Abstract
Commercial Saccharomyces strains are usually inoculated to ferment alcoholic beverages due to their ability to convert all fermentable sugars into ethanol. However, modern trends in winemaking have turned toward less known, non-Saccharomyces yeast species. These species perform the first stages of natural spontaneous fermentation and play important roles in wine variety. New alcoholic fermentation trends have begun to consider objectives other than alcohol production to improve flavor diversity. This review explores the influence of the most used and commercialized non-Saccharomyces yeast, Torulaspora delbrueckii, on fermentation quality parameters, such as ethanol, glycerol, volatile acidity, volatile profile, succinic acid, mannoproteins, polysaccharides, color, anthocyanins, amino acids, and sensory perception.
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References
Alves-Araujo C, Almeida MJ, Sousa MJ, Leao C (2004) Freeze tolerance of the yeast Torulaspora delbrueckii: cellular and biochemical basis. FEMS Microbiol Lett 240:7–14. https://doi.org/10.1016/j.femsle.2004.09.008
Azzolini M, Fedrizzi B, Tosi E, Finato F, Vagnoli P, Scrinzi C, Zapparoli G (2012) Effects of Torulaspora delbrueckii and Saccharomyces cerevisiae mixed cultures on fermentation and aroma of Amarone wine. Eur Food Res Technol 235:303–313. https://doi.org/10.1007/s00217-012-1762-3
Azzolini M, Tosi E, Lorenzini M, Finato F, Zapparoli G (2015) Contribution to the aroma of white wines by controlled Torulaspora delbrueckii cultures in association with Saccharomyces cerevisiae. World J Microbiol Biotechnol 31:277–293. https://doi.org/10.1007/s11274-014-1774-1
Balikci EK, Tanguler H, Jolly NP, Erten H (2016) Influence of Lachancea thermotoleranson cv. Emir wine fermentation. Yeast 33:313–321. https://doi.org/10.1002/yea.3166
Bañuelos MA, Loira I, Escott C, Del Fresno JM, Morata A, Sanz PD, Otero L, Suárez-Lepe JA (2016) Grape processing by high hydrostatic pressure: effect on use of non-Saccharomyces in must fermentation. Food Bioprocess Technol 9:1769–1778. https://doi.org/10.1007/s11947-016-1760-8
Basso RF, Alcarde AR, Portugal CB (2016) Could non-Saccharomyces yeasts contribute on innovative brewing fermentations? Food Res Int 86:112–120. https://doi.org/10.1016/j.foodres.2016.06.002
Belda I, Navascués E, Marquina D, Santos A, Calderon F, Benito S (2015) Dynamic analysis of physiological properties of Torulaspora delbrueckii in wine fermentations and its incidence on wine quality. Appl Microbiol Biotechnol 99:1911–1922. https://doi.org/10.1007/s00253-014-6197-2
Belda I, Navascués E, Marquina D, Santos A, Calderón F, Benito S (2016a) Outlining the influence of non-conventional yeasts in wine ageing over lees. Yeast 33:329–338. https://doi.org/10.1002/yea.3165
Belda I, Ruiz J, Beisert B, Navascués E, Marquina D, Calderón F, Rauhut D, Benito S, Santos A (2017) Influence of Torulaspora delbrueckii in varietal thiol (3-SH and 4-MSP) release in wine sequential fermentations. Int J Food Microbiol 257:183–191. https://doi.org/10.1016/j.ijfoodmicro.2017.06.028
Belda I, Ruiz J, Navascués E, Marquina D, Santos A (2016b) Improvement of aromatic thiol release through the selection of yeasts with increased β-lyase activity. Int J Food Microbiol 225:1–8. https://doi.org/10.1016/j.ijfoodmicro.2016.03.001
Bely M, Stoeckle P, Masneuf-Pomarède I, Dubourdieu D (2008) Impact of mixed Torulaspora delbrueckii–Saccharomyces cerevisiae culture on high-sugar fermentation. Int J Food Microbiol 122:312–320. https://doi.org/10.1016/j.ijfoodmicro.2007.12.023
Benito A, Calderon F, Benito S (2017) The combined use of Schizosaccharomyces pombe and Lachancea thermotolerans-effect on the anthocyanin wine composition. Molecules 22:739. https://doi.org/10.3390/molecules22050739
Benito Á, Calderón F, Benito S (2016a) Combined use of S. pombe and L. thermotolerans in winemaking. Beneficial effects determined through the study of wines’ analytical characteristics. Molecules 21:1744. https://doi.org/10.3390/molecules21121744
Benito Á, Calderón F, Palomero F, Benito S (2015a) Combine use of selected Schizosaccharomyces pombe and Lachancea thermotolerans yeast strains as an alternative to thetraditional malolactic fermentation in red wine production. Molecules 20:9510–9523. https://doi.org/10.3390/molecules20069510
Benito Á, Jeffares D, Palomero F, Calderón F, Bai F-Y, Bähler J, Benito S (2016b) Selected Schizosaccharomyces pombe strains have characteristics that are beneficial for winemaking. PLoS One 11:e0151102. https://doi.org/10.1371/journal.pone.0151102
Benito S, Hofmann T, Laier M, Lochbühler B, Schüttler A, Ebert K, Fritsch S, Röcker J, Rauhut D (2015b) Effect on quality and composition of Riesling wines fermented by sequential inoculation with non-Saccharomyces and Saccharomyces cerevisiae. Eur Food Res Technol 241:707–717. https://doi.org/10.1007/s00217-015-2497-8
Benito S, Morata A, Palomero F, González MC, Suárez-Lepe JA (2011) Formation of vinylphenolic pyranoanthocyanins by Saccharomyces cerevisiae and Pichia guillermondii in red wines produced following different fermentation strategies. Food Chem 124:15–23. https://doi.org/10.1016/j.foodchem.2010.05.096
Benito S, Palomero F, Morata A, Uthurry C, Suárez-Lepe JA (2009) Minimization of ethylphenol precursors in red wines via the formation of pyranoanthocyanins by selected yeasts. Int J Food Microbiol 132:145–152. https://doi.org/10.1016/j.ijfoodmicro.2009.04.015
Bonciani T, Solieri L, De Vero L, Giudici P (2016) Improved wine yeasts by direct mating and selection under stressful fermentative conditions. Eur Food Res Technol 242:899–910. https://doi.org/10.1007/s00217-015-2596-6
Bonestroo MH, de Wit JC, Kusters BJM, Rombouts FM (1993) Inhibition of the growth of yeasts in fermented salads. Int J Food Microbiol 17:311–320. https://doi.org/10.1016/0168-1605(93)90201-q
Canonico L, Comitini F, Ciani M (2017) Torulaspora delbrueckii contribution in mixed brewing fermentations with different Saccharomyces cerevisiae strains. Int J Food Microbiol 259:7–13. https://doi.org/10.1016/j.ijfoodmicro.2017.07.017
Chen D, Liu S-Q (2016) Impact of simultaneous and sequential fermentation with Torulaspora delbrueckii and Saccharomyces cerevisiae on non-volatiles and volatiles of lychee wines. LWT Food Sci Technol 65:53–61. https://doi.org/10.1016/j.lwt.2015.07.050
Chen D, Yap ZY, Liu S-Q (2015) Evaluation of the performance of Torulaspora delbrueckii, Williopsis saturnus, and Kluyveromyces lactis in lychee wine fermentation. Int J Food Microbiol 206:45–50. https://doi.org/10.1016/j.ijfoodmicro.2015.04.020
Chen K, Escott C, Loira I, del Fresno JM, Morata A, Tesfaye W, Calderon F, Suárez-Lepe JA, Han S, Benito S (2018) Use of non-Saccharomyces yeasts and oenological tannin in red winemaking: influence on colour, aroma and sensorial properties of young wines. Food Microbiol 69:51–63. https://doi.org/10.1016/j.fm.2017.07.018
Ciani M, Maccarelli F (1998) Oenological properties of non Saccharomyces yeasts associated with winemaking. World J Microbiol Biotechnol 14:199–203. https://doi.org/10.1023/a:1008825928354
Ciani M, Morales P, Comitini F, Tronchoni J, Canonico L, Curiel JA, Oro L, Rodrigues AJ, Gonzalez R (2016) Non-conventional yeast species for lowering ethanol content of wines. Front Microbiol 7:642. https://doi.org/10.3389/fmicb.2016.00642
Contreras A, Hidalgo C, Henschke PA, Chambers PJ, Curtin C, Varela C (2014) Evaluation of non-Saccharomyces yeasts for the reduction of alcohol content in wine. Appl Environ Microbiol 80:1670–1678. https://doi.org/10.1128/aem.03780-13
Cordero-Bueso G, Esteve-Zarzoso B, Cabellos JM, Gil-Díaz M, Arroyo T (2013) Biotechnological potential of non-Saccharomyces yeasts isolated during spontaneous fermentations of Malvar (Vitis vinifera cv. L.) Eur Food Res Technol 236:193–207. https://doi.org/10.1007/s00217-012-1874-9
Cus F, Jenko M (2013) The influence of yeast strains on the composition and sensory quality of Gewürztraminer wine. Food Technol Biotechnol 51:547–553
Deák T (2008) Handbook of food spoilage yeasts, 2nd edn. CRC Press, Boca Raton
Domizio P, Liu Y, Bisson LF, Barile D (2014) Use of non-Saccharomyces wine yeasts as novel sources of mannoproteins in wine. Food Microbiol 43:5–15. https://doi.org/10.1016/j.fm.2014.04.005
Domizio P, Liu Y, Bisson LF, Barile D (2017) Cell wall polysaccharides released during the alcoholic fermentation by Schizosaccharomyces pombe and S. japonicus: quantification and characterization. Food Microbiol 61:136–149. https://doi.org/10.1016/j.fm.2016.08.010
Du Plessis H, Du Toit M, Hoff J, Hart R, Ndimba B, Jolly N (2017) Characterisation of non-Saccharomyces yeasts using different methodologies and evaluation of their compatibility with malolactic fermentation. South Afr J Enol Vitic 38:46–63. https://doi.org/10.21548/38-1-819
Dubourdieu D, Tominaga T, Masneuf I, des Gachons CP, Murat ML (2006) The role of yeasts in grape flavor development during fermentation: the example of sauvignon blanc. Am J Enol Vitic 57:81–88
Escribano R, González-Arenzana L, Portu J, Garijo P, López-Alfaro I, López R, Santamaría P, Gutiérrez AR (2018) Aromatic compound production and fermentative behavior within different non-Saccharomyces species and clones. J Appl Microbiol, Accepted
Fedrizzi B, Pardon KH, Sefton MA, Elsey GM, Jeffery DW (2009) First identification of 4-S-glutathionyl-4-methylpentan-2-one, a potential precursor of 4-mercapto-4-methylpentan-2-one, in sauvignon blanc juice. J Agric Food Chem 57:991–995. https://doi.org/10.1021/jf802799w
Fleet GH, Heard GM (1993) Yeasts: growth during fermentation. In: Fleet GH (ed) Wine microbiol biotechnol. Harwood Academic Publishers, Chur, Switzerland, pp 27–54
Fleet G (2006) The commercial and community significance of yeasts in food and beverage production. In: Querol A, Fleet GH (eds) Yeasts in food and beverages. Springer, Berlin, Heidelberg, pp 1–12
Fröhlich-Wyder MT (2003) Yeasts in foods. Beneficial and detrimental aspects. In: Boekhout T, Robert V (eds) Yeasts in food: beneficial and detrimental aspects. Behr’s Verlag, Hamburg, pp 209–237
Gamero A, Quintilla R, Groenewald M, Alkema W, Boekhout T, Hazelwood L (2016) High-throughput screening of a large collection of non-conventional yeasts reveals their potential for aroma formation in food fermentation. Food Microbiol 60:147–159. https://doi.org/10.1016/j.fm.2016.07.006
García M, Apolinar-Valiente R, Williams P, Esteve-Zarzoso B, Arroyo T, Crespo J, Doco T (2017) Polysaccharides and oligosaccharides produced on malvar wines elaborated with Torulaspora delbrueckii CLI 918 and Saccharomyces cerevisiae CLI 889 native yeasts from D.O. “vinos de madrid”. J Agric Food Chem 65:6656–6664. https://doi.org/10.1021/acs.jafc.7b01676
Gonzalez-Ramos D, Cebollero E, Gonzalez R (2008) A recombinant Saccharomyces cerevisiae strain overproducing mannoproteins stabilizes wine against protein haze. Appl Environ Microbiol 74:5533–5540. https://doi.org/10.1128/aem.00302-08
González-Royo E, Pascual O, Kontoudakis N, Esteruelas M, Esteve-Zarzoso B, Mas A, Canals JM, Zamora F (2015) Oenological consequences of sequential inoculation with non-Saccharomyces yeasts (Torulaspora delbrueckii or Metschnikowia pulcherrima) and Saccharomyces cerevisiae in base wine for sparkling wine production. Eur Food Res Technol 240:999–1012. https://doi.org/10.1007/s00217-014-2404-8
Jolly N, Augustyn O, Pretorius I (2003a) The use of Candida pulcherrima in combination with Saccharomyces cerevisiae for the production of Chenin blanc wine. South Afr J Enol Vitic 24:63–69. https://doi.org/10.21548/24-2-2641
Jolly NP, Augustyn OPH, Pretorius IS (2003b) The effect of non-Saccharomyces yeasts on fermentation and wine quality. South Afr J Enol Vitic 24:55–62. https://doi.org/10.21548/24-2-2638
Jolly NP, Varela C, Pretorius IS (2014) Not your ordinary yeast: non-Saccharomycesyeasts in wine production uncovered. FEMS Yeast Res 14:215–237. https://doi.org/10.1111/1567-1364.12111
Kurtzman CP (2011) Torulaspora lindner (1904). In: Kurtzman C, Fell JW, Boekhout T (eds) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam, pp 867–874
Loira I, Vejarano R, Bañuelos MA, Morata A, Tesfaye W, Uthurry C, Villa A, Cintora I, Suárez-Lepe JA (2014) Influence of sequential fermentation with Torulaspora delbrueckii and Saccharomyces cerevisiae on wine quality. LWT Food Sci Technol 59:915–922. https://doi.org/10.1016/j.lwt.2014.06.019
Lu Y, Chua J-Y, Huang D, Lee P-R, Liu S-Q (2016) Biotransformation of chemical constituents of durian wine with simultaneous alcoholic fermentation by Torulaspora delbrueckii and malolactic fermentation by Oenococcus oeni. Appl Microbiol Biotechnol 100:8877–8888. https://doi.org/10.1007/s00253-016-7720-4
Magyar I, Tóth T (2011) Comparative evaluation of some oenological properties in wine strains of Candida stellata, Candida zemplinina, Saccharomyces uvarum and Saccharomyces cerevisiae. Food Microbiol 28:94–100. https://doi.org/10.1016/j.fm.2010.08.011
Medina-Trujillo L, González-Royo E, Sieczkowski N, Heras J, Canals JM, Zamora F (2017) Effect of sequential inoculation (Torulaspora delbrueckii/Saccharomyces cerevisiae) in the first fermentation on the foaming properties of sparkling wine. Eur Food Res Technol 243:681–688. https://doi.org/10.1007/s00217-016-2781-2
Milanovic V, Ciani M, Oro L, Comitini F (2012) Starmerella bombicola influences the metabolism of Saccharomyces cerevisiae at pyruvate decarboxylase and alcohol dehydrogenase level during mixed wine fermentation. Microb Cell Factories 11:18. https://doi.org/10.1186/1475-2859-11-18
Minnaar P, Ntushelo N, Ngqumba Z, Van Breda V, Jolly N (2015) Effect of Torulaspora delbrueckii yeast on the anthocyanin and flavanol concentrations of Cabernet franc and Pinotage wines. South Afr J Enol Vitic 36:50–58
Morales P, Rojas V, Quirós M, Gonzalez R (2015) The impact of oxygen on the final alcohol content of wine fermented by a mixed starter culture. Appl Microbiol Biotechnol 99:3993–4003. https://doi.org/10.1007/s00253-014-6321-3
Ngqumba Z, Ntushelo N, Jolly N, Ximba B, Minnaar P (2017) Effect of Torulaspora delbrueckii yeast treatment on flavanols and phenolic acids of Chenin blanc wines. South Afr J Enol Vitic 38:192–200. https://doi.org/10.21548/38-2-1391
Padilla B, Gil JV, Manzanares P (2016) Past and future of non-Saccharomyces yeasts: from spoilage microorganisms to biotechnological tools for improving wine aroma complexity. Front Microbiol 7:411. https://doi.org/10.3389/fmicb.2016.00411
Petruzzi L, Capozzi V, Berbegal C, Corbo MR, Bevilacqua A, Spano G, Sinigaglia M (2017) Microbial resources and enological significance: opportunities and benefits. Front Microbiol 8:995. https://doi.org/10.3389/fmicb.2017.00995
Puertas B, Jiménez MJ, Cantos-Villar E, Cantoral JM, Rodríguez ME (2017) Use of Torulaspora delbrueckii and Saccharomyces cerevisiae in semi-industrial sequential inoculation to improve quality of palomino and chardonnay wines in warm climates. J Appl Microbiol 122:733–746. https://doi.org/10.1111/jam.13375
Ramírez M, Velázquez R, Maqueda M, López-Piñeiro A, Ribas JC (2015) A new wine Torulaspora delbrueckii killer strain with broad antifungal activity and its toxin-encoding double-stranded RNA virus. Front Microbiol 6:983. https://doi.org/10.3389/fmicb.2015.00983
Ramírez M, Velázquez R, Maqueda M, Zamora E, López-Piñeiro A, Hernández LM (2016) Influence of the dominance of must fermentation by Torulaspora delbrueckii on the malolactic fermentation and organoleptic quality of red table wine. Int J Food Microbiol 238:311–319. https://doi.org/10.1016/j.ijfoodmicro.2016.09.029
Renault P, Coulon J, de Revel G, Barbe J-C, Bely M (2015) Increase of fruity aroma during mixed T. delbrueckii/S. cerevisiae wine fermentation is linked to specific esters enhancement. Int J Food Microbiol 207:40–48. https://doi.org/10.1016/j.ijfoodmicro.2015.04.037
Renault P, Coulon J, Moine V, Thibon C, Bely M (2016) Enhanced 3-sulfanylhexan-1-ol production in sequential mixed fermentation with Torulaspora delbrueckii/Saccharomyces cerevisiae reveals a situation of synergistic interaction between two industrial strains. Front Microbiol 7:293. https://doi.org/10.3389/fmicb.2016.00293
Renault P, Miot-Sertier C, Marullo P, Hernández-Orte P, Lagarrigue L, Lonvaud-Funel A, Bely M (2009) Genetic characterization and phenotypic variability in Torulaspora delbrueckii species: potential applications in the wine industry. Int J Food Microbiol 134:201–210. https://doi.org/10.1016/j.ijfoodmicro.2009.06.008
Röcker J, Schmitt M, Pasch L, Ebert K, Grossmann M (2016b) The use of glucose oxidase and catalase for the enzymatic reduction of the potential ethanol content in wine. Food Chem 210:660–670. https://doi.org/10.1016/j.foodchem.2016.04.093
Röcker J, Strub S, Ebert K, Grossmann M (2016a) Usage of different aerobic non-Saccharomyces yeasts and experimental conditions as a tool for reducing the potential ethanol content in wines. Eur Food Res Technol 242:2051–2070. https://doi.org/10.1007/s00217-016-2703-3
Sadineni V, Kondapalli N, Obulam VSR (2012) Effect of co-fermentation with Saccharomyces cerevisiae and Torulaspora delbrueckii or Metschnikowia pulcherrima on the aroma and sensory properties of mango wine. Ann Microbiol 62:1353–1360. https://doi.org/10.1007/s13213-011-0383-6
Sadoudi M, Tourdot-Maréchal R, Rousseaux S, Steyer D, Gallardo-Chacón J-J, Ballester J, Vichi S, Guérin-Schneider R, Caixach J, Alexandre H (2012) Yeast–yeast interactions revealed by aromatic profile analysis of sauvignon blanc wine fermented by single or co-culture of non-Saccharomyces and Saccharomyces yeasts. Food Microbiol 32:243–253. https://doi.org/10.1016/j.fm.2012.06.006
Swiegers JH, Bartowsky EJ, Henschke PA, Pretorius IS (2005) Yeast and bacterial modulation of wine aroma and flavour. Aust J Grape Wine Res 11:139–173. https://doi.org/10.1111/j.1755-0238.2005.tb00285.x
Swiegers JH, Pretorius IS (2007) Modulation of volatile sulfur compounds by wine yeast. Appl Microbiol Biotechnol 74:954–960. https://doi.org/10.1007/s00253-006-0828-1
Taillandier P, Lai QP, Julien-Ortiz A, Brandam C (2014) Interactions between Torulaspora delbrueckii and Saccharomyces cerevisiae in wine fermentation: influence of inoculation and nitrogen content. World J Microbiol Biotechnol 30:1959–1967. https://doi.org/10.1007/s11274-014-1618-z
Tominaga T, Masneuf I, Dubourdieu D (1996) Mise en evidence d'un S-conjugue de la cysteine, precurseur d'arome du Sauvignon [4-methyl-4-mercaptopentan-2-one; betalyase]. J Int Sci Vigne Vin 29:227–232
Varela C (2016) The impact of non-Saccharomyces yeasts in the production of alcoholic beverages. Appl Microbiol Biotechnol 100:9861–9874. https://doi.org/10.1007/s00253-016-7941-6
Varela C, Sengler F, Solomon M, Curtin C (2016) Volatile flavour profile of reduced alcohol wines fermented with the non-conventional yeast species Metschnikowia pulcherrima and Saccharomyces uvarum. Food Chem 209:57–64. https://doi.org/10.1016/j.foodchem.2016.04.024
Velazquez R, Zamora E, Alvarez ML, Hernandez LM, Ramirez M (2015) Effects of new Torulaspora delbrueckii killer yeasts on the must fermentation kinetics and aroma compounds of white table wine. Front Microbiol 6:1222. https://doi.org/10.3389/fmicb.2015.01222
Villalba ML, Susana Sáez J, del Monaco S, Lopes CA, Sangorrín MP (2016) TdKT, a new killer toxin produced by Torulaspora delbrueckii effective against wine spoilage yeasts. Int J Food Microbiol 217:94–100. https://doi.org/10.1016/j.ijfoodmicro.2015.10.006
Visintin S, Ramos L, Batista N, Dolci P, Schwan F, Cocolin L (2017) Impact of Saccharomyces cerevisiae and Torulaspora delbrueckii starter cultures on cocoa beans fermentation. Int J Food Microbiol 257:31–40. https://doi.org/10.1016/j.ijfoodmicro.2017.06.004
Wang C, Mas A, Esteve-Zarzoso B (2016) The interaction between Saccharomyces cerevisiae and non-Saccharomyces yeast during alcoholic fermentation is species and strain specific. Front Microbiol 7:502. https://doi.org/10.3389/fmicb.2016.00502
Whitener MEB, Stanstrup J, Carlin S, Divol B, Du Toit M, Vrhovsek U (2017) Effect of non-Saccharomyces yeasts on the volatile chemical profile of Shiraz wine. Aust J Grape Wine Res 23:179–192. https://doi.org/10.1111/ajgw.12269
Zott K, Thibon C, Bely M, Lonvaud-Funel A, Dubourdieu D, Masneuf-Pomarede I (2011) The grape must non-Saccharomyces microbial community: impact on volatile thiol release. Int J Food Microbiol 151:210–215. https://doi.org/10.1016/j.ijfoodmicro.2011.08.026
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Funding for the research in this paper was provided by Ossian Vides y Vinos S.L, under the framework of the project FPA1720300120 IDI-20170703 (Centre for Industrial Technological Development-CDTI, Spain).
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Benito, S. The impact of Torulaspora delbrueckii yeast in winemaking. Appl Microbiol Biotechnol 102, 3081–3094 (2018). https://doi.org/10.1007/s00253-018-8849-0
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DOI: https://doi.org/10.1007/s00253-018-8849-0