Impact of the Inoculation Method of Geotrichum candidum, Used as Biocontrol Agent, on T-2 Toxin Produced by Fusarium sporotrichioides and F. langsethiae during the Malting Process
Abstract
:1. Introduction
2. Results
2.1. G. candidum Growth and PLA Production Kinetics
2.2. Co-Culture between G. candidum and Fusarium Strains in Ym Synthetic Medium
2.3. Micro-Malting Assays
3. Discussion
4. Conclusions
5. Materials and Methods
5.1. Reagents and Chemicals
5.2. Strains, Media and Culture Conditions
5.3. Co-Culture of Fusarium Strains and G. candidum in Ym Synthetic Medium
5.4. Micro-Malting Assays
5.5. G. candidum, F. sporotrichioides 186 and F. langsethiae 2297 Biomass Evaluation in Co-Cultures
5.6. T-2 Toxin and PLA Quantification by HPLC-DAD
5.6.1. T-2 Toxin Quantification
5.6.2. PLA Quantification
5.7. Statistical Analysis
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Rodríguez-Carrasco, Y.; Fattore, M.; Albrizio, S.; Berrada, H.; Mañes, J. Occurrence of Fusarium mycotoxins and their dietary intake through beer consumption by the European population. Food Chem. 2015, 178, 149–155. [Google Scholar] [CrossRef]
- Piacentini, K.C.; Rocha, L.O.; Fontes, L.C.; Carnielli, L.; Reis, T.A.; Corrêa, B. Mycotoxin analysis of industrial beers from Brazil: The influence of fumonisin B1 and deoxynivalenol in beer quality. Food Chem. 2017, 218, 64–69. [Google Scholar] [CrossRef] [PubMed]
- The Brewers of Europe. European Beer Trends—Statistics Report; The Brewers of Europe: Brussel, Belgium, 2019. [Google Scholar]
- Nielsen, L.K.; Cook, D.J.; Edwards, S.G.; Ray, R.V. The prevalence and impact of Fusarium head blight pathogens and mycotoxins on malting barley quality in UK. Int. J. Food Microbiol. 2014, 179, 38–49. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Magan, N.; Hope, R.; Colleate, A.; Baxter, E.S. Relationship between growth and mycotoxin production by Fusarium species, biocides and environment. Eur. J. Plant Pathol. 2002, 108, 685–690. [Google Scholar] [CrossRef]
- Malachova, A.; Cerkal, R.; Ehrenbergerova, J.; Dzuman, Z.; Vaculova, K.; Hajslova, J. Fusarium mycotoxins in various barley cultivars and their transfer into malt. J. Sci. Food Agric. 2010, 90, 2495–2505. [Google Scholar] [CrossRef] [PubMed]
- Strub, C.; Pocaznoi, D.; Lebrihi, A.; Fournier, R.; Mathieu, F. Influence of barley malting operating parameters on T-2 and HT-2 toxinogenesis of Fusarium langsethiae, a worrying contaminant of malting barley in Europe. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2010, 27, 1247–1252. [Google Scholar] [CrossRef]
- Piacentini, K.C.; Bĕláková, S.; Benešová, K.; Pernica, M.; Savi, G.D.; Rocha, L.O.; Hartman, I.; Čáslavský, J.; Corrêa, B. Fusarium mycotoxins stability during the malting and brewing processes. Toxins 2019, 11, 257. [Google Scholar] [CrossRef] [Green Version]
- Inoue, T.; Nagatomi, Y.; Uyama, A.; Mochizuki, N. Fate of mycotoxins during beer brewing and fermentation. Biosci. Biotechnol. Biochem. 2013, 77, 1410–1415. [Google Scholar] [CrossRef] [Green Version]
- Grajewski, J.; Kosicki, R.; Twarużek, M.; Błajet-Kosicka, A. Occurrence and risk assessment of mycotoxins through polish beer consumption. Toxins 2019, 11, 254. [Google Scholar] [CrossRef] [Green Version]
- Varga, E.; Malachova, A.; Schwartz, H.; Krska, R.; Berthiller, F. Survey of deoxynivalenol and its conjugates deoxynivalenol-3-glucoside and 3-acetyl-deoxynivalenol in 374 beer samples. Food Addit. Contam. Part A Chem. Anal. Control Expo. Risk Assess. 2013, 30, 137–146. [Google Scholar] [CrossRef]
- Peters, J.; Van Dam, R.; Van Doorn, R.; Katerere, D.; Berthiller, F.; Haasnoot, W.; Nielen, M.W.F. Mycotoxin profiling of 1000 beer samples with a special focus on craft beer. PLoS ONE 2017, 12, e0185887. [Google Scholar] [CrossRef] [Green Version]
- Kalantari, H.; Moosavi, M. Review on T-2 toxin. J. Nat. Pharm. Prod. 2010, 5, 26–38. [Google Scholar]
- van der Fels-Klerx, H.; Stratakou, I. T-2 toxin and HT-2 toxin in grain and grain-based commodities in Europe: Occurrence, factors affecting occurrence, co-occurrence and toxicological effects. World Mycotoxin J. 2010, 3, 349–367. [Google Scholar] [CrossRef]
- Schuhmacher-Wolz, U.; Heine, K.; Schneider, K. Report on toxicity data on trichothecene mycotoxins HT-2 and T-2 toxins. EFSA J. 2010, 7, 1–57. [Google Scholar] [CrossRef]
- IARC Some naturally occurring substances: Food items and constituents, heterocyclic aromatic amines and mycotoxins. IARC Monogr. Eval. Carcinog. Risks Humans. 1993, 56, 245–395.
- European Commission (EC) Recomendations on the presence of T-2 and HT-2 toxin in cereals and cereal products. Off. J. Eur. Union 2013, 56, 12–15. [CrossRef]
- Boivin, P.; Malanda, M. Inoculation by Geotrichum Candidum during Malting of Cereals or Other Plants. U.S. Patent 5,955,070, 21 September 1999. [Google Scholar]
- Gastélum-Martínez, E.; Compant, S.; Taillandier, P.; Mathieu, F. Control of T-2 toxin in Fusarium langsethiae and Geotrichum candidum co-culture. Arh. Hig. Rada Toksikol. 2012, 63, 447–456. [Google Scholar] [CrossRef]
- Kawtharani, H.; Snini, S.P.; Heang, S.; Bouajila, J.; Taillandier, P.; Mathieu, F.; Beaufort, S. Phenyllactic Acid Produced by Geotrichum candidum reduces Fusarium sporotrichioides and F. langsethiae growth and T-2 Toxin concentration. Toxins 2020, 12, 209. [Google Scholar] [CrossRef] [Green Version]
- Dziuba, E.; Wojtatowicz, M.; Stempniewicz, R.; Fosczyńska, B. The use of Geotrichum candidum starger cultures in malting of brewery barley. Prog. Biotechnol. 2000, 17, 311–316. [Google Scholar] [CrossRef]
- Wolf-Hall, C.E. Mold and mycotoxin problems encountered during malting and brewing. Int. J. Food Microbiol. 2007, 119, 89–94. [Google Scholar] [CrossRef]
- Sullivan, M.L.; Bradford, B.J. Viable cell yield from active dry yeast products and effects of storage temperature and diluent on yeast cell viability. J. Dairy Sci. 2011, 94, 526–531. [Google Scholar] [CrossRef] [PubMed]
- Thammavongs, B.; Denou, E.; Missous, G.; Guéguen, M.; Panoff, J.M. Response to environmental stress as a global phenomenon in biology: The Example of microorganisms. Microbes Environ. 2008, 23, 20–23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abadias, M.; Benabarre, A.; Teixidó, N.; Usall, J.; Vias, I. Effect of freeze drying and protectants on viability of the biocontrol yeast Candida sake. Int. J. Food Microbiol. 2001, 65, 173–182. [Google Scholar] [CrossRef]
- Berner, D.; Viernstein, H. Effect of protective agents on the viability of Lactococcus lactis subjected to freeze-thawing and freeze-drying. Sci. Pharm. 2006, 74, 137–149. [Google Scholar] [CrossRef] [Green Version]
- Usall, J.; Teixidó, N.; Fons, E.; Viñas, I. Biological control of blue mould on apple by a strain of Candida sake under several controlled atmosphere conditions. Int. J. Food Microbiol. 2000, 58, 83–92. [Google Scholar] [CrossRef]
- Abadias, M.; Teixidó, N.; Usall, J.; Benabarre, A.; Viñas, I. Viability, efficacy, and storage stability of freeze-dried biocontrol agent Candida sake using different protective and rehydration media. J. Food Prot. 2001, 64, 856–861. [Google Scholar] [CrossRef]
- Naz, S.; Gueguen-Minerbe, M.; Cretenet, M.; Vernoux, J.P. Aromatic amino acids as precursors of antimicrobial metabolites in Geotrichum candidum. FEMS Microbiol. Lett. 2013, 344, 39–47. [Google Scholar] [CrossRef] [Green Version]
- Boutrou, R.; Guéguen, M. Interests in Geotrichum candidum for cheese technology. Int. J. Food Microbiol. 2005, 102, 1–20. [Google Scholar] [CrossRef]
- Martin, N.; Savonitto, S.; Molimard, P.; Berger, C.; Brousse, M.; Spinnler, H.E. Flavor generation in cheese curd by coculturing with selected yeast, mold, and bacteria. J. Dairy Sci. 1999, 82, 1072–1080. [Google Scholar] [CrossRef]
- Martin, N.; Berger, C.; Le Du, C.; Spinnler, H.E. Aroma compound production in cheese curd by coculturing with selected yeast and bacteria. J. Dairy Sci. 2001, 84, 2125–2135. [Google Scholar] [CrossRef]
- Kure, C.F.; Wasteson, Y.; Brendehaug, J.; Skaar, I. Mould contaminants on Jarlsberg and Norvegia cheese blocks from four factories. Int. J. Food Microbiol. 2001, 70, 21–27. [Google Scholar] [CrossRef]
- Arfi, K.; Spinnler, H.; Tache, R.; Bonnarme, P. Production of volatile compounds by cheese-ripening yeasts: Requirement for a methanethiol donor for S-methyl thioacetate synthesis by Kluyveromyces lactis. Appl. Microbiol. Biotechnol. 2002, 58, 503–510. [Google Scholar] [CrossRef] [PubMed]
- Walker, G.M.; De Nicola, R.; Anthony, S.; Learmonth, R. Yeast-metal interactions: Impact on brewing and distilling fermentations. Enzyme Microb. Technol. 2006, 26, 678–687. [Google Scholar]
- Walker, G.M. Metals in yeast fermentation processes. Adv. Appl. Microbiol. 2004, 54, 197–229. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Medina, A.; Valle-Algarra, F.M.; Jiménez, M.; Magan, N. Different sample treatment approaches for the analysis of T-2 and HT-2 toxins from oats-based media. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2010, 878, 2145–2149. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Incubation Time (Days) | |||||
---|---|---|---|---|---|
Inoculation Condition | 1 | 2 | 3 | 5 | 7 |
0.2 g/L freeze-dried | ND | 0.181 ± 0.038 a | 0.112 ± 0.004 a | 0.034 ± 0.001 a | 0.001 ± 0.0002 a |
0.4 g/L freeze-dried | 0.175 ± 0.011 | 0.186 ± 0.004 a | 0.059 ± 0.003 b | 0.049 ± 0.008 a | 0.001 ± 0.0002 a |
0.4 g/L activated | 0.136 ± 0.006 | 0.157 ± 0.01 a | 0.129 ± 0.002 a | 0.098 ± 0.008 b | 0.086 ± 0.001 b |
F. langsethiae 2297 | F. sporotrichioides 186 | |||
---|---|---|---|---|
Incubation Time (Days) | Incubation Time (Days) | |||
G. candidum inoculation condition | 3 | 5 | 3 | 5 |
0.2 g/L freeze-dried | 0.29 (±0.00) a | 0.13 (±0.02) a | 0.30 (±0.01) a | 0.14 (±0.01) a |
0.4 g/L freeze-dried | 0.49 (±0.03) b | 0.25 (±0.01) b | 0.43 (±0.01) b | 0.23 (±0.01) b |
0.2 g/L activated | 0.49 (±0.01) b | 0.19 (±0.01) a,b | 0.50 (±0.01) b | 0.22 (±0.01) b |
0.4 g/L activated | 0.73 (±0.02) c | 0.39 (±0.02) c | 0.72 (±0.02) c | 0.77 (±0.01) c |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 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
Kawtharani, H.; Beaufort, S.; Anson, P.; Taillandier, P.; Mathieu, F.; Snini, S.P. Impact of the Inoculation Method of Geotrichum candidum, Used as Biocontrol Agent, on T-2 Toxin Produced by Fusarium sporotrichioides and F. langsethiae during the Malting Process. Toxins 2022, 14, 239. https://doi.org/10.3390/toxins14040239
Kawtharani H, Beaufort S, Anson P, Taillandier P, Mathieu F, Snini SP. Impact of the Inoculation Method of Geotrichum candidum, Used as Biocontrol Agent, on T-2 Toxin Produced by Fusarium sporotrichioides and F. langsethiae during the Malting Process. Toxins. 2022; 14(4):239. https://doi.org/10.3390/toxins14040239
Chicago/Turabian StyleKawtharani, Hiba, Sandra Beaufort, Philippe Anson, Patricia Taillandier, Florence Mathieu, and Selma Pascale Snini. 2022. "Impact of the Inoculation Method of Geotrichum candidum, Used as Biocontrol Agent, on T-2 Toxin Produced by Fusarium sporotrichioides and F. langsethiae during the Malting Process" Toxins 14, no. 4: 239. https://doi.org/10.3390/toxins14040239