Use of Yeast Mannoproteins by Oenococcus oeni during Malolactic Fermentation under Different Oenological Conditions
Abstract
:1. Introduction
2. Materials and Methods
2.1. Microorganisms
2.2. Experimental Fermentations
2.2.1. Fermentations in Wine-Like Medium
2.2.2. Fermentations in Natural Grape Must
2.3. Wine Characterization
2.4. Sampling and RNA Extraction
2.5. RT-qPCR
2.6. Statistical Analysis
3. Results and Discussion
3.1. Fermentations
3.2. Mannoprotein Utilization
3.3. General Wine Chemical Compounds
3.4. Transcriptional Response of Mannose-Related Genes
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Lonvaud, A. Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie Leeuwenhoek 1999, 76, 317–331. [Google Scholar] [CrossRef]
- Bartowsky, E.J. Oenococcus oeni and malolactic fermentation—Moving into the molecular arena. Aust. J. Grape Wine Res. 2005, 11, 174–187. [Google Scholar] [CrossRef]
- Lerm, E.; Engelbrecht, L.; Du Toit, M. Malolactic Fermentation: The ABC’s of MLF. S. Afr. J. Enol. Vitic. 2016, 31, 186–212. [Google Scholar] [CrossRef] [Green Version]
- Davis, C.R.; Wibowo, D.; Eschenbruch, R.; Lee, T.H.; Fleet, G.H. Practical Implications of Malolactic Fermentation: A Review. Am. J. Enol. Vitic. 1985, 36, 290–301. [Google Scholar]
- Liu, S.-Q. Malolactic fermentation in wine—Beyond deacidification. J. Appl. Microbiol. 2002, 92, 589–601. [Google Scholar] [CrossRef]
- Bauer, R.; Dicks, L. Control of Malolactic Fermentation in Wine. A Review. S. Afr. J. Enol. Vitic. 2017, 25, 74–88. [Google Scholar] [CrossRef] [Green Version]
- Beltran, G.; Torija, M.J.; Novo, M.; Ferrer, N.; Poblet, M.; Guillamón, J.M.; Rozès, N.; Mas, A. Analysis of yeast populations during alcoholic fermentation: A six year follow-up study. Syst. Appl. Microbiol. 2002, 25, 287–293. [Google Scholar] [CrossRef]
- Diez, L.; Guadalupe, Z.; Ayestarán, B.; Ruiz-Larrea, F. Effect of Yeast Mannoproteins and Grape Polysaccharides on the Growth of Wine Lactic Acid and Acetic Acid Bacteria. J. Agric. Food Chem. 2010, 58, 7731–7739. [Google Scholar] [CrossRef]
- Belda, I.; Conchillo, L.B.; Ruiz, J.; Navascués, E.; Marquina, D.; Santos, A. Selection and use of pectinolytic yeasts for improving clarification and phenolic extraction in winemaking. Int. J. Food Microbiol. 2016, 223, 1–8. [Google Scholar] [CrossRef]
- Balmaseda, A.; Bordons, A.; Reguant, C.; Bautista-Gallego, J. Non-Saccharomyces in Wine: Effect Upon Oenococcus oeni and Malolactic Fermentation. Front. Microbiol. 2018, 9, 534. [Google Scholar] [CrossRef]
- Mills, D.A.; Rawsthorne, H.; Parker, C.; Tamir, D.; Makarova, K. Genomic analysis of Oenococcus oeni PSU-1 and its relevance to winemaking. FEMS Microbiol. Rev. 2005, 29, 465–475. [Google Scholar] [CrossRef] [Green Version]
- Bartowsky, E.J. Oenococcus oeni and the genomic era. FEMS Microbiol. Rev. 2017, 41, S84–S94. [Google Scholar] [CrossRef]
- Ribéreau-Gayon, P.; Dubourdieu, D.; Donèche, B.; Lonvaud, A. Handbook of Enology: Volume 1, The Microbiology of Wine and Vinifications; Wiley: Hoboken, NJ, USA, 2006; Volume 1. [Google Scholar]
- Padilla, B.; Gil, J.V.; Manzanares, P. Past and Future of Non-Saccharomyces Yeasts: From Spoilage Microorganisms to Biotechnological Tools for Improving Wine Aroma Complexity. Front. Microbiol. 2016, 7, 411. [Google Scholar] [CrossRef] [Green Version]
- Petruzzi, L.; Capozzi, V.; Berbegal, C.; Corbo, M.R.; Bevilacqua, A.; Spano, G.; Sinigaglia, M. Microbial Resources and Enological Significance: Opportunities and Benefits. Front. Microbiol. 2017, 8, 995. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Belda, I.; Navascués, E.; Marquina, D.; Santos, A.; Calderon, F.; Benito, S. Dynamic analysis of physiological properties of Torulaspora delbrueckii in wine fermentations and its incidence on wine quality. Appl. Microbiol. Biotechnol. 2014, 99, 1911–1922. [Google Scholar] [CrossRef] [PubMed]
- Contreras, A.; Hidalgo, C.; Henschke, P.A.; Chambers, P.J.; Curtin, C.; Varela, C. Evaluation of Non-Saccharomyces Yeasts for the Reduction of Alcohol Content in Wine. Appl. Environ. Microbiol. 2014, 80, 1670–1678. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Balmaseda, A.; Rozès, N.; Ángel, L.M.; Bordons, A.; Reguant, C. Impact of changes in wine composition produced by non-Saccharomyces on malolactic fermentation. Int. J. Food Microbiol. 2021, 337, 108954. [Google Scholar] [CrossRef]
- Benito, S. The impact of Torulaspora delbrueckii yeast in winemaking. Appl. Microbiol. Biotechnol. 2018, 102, 3081–3094. [Google Scholar] [CrossRef] [PubMed]
- Belda, I.; Navascués, E.; Marquina, D.; Santos, A.; Calderón, F.; Benito, S. Outlining the influence of non-conventional yeasts in wine ageing over lees. Yeast 2016, 33, 329–338. [Google Scholar] [CrossRef]
- Romano, P. Function of yeast species and strains in wine flavour. Int. J. Food Microbiol. 2003, 86, 169–180. [Google Scholar] [CrossRef]
- Fleet, G.H. Wine yeasts for the future. FEMS Yeast Res. 2008, 8, 979–995. [Google Scholar] [CrossRef] [Green Version]
- Martín-Garcia, A.; Balmaseda, A.; Bordons, A.; Reguant, C. Effect of the inoculation strategy of non-Saccharomyces yeasts on wine malolactic fermentation. OENO One 2020, 54, 101–108. [Google Scholar] [CrossRef] [Green Version]
- Guillouxbenatier, M.; Le Fur, Y.; Feuillat, M. Influence of fatty acids on the growth of wine microorganisms Saccharomyces cerevisiae and Oenococcus oeni. J. Ind. Microbiol. Biotechnol. 1998, 20, 144–149. [Google Scholar] [CrossRef]
- Guilloux-Benatier, M.; Guerreau, J.; Feuillat, M. Influence of Initial Colloid Content on Yeast Macromolecule Production and on the Metabolism of Wine Microorganisms. Am. J. Enol. Vitic. 1995, 46, 486–492. [Google Scholar]
- Giovani, G.; Rosi, I.; Bertuccioli, M. Quantification and characterization of cell wall polysaccharides released by non-Saccharomyces yeast strains during alcoholic fermentation. Int. J. Food Microbiol. 2012, 160, 113–118. [Google Scholar] [CrossRef]
- Vejarano, R. Non-Saccharomyces in Winemaking: Source of Mannoproteins, Nitrogen, Enzymes, and Antimicrobial Compounds. Fermentation 2020, 6, 76. [Google Scholar] [CrossRef]
- Liu, Y.; Rousseaux, S.; Tourdot-Maréchal, R.; Sadoudi, M.; Gougeon, R.; Schmitt-Kopplin, P.; Alexandre, H. Wine microbiome: A dynamic world of microbial interactions. Crit. Rev. Food Sci. Nutr. 2015, 57, 856–873. [Google Scholar] [CrossRef]
- Alexandre, H.; Costello, P.J.; Remize, F.; Guzzo, J.; Guilloux-Benatier, M. Saccharomyces cerevisiae–Oenococcus oeni interactions in wine: Current knowledge and perspectives. Int. J. Food Microbiol. 2004, 93, 141–154. [Google Scholar] [CrossRef] [PubMed]
- Jamal, Z.; Miot-Sertier, C.; Thibau, F.; Dutilh, L.; Lonvaud-Funel, A.; Ballestra, P.; Le Marrec, C.; Dols-Lafargue, M. Distribution and Functions of Phosphotransferase System Genes in the Genome of the Lactic Acid Bacterium Oenococcus oeni. Appl. Environ. Microbiol. 2013, 79, 3371–3379. [Google Scholar] [CrossRef] [Green Version]
- Cibrario, A.; Peanne, C.; Lailheugue, M.; Campbell-Sills, H.; Dols-Lafargue, M. Carbohydrate metabolism in Oenococcus oeni: A genomic insight. BMC Genom. 2016, 17, 1–19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Margalef-Català, M.; Stefanelli, E.; Araque, I.; Wagner, K.; Felis, G.E.; Bordons, A.; Torriani, S.; Reguant, C. Variability in gene content and expression of the thioredoxin system in Oenococcus oeni. Food Microbiol. 2017, 61, 23–32. [Google Scholar] [CrossRef] [PubMed]
- Bordas, M.; Araque, I.; Bordons, A.; Reguant, C. Differential expression of selected Oenococcus oeni genes for adaptation in wine-like media and red wine. Ann. Microbiol. 2015, 65, 2277–2285. [Google Scholar] [CrossRef]
- Balmaseda, A.; Rozès, N.; Bordons, A.; Reguant, C. Simulated lees of different yeast species modify the performance of malolactic fermentation by Oenococcus oeni in wine-like medium. Food Microbiol. 2021, 99, 103839. [Google Scholar] [CrossRef] [PubMed]
- Olguin, N.T.; Bordons, A.; Reguant, C. Influence of ethanol and pH on the gene expression of the citrate pathway in Oenococcus oeni. Food Microbiol. 2009, 26, 197–203. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
- Ferrando, N.; Araque, I.; Ortís, A.; Thornes, G.; Bautista-Gallego, J.; Bordons, A.; Reguant, C. Evaluating the effect of using non-Saccharomyces on Oenococcus oeni and wine malolactic fermentation. Food Res. Int. 2020, 138, 109779. [Google Scholar] [CrossRef]
- Loira, I.; Vejarano, R.; Bañuelos, M.; Morata, A.; Tesfaye, W.; Uthurry, C.; Villa, A.; Cintora, I.; Suárez-Lepe, J. Influence of sequential fermentation with Torulaspora delbrueckii and Saccharomyces cerevisiae on wine quality. LWT 2014, 59, 915–922. [Google Scholar] [CrossRef] [Green Version]
- Roca-Mesa, H.; Sendra, S.; Mas, A.; Beltran, G.; Torija, M.-J. Nitrogen Preferences during Alcoholic Fermentation of Different Non-Saccharomyces Yeasts of Oenological Interest. Microorganisms 2020, 8, 157. [Google Scholar] [CrossRef] [Green Version]
- Bordet, F.; Joran, A.; Klein, G.; Roullier-Gall, C.; Alexandre, H. Yeast–Yeast Interactions: Mechanisms, Methodologies and Impact on Composition. Microorganisms 2020, 8, 600. [Google Scholar] [CrossRef] [Green Version]
- Giaramida, P.; Ponticello, G.; Di Maio, S.; Squadrito, M.; Genna, G.; Barone, E.; Scacco, A.; Corona, O.; Amore, G.; Di Stefano, R.; et al. Candida zemplinina for Production of Wines with Less Alcohol and More Glycerol. S. Afr. J. Enol. Vitic. 2016, 34, 204–211. [Google Scholar] [CrossRef] [Green Version]
- Kim, O.B.; Richter, H.; Zaunmüller, T.; Graf, S.; Unden, G. Role of Secondary Transporters and Phosphotransferase Systems in Glucose Transport by Oenococcus oeni. J. Bacteriol. 2011, 193, 6902–6911. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stefanelli, E. Stress Response and Intraspecific Diversity in Oenococcus oeni. Ph.D. Thesis, Università degli Studi di Verona, Verona, Italy, 2014. [Google Scholar]
- Desroche, N.; Beltramo, C.; Guzzo, J. Determination of an internal control to apply reverse transcription quantitative PCR to study stress response in the lactic acid bacterium Oenococcus oeni. J. Microbiol. Methods 2005, 60, 325–333. [Google Scholar] [CrossRef] [PubMed]
Consumption Rate (g/L·day) * | Duration (days) | pH | Glucose + Fructose (g/L) | Citric Acid (g/L) | Acetic Acid (g/L) | D-lactic Acid (mg/L) | ||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
MLF | Post-MLF | MLF | Post-MLF | MLF | Post-MLF | MLF | Post-MLF | MLF | Post-MLF | |||
No addition | 0.48 ± 0.02 b | 5 | 3.60 ± 0.01 a | 3.61 ± 0.0 a | 1.63 ± 0.01 a | 1.63 ± 0.02 a | 0.43 ± 0.03 a | 0.27 ± 0.08 a | 0.31 ± 0.01 a | 0.31 ± 0.01 a | 20.2 ± 1.2 b | 22.8 ± 0.6 b |
100 mg/L | 0.55 ± 0.02 a | 5 | 3.60 ± 0.02 a | 3.61 ± 0.01 a | 1.63 ± 0.03 a | 1.63 ± 0.03 a | 0.41 ± 0.03 a | 0.31 ± 0.02 ab | 0.33 ± 0.01 a | 0.32 ± 0.01 a | 40.5 ± 7.3 a | 49.5 ± 1.3 a |
200 mg/L | 0.49 ± 0.02 b | 5 | 3.59 ± 0.01 a | 3.61 ± 0.01 a | 1.65 ± 0.06 a | 1.68 ± 0.02 a | 0.43 ± 0.03 a | 0.35 ± 0.04 ab | 0.30 ± 0.01 a | 0.33 ± 0.01 a | 37.9 ± 9.0 a | 51.8 ± 1.0 a |
400 mg/L | 0.48 ± 0.02 b | 5 | 3.61 ± 0.01 a | 3.61 ± 0.01 a | 1.65 ± 0.02 a | 1.68 ± 0.04 a | 0.45 ± 0.03 a | 0.37 ± 0.04 b | 0.29 ± 0.01 a | 0.32 ± 0.02 a | 38.5 ± 3.2 a | 56.1 ± 4.5 a |
Consumption Rate (g/L·day) * | Duration (Days) | YAN (AF) | pH | Glucose + Fructose (g/L) | Citric Acid (g/L) | Acetic Acid (g/L) | D-Lactic Acid (g/L) | Ethanol (% v/v) | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
NOPA | NH4 | AF | MLF | AF | MLF | AF | MLF | AF | MLF | MLF | AF | ||||
ScQA23 | 0.53 ± 0.02 b | 4 | 34.93 ± 6.90 ab | 17.67 ± 1.53 a | 3.49 ± 0.04 ab | 3.77 ± 0.04 d | n.d.a | n.d.b | 0.59 ± 0.02 ab | 0.21 ± 0.02 b | 0.29 ± 0.02 b | 0.70 ± 0.01 b | 0.20 ± 0.01 b | 10.8 ± 0.2 a | |
Sc3D | 0.80 ± 0.02 a | 2 | 24.36 ± 0.76 b | 13.67 ± 2.08 a | 3.47 ± 0.01 ab | 3.67 ± 0.01 bc | 1.66 ± 0.48 b | 1.67 ± 0.07 a | 0.62 ± 0.03 b | 0.11 ± 0.01 a | 0.28 ± 0.04 b | 0.66 ± 0.00 b | 0.26 ± 0.06 cd | 11.0 ± 0.2 a | |
TdViniferm | 0.73 ± 0.02 a | 2 | 23.71 ± 2.68 b | 16.00 ± 2.00 a | 3.42 ± 0.01 a | 3.59 ± 0.01 a | 1.05 ± 0.26 ab | 0.47 ± 0.38 a | 0.69 ± 0.00 c | 0.11 ± 0.02 a | 0.25 ± 0.04 ab | 0.47 ± 0.04 a | 0.29 ± 0.01 d | 11.2 ± 0.2 a | |
TdZymaflore | 0.76 ± 0.02 a | 2 | 28.59 ± 5.09 ab | 13.67 ± 1.15 a | 3.44 ± 0.02 a | 3.62 ± 0.01 ab | 1.55 ± 0.14 ab | 0.61 ± 0.21 a | 0.73 ± 0.02 c | 0.11 ± 0.02 a | 0.17 ± 0.04 a | 0.43 ± 0.07 a | 0.24 ± 0.00 c | 10.7 ± 0.2 a | |
MpFlavia | 0.50 ± 0.02 b | 4 | 37.29 ± 2.85 a | 13.33 ± 1.15 a | 3.54 ± 0.04 b | 3.71 ± 0.01 c | 1.41 ± 0.01 ab | 1.12 ± 0.57 a | 0.56 ± 0.02 a | 0.11 ± 0.01 a | 0.59 ± 0.04 c | 0.74 ± 0.01 b | 0.14 ± 0.01 a | 10.8 ± 0.2 a |
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Balmaseda, A.; Aniballi, L.; Rozès, N.; Bordons, A.; Reguant, C. Use of Yeast Mannoproteins by Oenococcus oeni during Malolactic Fermentation under Different Oenological Conditions. Foods 2021, 10, 1540. https://doi.org/10.3390/foods10071540
Balmaseda A, Aniballi L, Rozès N, Bordons A, Reguant C. Use of Yeast Mannoproteins by Oenococcus oeni during Malolactic Fermentation under Different Oenological Conditions. Foods. 2021; 10(7):1540. https://doi.org/10.3390/foods10071540
Chicago/Turabian StyleBalmaseda, Aitor, Laura Aniballi, Nicolas Rozès, Albert Bordons, and Cristina Reguant. 2021. "Use of Yeast Mannoproteins by Oenococcus oeni during Malolactic Fermentation under Different Oenological Conditions" Foods 10, no. 7: 1540. https://doi.org/10.3390/foods10071540