Starmerella bacillaris Released in Vineyards at Different Concentrations Influences Wine Glycerol Content Depending on the Vinification Protocols
Abstract
:1. Introduction
2. Materials and Methods
2.1. Yeast Strains and Growth Conditions
2.2. Yeast Release in the Vineyard and Experimental Procedure
2.3. Fermentation Trials
2.4. Microbiological Analysis
2.5. Chemical Analysis
2.6. Real Time PCR Quantification of Starmerella Bacillaris
2.7. Statistical Analysis
3. Results and Discussion
3.1. Release of Starmerella Bacillaris in Vineyard and Inoculum Evaluation
3.2. Fermentation Trials
3.3. Quantification of Total Yeasts and Starmerella Bacillaris
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Drumonde-Neves, J.; Franco-Duarte, R.; Lima, T.; Schuller, D.; Pais, C. Association between grape yeast communities and the vineyard ecosystems. PLoS ONE 2017, 12, e0169883. [Google Scholar] [CrossRef] [PubMed]
- Varela, C.; Borneman, A.R. Yeasts found in vineyards and wineries. Yeast 2017, 34, 111–128. [Google Scholar] [CrossRef] [PubMed]
- Bovo, B.; Giacomini, A.; Corich, V. Effects of grape marcs acidification treatment on the evolution of indigenous yeast populations during the production of grappa. J. Appl. Microbiol. 2011, 111, 382–388. [Google Scholar] [CrossRef] [PubMed]
- Csoma, H.; Sipiczki, M. Taxonomic reclassification of Candida stellata strains reveals frequent occurrence of Candida zemplinina in wine fermentation. FEMS Yeast Res. 2008, 8, 328–336. [Google Scholar] [CrossRef] [Green Version]
- Sipiczki, M. Candida zemplinina sp. nov., an osmotolerant and psychrotolerant yeast that ferments sweet botrytized wines. Int. J.Syst. Evol. Microbiol. 2003, 53, 2079–2083. [Google Scholar] [CrossRef] [Green Version]
- Benito, Á.; Calderón, F.; Benito, S. The influence of non-Saccharomyces species on wine fermentation quality parameters. Fermentation 2019, 5, 54. [Google Scholar] [CrossRef] [Green Version]
- Englezos, V.; Giacosa, S.; Rantsiou, K.; Rolle, L.; Cocolin, L. Starmerella bacillaris in winemaking: Opportunities and risks. Curr. Opin. Food Sci. 2017, 17, 30–35. [Google Scholar] [CrossRef]
- Lemos, W.J.F., Jr.; Nadai, C.; Crepalde, L.T.; de Oliveira, V.S.; de Matos, A.D.; Giacomini, A.; Corich, V. Potential use of Starmerella bacillaris as fermentation starter for the production of low-alcohol beverages obtained from unripe grapes. Int. J. Food Microbiol. 2019, 303, 1–8. [Google Scholar] [CrossRef]
- Nadai, C.; Lemos, W.J., Jr.; Favaron, F.; Giacomini, A.; Corich, V. Biocontrol activity of Starmerella bacillaris yeast against blue mold disease on apple fruit and its effect on cider fermentation. PLoS ONE 2018, 13, e0204350. [Google Scholar] [CrossRef]
- Magyar, I.; Tóth, T. Comparative evaluation of some oenological properties in wine strains of Candida stellata, Candida zemplinina, Saccharomyces uvarum and Saccharomyces cerevisiae. Food Microbiol. 2011, 28, 94–100. [Google Scholar] [CrossRef]
- Raymond Eder, M.L.; Rosa, A.L. Genetic, physiological, and industrial aspects of the fructophilic non-Saccharomyces yeast species, Starmerella bacillaris. Fermentation 2021, 7, 87. [Google Scholar] [CrossRef]
- Tufariello, M.; Fragasso, M.; Pico, J.; Panighel, A.; Castellarin, S.D.; Flamini, R.; Grieco, F. Influence of non-Saccharomyces on wine chemistry: A focus on aroma-related compounds. Molecules 2021, 26, 644. [Google Scholar] [CrossRef]
- Lemos, W.J.F., Jr.; Nadai, C.; Rolle, L.; Da Silva Gulao, E.; Miguez da Rocha Leãoe, M.H.; Giacomini, A.; Corich, V.; Vincenzi, S. Influence of the mannoproteins of different strains of Starmerella bacillaris used in single and sequential fermentations on foamability, tartaric and protein stabilities of wines. OENO ONE 2020, 54, 231–243. [Google Scholar] [CrossRef] [Green Version]
- Moreira, L.D.P.D.; Nadai, C.; da Silva Duarte, V.; Brearley-Smith, E.J.; Marangon, M.; Vincenzi, S.; Giacomini, A.; Corich, V. Starmerella bacillaris strains used in sequential alcoholic fermentation with Saccharomyces cerevisiae improves protein stability in white wines. Fermentation 2022, 8, 252. [Google Scholar] [CrossRef]
- Rosa, A.L.; Miot-Sertier, C.; Salin, F.; Sipiczki, M.; Bely, M. Draft genome sequence of the Starmerella bacillaris (syn., Candida zemplinina) type strain CBS 9494. Microbiol. Resour. Announc. 2018, 7, 3. [Google Scholar] [CrossRef] [Green Version]
- Lemos, W.J.F., Jr.; Treu, L.; Duarte, V.D.S.; Campanaro, S.; Nadai, C.; Giacomini, A.; Corich, V. Draft genome sequence of the yeast Starmerella bacillaris (syn. Candida zemplinina) FRI751 isolated from fermenting must of dried Raboso grapes. Genome Announc. 2017, 5, e00224–e00317. [Google Scholar] [CrossRef] [Green Version]
- Lemos, W.J.F., Jr.; Treu, L.; da Silva Duarte, V.; Carlot, M.; Nadai, C.; Campanaro, S.; Giacomini, A.; Corich, V. Whole-genome sequence of Starmerella bacillaris PAS13, a non-conventional enological yeast with antifungal activity. Genome Announc. 2017, 5, e00788–e00817. [Google Scholar] [CrossRef] [Green Version]
- Ko, H.-J.; Park, H.J.; Lee, S.H.; Jeong, H.; Bae, J.-H.; Sung, B.H.; Choi, I.-G.; Sohn, J.-H. Draft genome sequence of an acid-tolerant yeast, Candida zemplinina NP2, a potential producer of organic acids. Genome Announc. 2017, 5, e01052-17. [Google Scholar] [CrossRef] [Green Version]
- Lemos, W., Jr.; da Silva Duarte, V.; Treu, L.; Campanaro, S.; Nadai, C.; Giacomini, A.; Corich, V. Whole genome comparison of two Starmerella bacillaris strains with other wine yeasts uncovers genes involved in modulating important winemaking traits. FEMS Yeast Res. 2018, 18, foy069. [Google Scholar] [CrossRef]
- Lemos, W.J.F., Jr.; de Oliveira, V.S.; Guerra, A.F.; Giacomini, A.; Corich, V. From the vineyard to the cellar: New insights of Starmerella bacillaris (synonym Candida zemplinina) technological properties and genomic perspective. Appl. Microbiol. Biotechnol. 2021, 105, 493–501. [Google Scholar] [CrossRef]
- Lemos, W.J., Jr.; Bovo, B.; Nadai, C.; Crosato, G.; Carlot, M.; Favaron, F.; Giacomini, A.; Corich, V. Biocontrol ability and action mechanism of Starmerella bacillaris (synonym Candida zemplinina) isolated from wine musts against gray mold disease agent Botrytis cinerea on grape and their effects on alcoholic fermentation. Front. Microbiol. 2016, 7, 1249. [Google Scholar] [CrossRef] [PubMed]
- Rantsiou, K.; Dolci, P.; Giacosa, S.; Torchio, F.; Tofalo, R.; Torriani, S.; Suzzi, G.; Rolle, L.; Cocolin, L. Candida zemplinina can reduce acetic acid produced by Saccharomyces cerevisiae in sweet wine fermentations. Appl. Environ. Microbiol. 2012, 78, 1987–1994. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tofalo, R.; Patrignani, F.; Lanciotti, R.; Perpetuini, G.; Schirone, M.; Di Gianvito, P.; Pizzoni, D.; Arfelli, G.; Suzzi, G. Aroma profile of Montepulciano d’ Abruzzo wine fermented by single and co-culture starters of autochthonous Saccharomyces and non-Saccharomyces yeasts. Front. Microbiol. 2016, 7, 610. [Google Scholar] [CrossRef] [PubMed]
- Wang, C.; Esteve-Zarzoso, B.; Mas, A. Monitoring of Saccharomyces cerevisiae, Hanseniaspora uvarum, and Starmerella bacillaris (synonym Candida zemplinina) populations during alcoholic fermentation by fluorescence in situ hybridization. Int. J. Food Microbiol. 2014, 191, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Russo, P.; Tufariello, M.; Renna, R.; Tristezza, M.; Taurino, M.; Palombi, L.; Capozzi, V.; Rizzello, C.G.; Grieco, F. New insights into the oenological significance of Candida zemplinina: Impact of selected autochthonous strains on the volatile profile of apulian wines. Microorganisms 2020, 8, 628. [Google Scholar] [CrossRef] [PubMed]
- Englezos, V.; Rantsiou, K.; Torchio, F.; Rolle, L.; Gerbi, V.; Cocolin, L. Exploitation of the non-Saccharomyces yeast Starmerella bacillaris (synonym Candida zemplinina) in wine fermentation: Physiological and molecular characterizations. Int. J. Food Microbiol. 2015, 199, 33–40. [Google Scholar] [CrossRef]
- Ribéreau-Gayon, P.; Dubourdieu, D.; Donèche, B.; Lonvaud, A. Handbook of Enology: The Microbiology of Wine and Vinifications; John Wiley and Sons Ltd.: Chichester, UK, 2006. [Google Scholar]
- Nadai, C.; Giacomini, A.; Corich, V. The addition of wine yeast Starmerella bacillaris to grape skin surface influences must fermentation and glycerol production. OENO ONE 2021, 55, 47–55. [Google Scholar] [CrossRef]
- Bovo, B.; Nadai, C.; Vendramini, C.; Lemos, W.J., Jr.; Carlot, M.; Skelin, A.; Giacomini, A.; Corich, V. Aptitude of Saccharomyces yeasts to ferment unripe grapes harvested during cluster thinning for reducing alcohol content of wine. Int. J. Food Microbiol. 2016, 236, 56–64. [Google Scholar] [CrossRef]
- Nadai, C.; Campanaro, S.; Giacomini, A.; Corich, V. Selection and validation of reference genes for quantitative Real-Time PCR studies during Saccharomyces cerevisiae alcoholic fermentation in the presence of sulfite. Int. J. Food Microbiol. 2015, 215, 49–56. [Google Scholar] [CrossRef]
- Soares-Santos, V.; Pardo, I.; Ferrer, S. Cells-qPCR as a direct quantitative PCR method to avoid microbial DNA extractions in grape musts and wines. Int. J. Food Microbiol. 2017, 261, 25–34. [Google Scholar] [CrossRef]
- Agarbati, A.; Canonico, L.; Pecci, T.; Romanazzi, G.; Ciani, M.; Comitini, F. Biocontrol of non-saccharomyces yeasts in vineyard against the gray mold disease agent Botrytis cinerea. Microorganisms 2002, 10, 200. [Google Scholar] [CrossRef] [PubMed]
- Karabulut, O.A.; Smilanick, J.L.; Gabler, F.M.; Mansour, M.; Droby, S. Near-harvest applications of Metschnikowia fructicola, ethanol, and sodium bicarbonate to control postharvest diseases of grape in central California. Plant Dis. 2003, 87, 1384–1389. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pawlikowska, E.; James, S.A.; Breierova, E.; Antolak, H.; Kregiel, D. Biocontrol capability of local Metschnikowia sp. isolates. Antonie van Leeuwenhoek 2019, 112, 1425–1445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gobert, A.; Tourdot-Maréchal, R.; Morge, C.; Sparrow, C.; Liu, Y.; Quintanilla-Casas, B.; Vichi, S.; Alexandre, H. Non-Saccharomyces yeasts nitrogen source preferences: Impact on sequential fermentation and wine volatile compounds profile. Front. Microbiol. 2017, 8, 2175. [Google Scholar] [CrossRef] [Green Version]
- Englezos, V.; Rantsiou, K.; Cravero, F.; Torchio, F.; Ortiz-Julien, A.; Gerbi, V.; Rolle, L.; Cocolin, L. Starmerella bacillaris and Saccharomyces cerevisiae mixed fermentations to reduce ethanol content in wine. Appl. Microbiol. Biotechnol. 2016, 100, 5515–5526. [Google Scholar] [CrossRef]
- Bely, M.; Renault, P.; da Silva, T.; Masneuf-Pomarède, I.; Warren, A.; Moine, V.; Coulon, J.; Sicard, D.; de Vienne, D.; Marullo, P. Alcohol level reduction in wine. In Non-Conventional Yeasts and Alcohol Level Reduction; Teissedre, P.L., Ed.; Vigne et Vin Publications Internationales: Bordeaux, France, 2013; pp. 33–37. [Google Scholar]
- Macías, M.M.; Manso, A.G.; Orellana, C.J.G.; Velasco, H.M.G.; Caballero, R.G.; Chamizo, J.C.P. Acetic acid detection threshold in synthetic wine samples of a portable electronic nose. Sensors 2013, 13, 208–220. [Google Scholar] [CrossRef]
- Tilloy, V.; Cadière, A.; Ehsani, M.; Dequin, S. Microbiological strategies to reduce alcohol levels in wines. In Non-Conventional Yeasts and Alcohol Level Reduction; Teissedre, P.L., Ed.; Vigne et Vin Publications Internationales: Bordeaux, France, 2013; pp. 29–32. [Google Scholar]
Primer | Sequence (5′-3′) | Tm | Amplicon Length |
---|---|---|---|
Sb Fw | ATA CCG ACT GCC ATC TAT C | 65 °C | 170 bp |
Sb Rev | TAA CTG CTA CTG CTA CCT AC | 66 °C |
Sugars (g/L) | Amino Nitrogen (mg/L) | Ammonia Nitrogen (mg/L) | ||
---|---|---|---|---|
JUICE | NT | 188.33 ± 0.58 A | 71.63 ± 1.55 BC | 35.33 ± 0.58 B |
LCC | 193.67 ± 1.15 B | 67.87 ± 1.63 AB | 38.67 ± 0.58 D | |
HCC | 195.67 ± 1.53 BC | 74.90 ± 0.44 CD | 48.67 ± 0.58 E | |
CRYO | NT | 195.33 ± 1.15 BC | 77.97 ± 3.06 D | 29.33 ± 0.58 A |
LCC | 188.67 ± 1.15 A | 74.83 ± 0.86 CD | 36.67 ± 0.58 BC | |
HCC | 188.33 ± 2.08 A | 64.37 ± 1.59 A | 28.33 ± 0.58 A | |
JUICE +MARC | NT | 195.33 ± 1.15 BC | 77.63 ± 1.72 D | 37.67 ± 0.58 CD |
LCC | 188.33 ± 1.15 A | 67.17 ± 1.59 AB | 39.00 ± 1.00 D | |
HCC | 198.67 ± 0.58 C | 77.83 ± 2.89 D | 49.33 ± 0.58 E |
Sugars | YAN | ||
---|---|---|---|
JUICE | NT | 31.67 ± 3.32 B | 97.20 ± 0.90 D |
LCC | 4.98 ± 2.80 C | 38.97 ± 5.14 C | |
HCC | 4.26 ± 0.75 C | 35.07 ± 1.08 BC | |
CRYO | NT | 29.70 ± 1.06 B | 97.22 ± 0.86 D |
LCC | 4.41 ± 1.19 C | 30.50 ± 3.21 BC | |
HCC | 2.12 ± 1.40 C | 26.77 ± 3.45 B | |
JUICE +MARC | NT | 42.66 ± 0.77 A | 95.38 ± 1.28 D |
LCC | 0.00 ± 0.00 - | 0.00 ± 0.00 - | |
HCC | 6.21 ± 2.47 C | 12.64 ± 2.44 A |
Ethanol (% v/v) | Acetic Acid (g/L) | Glycerol (g/L) | ||
---|---|---|---|---|
JUICE | NT | 12.65 ± 0.10 E | 0.16 ± 0.01 BC | 5.94 ± 0.30 AB |
LCC | 12.45 ± 0.02 DE | 0.21 ± 0.03 CD | 6.31 ± 0.11 AB | |
HCC | 12.64 ± 0.19 E | 0.50 ± 0.02 F | 9.11 ± 0.97 E | |
CRYO | NT | 12.55 ± 0.02 DE | 0.13 ± 0.01 AB | 5.78 ± 0.06 A |
LCC | 12.06 ± 0.03 AB | 0.47 ± 0.03 EF | 7.71 ± 0.19 CD | |
HCC | 12.31 ± 0.02 BCD | 0.43 ± 0.02 E | 8.02 ± 0.06 CDE | |
JUICE +MARC | NT | 12.14 ± 0.05 BC | 0.24 ± 0.02 D | 5.82 ± 0.24 AB |
LCC | 11.83 ± 0.16 A | 0.09 ± 0.02 A | 6.90 ± 0.43 BC | |
HCC | 12.41 ± 0.09 CDE | 0.19 ± 0.02 CD | 8.10 ± 0.23 DE |
NT | LCC | HCC | |
---|---|---|---|
JUICE | 0.032 ± 0.002 A | 0.033 ± 0.000 A | 0.047 ± 0.005 B |
NT | LCC | HCC | |
CRYO | 0.030 ± 0.000 A | 0.041 ± 0.001 B | 0.043 ± 0.000 B |
NT | LCC | HCC | |
JUICE+ MARC | 0.030 ± 0.001 A | 0.037 ± 0.002 B | 0.041 ± 0.001 B |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 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
Nadai, C.; da Silva Duarte, V.; Sica, J.; Vincenzi, S.; Carlot, M.; Giacomini, A.; Corich, V. Starmerella bacillaris Released in Vineyards at Different Concentrations Influences Wine Glycerol Content Depending on the Vinification Protocols. Foods 2023, 12, 3. https://doi.org/10.3390/foods12010003
Nadai C, da Silva Duarte V, Sica J, Vincenzi S, Carlot M, Giacomini A, Corich V. Starmerella bacillaris Released in Vineyards at Different Concentrations Influences Wine Glycerol Content Depending on the Vinification Protocols. Foods. 2023; 12(1):3. https://doi.org/10.3390/foods12010003
Chicago/Turabian StyleNadai, Chiara, Vinícius da Silva Duarte, Jacopo Sica, Simone Vincenzi, Milena Carlot, Alessio Giacomini, and Viviana Corich. 2023. "Starmerella bacillaris Released in Vineyards at Different Concentrations Influences Wine Glycerol Content Depending on the Vinification Protocols" Foods 12, no. 1: 3. https://doi.org/10.3390/foods12010003
APA StyleNadai, C., da Silva Duarte, V., Sica, J., Vincenzi, S., Carlot, M., Giacomini, A., & Corich, V. (2023). Starmerella bacillaris Released in Vineyards at Different Concentrations Influences Wine Glycerol Content Depending on the Vinification Protocols. Foods, 12(1), 3. https://doi.org/10.3390/foods12010003