.; Corbo, M.R.; Garofalo, C.; Baiano, A.; Sinigaglia, M. Selection of autochtonous Saccharomyces cerevisiae strains as wine starters using a polyphasic approach and ochratoxin A removal. J. Food Prot. 2014, 77, 1168–1177. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Wang, Q.; Wang, S.; Cai, R.; Yuan, Y.; Yue, T.; Wang, Z. Bio-control on the contamination of Ochratoxin A in food: Current research and future prospects. Curr. Res. Food Sci. 2022, 5, 1539–1549. [Google Scholar] [CrossRef] [PubMed]
- Shimizu, S.; Kataoka, M.; Honda, K.; Sakamoto, K. Lactone-ring-cleaving enzymes of microorganisms: Their diversity and applications. J. Biotechnol. 2001, 92, 187–194. [Google Scholar] [CrossRef] [PubMed]
- Abrunhosa, L.; Paterson, R.R.M.; Venâncio, A. Biodegradation of Ochratoxin A for Food and Feed Decontamination. Toxins 2010, 2, 1078–1099. [Google Scholar] [CrossRef]
- Li, S.; Marquardt, R.R.; Frohlich, A.A.; Vitti, T.G.; Crow, G. Pharmacokinetics of ochratoxin A and its metabolites in rats. Toxicol. Appl. Pharmacol. 1997, 145, 82–90. [Google Scholar] [CrossRef]
- Abrunhosa, L.; Serra, R.; Venâncio, A. Biodegradation of ochratoxin A by fungi isolated from grapes. J. Agric. Food Chem. 2002, 50, 7493–7496. [Google Scholar] [CrossRef]
- Abrunhosa, L.; Inês, A.; Rodrigues, A.I.; Guimarães, A.; Pereirab, V.L.; Parpot, P.; Mendes-Faia, A.; Venâncio, A. Biodegradation of ochratoxin A by Pediococcus parvulus isolated from Douro wines. Int. J. Food Microbiol. 2014, 188, 45–52. [Google Scholar] [CrossRef]
- Bueno, D.J.; Casale, C.H.; Pizzolitto, R.P.; Salano, M.A.; Olivier, G. Physical adsorption of aflatoxin B1 by lactic acid bacteria and Saccharomyces cerevisiae: A theoretical model. J. Food Prot. 2007, 70, 2148–2154. [Google Scholar] [CrossRef]
- Fuchs, S.; Sontag, G.; Stidl, R.; Ehrlich, V.; Kundi, M.; Knasmüller, S. Detoxification of patulin and ochratoxin A, two abundant mycotoxins, by lactic acid bacteria. Food Chem. Toxicol. 2008, 46, 1398–1407. [Google Scholar] [CrossRef]
- Hathout, A.S.; Aly, S.E. Biological detoxification of mycotoxins: A review. Ann. Microbiol. 2014, 64, 905–919. [Google Scholar] [CrossRef]
- Perczak, A.; Goliński, P.; Bryła, M.; Waśkiewicz, A. The efficiency of lactic acid bacteria against pathogenic fungi and mycotoxins. Arch. Ind. Hyg. Toxicol. 2018, 69, 32–45. [Google Scholar] [CrossRef]
- Mateo, E.M.; Medina, A.; Mateo, F.; Valle-Algarra, F.M.; Pardo, I.; Jiménez, M. Ochratoxin A removal in synthetic media by living and heat-inactivated cells of Oenococcus oeni isolated from wines. Food Control 2010, 21, 23–28. [Google Scholar] [CrossRef]
- Piotrowska, M.; Masek, A. Saccharomyces cerevisiae cell wall components as tools for ochratoxin A decontamination. Toxins 2015, 7, 1151–1162. [Google Scholar] [CrossRef]
- Jakopović, Ž.; Hanousek Čiča, K.; Mrvčić, J.; Pucić, I.; Čanak, I.; Frece, J.; Pleadin, J.; Stanzer, D.; Zjalić, S.; Markov, K. Properties and fermentation activity of industrial yeasts Saccharomyces cerevisiae, S. uvarum, Candida utilis and Kluyveromyces marxianus exposed to AFB1, OTA and ZEA. Food Technol. Biotechnol. 2018, 56, 208–217. [Google Scholar] [CrossRef]
- Pfliegler, W.P.; Pusztahelyi, T.; Pócsi, I. Mycotoxins—Prevention and decontamination by yeasts. J. Basic. Microbiol. 2015, 55, 805–818. [Google Scholar] [CrossRef]
- Bejaoui, H.; Mathieu, F.; Taillandier, P.; Lebrihi, A. Ochratoxin A removal in synthetic and natural grape juices by selected oenological Saccharomyces strains. J. Appl. Microbiol. 2004, 97, 1038–1044. [Google Scholar] [CrossRef]
- Patharajan, S.; Reddy, K.R.N.; Karthikeyan, V.; Spadaro, D.; Lore, A.; Gullino, M.L.; Garibaldi, A. Potential of yeast antagonists on in vitro biodegradation of ochratoxin A. Food Control 2011, 22, 290–296. [Google Scholar] [CrossRef]
- Jiang, C.; Li, Z.; Shi, Y.; Guo, D.; Pang, B.; Chen, X.; Shao, D.; Liu, Y.; Shi, J. Bacillus subtilis inhibits Aspergillus carbonarius by producing iturin A, which disturbs the transport, energy metabolism, and osmotic pressure of fungal cells as revealed by transcriptomics analysis. Int. J. Food Microbiol. 2020, 330, 108783. [Google Scholar] [CrossRef] [PubMed]
- Liu, W.C.; Pushparaj, K.; Meyyazhagan, A.; Arumugam, V.A.; Pappuswamy, M.; Bhotla, H.K.; Baskaran, R.; Issara, U.; Balasubramanian, B.; Khaneghah, A.M. Ochratoxin A as an alarming health threat for livestock and human: A review on molecular interactions, mechanism of toxicity, detection, detoxification, and dietary prophylaxis. Toxicon 2022, 213, 59–75. [Google Scholar] [CrossRef] [PubMed]
- Zanon, M.S.A.; Barros, G.G.; Chulze, S.N. Non-aflatoxigenic Aspergillus flavus as a potential biocontrol agents to reduce aflatoxin contamination in the peanuts harvested in Northen Argentina. Int. J. Food Microbiol. 2016, 231, 63–68. [Google Scholar] [CrossRef] [PubMed]
- Llobregat, B.; Gonzales-Candelas, L.; Bellester, A.L. Ochratoxin A deffective Aspergillus carbonarius mutants as potential biocontrol agents. Toxins 2022, 14, 745. [Google Scholar] [CrossRef] [PubMed]
- Cubaiu, L.; Abbas, H.; Dobson, A.D.W.; Burdoni, M.; Migheli, Q. Saccharomyces cerevisiae wine strain inhibits growth and decreases ochratoxin A biosynthesis by Aspergillus carbonarius and Aspergillus ochraceus. Toxins 2013, 4, 1468–1681. [Google Scholar] [CrossRef] [PubMed]
- Fiori, S.; Urgheghe, P.P.; Hammami, W.; Razzu, S.; Jaoua, S.; Migheli, Q. Biocontrol of four non- and low-fermenting yeast strains against Aspergillus carbonarius and their ability to remove ochratoxin A from grape juice. Int. J. Food Microbiol. 2014, 189, 45–50. [Google Scholar] [CrossRef] [PubMed]
- Piotrowska, M.; Zakowska, Z. The elimination of ochratoxin A by lactic acid bacteria strains. Pol. J. Microb. 2005, 54, 279–286. [Google Scholar]
- Ali-Vehmas, T.; Rizzo, A.; Westermarck, T.; Atroshi, F. Measurement of antibacterial activities of T-2 toxin, deoxynivalenol, ochratoxin A, aflatoxin B1 and fumonisin B1 using microtitration tray-based turbidimetric techniques. J. Vet. Med. Ser. A 1998, 45, 453–458. [Google Scholar] [CrossRef]
- Šain, A. Changes in Morphological Characteristics of Selected Wine Yeasts and Lactic Acid Bacteria in the Presence of Ochratoxin A. Bachelor Thesis, University of Zagreb, Zagreb, Croatia, 19 September 2017. [Google Scholar]
- Pulvirenti, A.; De Vero, L.; Blaiotta, G.; Sidari, R.; Iosca, G.; Gullo, M.; Caridi, A. Selection of wine Saccharomyces cerevisiae strains and their screening for the adsorption activity of pigments, phenolics and ochratoxin A. Fermentation 2020, 6, 80. [Google Scholar] [CrossRef]
- Jakopović, Ž. Effect of Selected Wine Yeast Strains on Binding, Degradation and Toxicity of Ochratoxin A In Vitro. Ph.D. Thesis, University of Zagreb, Zagreb, Croatia, 8 October 2021. [Google Scholar]
- Freire, L.; Furtado, M.M.; Guerreiro, T.M.; da Graca, J.S.; da Silva, B.S.; Oliveira, D.N.; Catharino, R.R.; Sant’ana, A.S. The presence of ochratoxin A does not influence Saccharomyces cerevisiae growth kinetics but leads to the formation of modified ochratoxins. Food Chem. Toxicol. 2019, 133, 110756. [Google Scholar] [CrossRef]
- Markov, K.; Mrvčić, J.; Pleadin, J.; Delaš, F.; Frece, J. FT-IR spectroscopy applied to identification of functional groups on the surface of Gluconobacter oxydans involved in the bacteria–ochratoxin A interaction. In Proceedings of the Power of Fungi and Mycotoxins in Health and Disease, Šibenik, Croatia, 20–23 September 2015. [Google Scholar]
- Markov, K.; Frece, J.; Pleadin, J.; Bevardi, M.; Barišić, L.; Kljusurić, J.G.; Vulić, A.; Jakopović, Ž.; Mrvčić, J. Gluconobacter oxydans–potential biological agent for binding or biotransformation of mycotoxins. World Mycotoxin J. 2019, 12, 153–161. [Google Scholar] [CrossRef]
- Mwabulili, F.; Xie, Y.; Li, Q.; Sun, S.; Yang, Y.; Ma, W. Research progress of ochratoxin a bio-detoxification. Toxicon 2023, 222, 107005. [Google Scholar] [CrossRef]
- Del Prete, V.; Rodriguez, H.; Carrascosa, A.V.; Rivas, B.D.L.; Garcia-Moruno, E.; Munoz, R. In vitro removal of ochratoxin A by wine lactic acid bacteria. J. Food Prot. 2007, 70, 2155–2160. [Google Scholar] [CrossRef] [PubMed]
- Piotrowska, M. The adsorption of ochratoxin A by Lactobacillus species. Toxins 2014, 6, 2826–2839. [Google Scholar] [CrossRef]
- Shukla, S.; Park, J.H.; Chung, S.H.; Kim, M. Ochratoxin A reduction ability of biocontrol agent Bacillus subtilis isolated from Korean traditional fermented food Kimchi. Sci. Rep. 2018, 8, 8039. [Google Scholar] [CrossRef]
- Niderkorn, V.; Morgavi, D.P.; Aboab, B.; Lemaire, M.; Boudra, H. Cell wall component and mycotoxin moieties involved in the binding of fumonisin B1 and B2 by lactic acid bacteria. J. Appl. Microbiol. 2009, 106, 977–985. [Google Scholar] [CrossRef]
- Dalie, D.K.D.; Deschamps, A.M.; Richard-Foget, F. Lactic acid bacteria—Potential for control of mould growth and mycotoxins: A review. Food Control 2010, 21, 370–380. [Google Scholar] [CrossRef]
- Rodriguez, H.; Reveron, I.; Doria, F.; Constantini, A.; De Las Rivas, B.; Munoz, R.; Garcia-Moruno, E. Degradation of ochratoxin A by Brevibacterium species. J. Agric. Food Chem. 2011, 59, 10755–10760. [Google Scholar] [CrossRef]
- Chen, W.; Li, C.; Zhang, B.; Zhou, Z.; Shen, Y.; Liao, X.; Yang, J.; Wang, Y.; Li, X.; Li, Y.; et al. Advances in biodetoxification of ochratoxin AA review of the past five decades. Front. Microbiol. 2018, 9, 1386. [Google Scholar] [CrossRef] [PubMed]
- Santos, J.; Castro, T.; Venâncio, A.; Silva, C. Degradation of ochratoxins A and B by lipases: A kinetic study unraveled by molecular modeling. Heliyon 2023, 9, e19921. [Google Scholar] [CrossRef]
- Cecchini, F.; Morassut, M.; Garcia Moruno, E.; Di Stefano, R. Influence of yeast strain on ochratoxin A content during fermentation of white and red must. Food Microbiol. 2006, 23, 411–417. [Google Scholar] [CrossRef] [PubMed]
- Rodrigues, I.; Binder, E.M.; Schatzmayr, G. Microorganisms and Their Enzymes for Detoxifying Mycotoxins Posing a Risk to Livestock Animals. In Mycotoxin Prevention and Control in Agriculture; Appel, M., Kendra, D.F., Trucksess, M.W., Eds.; American Chemical Society: Washington, DC, USA, 2009; pp. 107–117. [Google Scholar]
- Zhang, H.; Zhang, Y.; Yin, T.; Wang, J.; Zhang, X. Heterologous expression and characterization of a novel ochratoxin a degrading enzyme, N-acyl-L-amino acid amidohydrolase, from Alcaligenes faecalis. Toxins 2019, 11, 518. [Google Scholar] [CrossRef] [PubMed]
- Wei, M.; Dhanasekaran, S.; Ngea, G.L.N.; Godana, E.A.; Zhang, X.; Yang, Q.; Zheng, X.; Zhang, H. Cryptococcus podzolicus Y3 degrades ochratoxin A by intracellular enzymes and simultaneously eliminates citrinin. Biocontrol 2022, 168, 104857. [Google Scholar] [CrossRef]
- Wei, M.; Dhanasekaran, S.; Ji, Q.; Yang, Q.; Zhang, H. Sustainable and efficient method utilizing N-acetyl-L-cysteine for complete and enhanced ochratoxin A clearance by antagonistic yeast. J. Hazard. Mater. 2023, 448, 130975. [Google Scholar] [CrossRef]
- Varga, J.; Rigo, K.; Teren, J. Degradation of ochratoxin A by Aspergillus species. Int. J. Food Microbiol. 2000, 59, 1–7. [Google Scholar] [CrossRef]
- Stander, M.A.; Bornscheuer, W.T.; Henke, E.; Steyn, P.S. Screening of commercial hydrolases for the degradation of ochratoxin A. J. Agric. Food. Chem. 2000, 48, 5736–5739. [Google Scholar] [CrossRef]
- Abrunhosa, L.; Santos, L.; Venancio, A. Degradation of ochratoxin A by proteases and by a crude enzyme of Aspergillus niger. Food Biotechnol. 2006, 20, 231–242. [Google Scholar] [CrossRef]
- Abrunhosa, L.; Venancio, A. Isolation and purification of an enzyme hydrolyzing ochratoxin A from Aspergillus niger. Biotech. Lett. 2007, 29, 1909–1914. [Google Scholar] [CrossRef]
- Dobritzsch, D.; Wand, H.; Schneider, G.; Yu, S. Structural and functional characterization of ochratoxinase, a novel mycotoxin-degrading enzyme. Biochem. J. 2014, 462, 441–452. [Google Scholar] [CrossRef]
- Liuzzi, V.C.; Fanelli, F.; Tristezza, M.; Haidukowski, M.; Picardi, E.; Manzari, C.; Lionetti, C.; Grieco, F.; Logrieco, A.F.; Thon, M.R.; et al. Transcriptional analysis of Acinetobacter sp neg1 capable of degrading Ochratoxin A. Front. Microbiol. 2016, 7, 2162. [Google Scholar] [CrossRef]
- Dellafiora, L.; Gonaus, C.; Streit, B.; Galaverna, G.; Moll, W.-D.; Vogtentanz, G.; Schatzmayr, G.; Dall’Asta, C.; Prasad, S. An In Silico Target Fishing Approach to Identify Novel Ochratoxin A Hydrolyzing Enzyme. Toxins 2020, 12, 258. [Google Scholar] [CrossRef]
- Peng, M.; Zhang, Z.; Xu, X.; Zhang, H.; Zhao, Z.; Liang, Z. Purification and characterization of the enzymes from Brevundimonas naejangsanensis that degrade ochratoxin A and B. Food Chem. 2023, 419, 135926. [Google Scholar] [CrossRef]
- Wei, W.; Qian, Y.; Wu, Y.; Chen, Y.; Peng, C.; Luo, M.; Xu, J.; Zhou, Y. Detoxification of ochratoxin A by Lysobacter sp. CW239 and characteristics of a novel degrading gene carboxypeptidase cp4. Environ. Pollut. 2020, 258, 113677. [Google Scholar] [CrossRef]
- Luo, H.; Wang, G.; Chen, N.; Fang, Z.; Xiao, Y.; Zhang, M.; Gerelt, K.; Qian, Y.; Lai, R.; Zhou, Y. A superefficient Ochratoxin A hydrolase with promising potential for industrial applications. Appl. Environ. Microbiol. 2022, 88, e01964-21. [Google Scholar] [CrossRef]
- Pitout, M.J. The hydrolysis of Ochratoxin A by some proteolytic enzymes. Biochem. Pharmacol. 1969, 18, 485–491. [Google Scholar] [CrossRef]
- Bejaoui, H.; Mathieu, F.; Taillandier, P.; Lebrihi, A. Biodegradation of Ochratoxin A by Aspergillus section Nigri species isolated from French grapes: A potential means of Ochratoxin A decontamination in grape juices and musts. FEMS Microbiol. Lett. 2006, 255, 203–208. [Google Scholar] [CrossRef]
- Shi, L.; Liang, Z.; Xu, S.; Zheng, H.; Huang, K. Adsorption and degradation of Ochratoxin A by Bacillus licheniformis Sl-1. J. Agric. Biotechnol. 2013, 21, 1420–1425. [Google Scholar]
- Shi, L.; Liang, Z.; Li, J.; Hao, J.; Xu, Y.; Huang, K.; Tian, J.; He, X.; Xu, W. Ochratoxin A biocontrol and biodegradation by Bacillus subtilis CW 14. J. Sci. Food Agric. 2014, 94, 1879–1885. [Google Scholar] [CrossRef]
- Böswald, C.; Engelhardt, G.; Vogel, H.; Wallnöfer, P.R. Metabolism of the Fusarium mycotoxins zearalenone and deoxynivalenol by yeast strains of technological relevance. Nat. Toxins 1995, 3, 138–144. [Google Scholar] [CrossRef]
Microorganism | Strain | OTA Removal (%) | Source |
---|---|---|---|
Saccharomyces cerevisiae | - | 82.8–85.1 in grape | 116 |
- | 73–90 | 84,110,111 | |
BS | 75–77 | 116 | |
EC 118 | 29–95 | 84 | |
Y28 | 81.87 | 83 | |
TP5 TT173 | 79–100/ 47–86 | 109 | |
Candida intermedia | - | >80 | 78 |
Debaryomyces hansenii | - | >98 | 84 |
Bacillus subtilis | - | 78 | 117 |
Gluconobacter oxydans | - | >80 | 113 |
Microorganism | Strain | OTA Degradation Rate (%) | Source |
---|---|---|---|
Saccharomyces cerevisiae | 83–85 | 78, 84 | |
Candida intermedia | >80 | 84 | |
Debaryomyces hansenii | >98 | 84 | |
Bacillus subtilis | 78 | 84, 117 | |
Brevibacterium casei | RM101 | 100 | 120 |
DSM 20657 T DSM 9657 ND DSM 20658 RM101 | 100 | 120 | |
Brevibacterium linens | DSM 20425 T | 100 | 120 |
Brevibacterium iodinum | DSM20626T | 100 | 120 |
Brevibacterium epidermidis | DSM 20660T | 100 | 120 |
Lactobacillus kefiri | KFLM3 | 81 | 121 |
Pediococcus parvulus | UTAD 168 | 89 | 89 |
UTAD 333 | 97 | 89 | |
UTAD 334 | 94 | 89 | |
UTAD 335 | 98 | 89 | |
UTAD 473 | 100 ± 0 | 89 | |
Aspergillus niger | >90% | 124 | |
Rhizopus sp. | 100 | 124 | |
Trichosporon mycotoxinivorans | MTV | 100 | 124 |
Microorganism | Enzyme | Degradation Product(s) | Source |
---|---|---|---|
Aspergillus niger | Lipase | Acid L-β-phenylalanine and (PHE) and OTα | 129 |
Protease A (acid protease) | OTα | 86 | |
Prolyve PAC (acid protease) | OTα | 86 | |
Saccharomyces cerevisiae | Carboxypeptidase Y (CPY) | OTα | 86 |
Stenotrophomonas acidaminiphila CW117 | Amido hydrolase ADH3 | OTα | 137 |
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Zjalic, S.; Markov, K.; Loncar, J.; Jakopovic, Z.; Beccaccioli, M.; Reverberi, M. Biocontrol of Occurrence Ochratoxin A in Wine: A Review. Toxins 2024, 16, 277. https://doi.org/10.3390/toxins16060277
Zjalic S, Markov K, Loncar J, Jakopovic Z, Beccaccioli M, Reverberi M. Biocontrol of Occurrence Ochratoxin A in Wine: A Review. Toxins. 2024; 16(6):277. https://doi.org/10.3390/toxins16060277
Chicago/Turabian StyleZjalic, Slaven, Ksenija Markov, Jelena Loncar, Zeljko Jakopovic, Marzia Beccaccioli, and Massimo Reverberi. 2024. "Biocontrol of Occurrence Ochratoxin A in Wine: A Review" Toxins 16, no. 6: 277. https://doi.org/10.3390/toxins16060277