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The impact of non-Saccharomyces yeasts in the production of alcoholic beverages

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Abstract

The conversion of fermentable sugars into alcohol during fermentation is the key process in the production of all alcoholic beverages. However, microbial activity during fermentation is considerably more complex than merely producing ethanol, usually involving the action of a great diversity of yeasts and bacteria and the production of metabolites that affect the organoleptic properties of fermented beverages. Non-Saccharomyces yeasts, which are naturally present in un-inoculated, spontaneous fermentations, can provide a means for increasing aroma and flavour diversity in fermented beverages. This review will cover the impacts of non-Saccharomyces yeasts on volatile composition and sensory profile of beer, wine, spirits and other fermented beverages, and look at future opportunities involving yeast interactions and regionality in alcoholic beverages.

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References

  • Alba-Lois L, Segal-Kischinevzky C (2010). Yeast fermentation and the making of beer and wine. Scitable, Nature Education

  • Albertin W, Setati ME, Miot-Sertier C, Mostert TT, Colonna-Ceccaldi B, Coulon J, Girard P, Moine V, Pillet M, Salin F, Bely M, Divol B, Masneuf-Pomarede I (2016) Hanseniaspora uvarum from winemaking environments show spatial and temporal genetic clustering. Front Microbiol 6:16

    Article  Google Scholar 

  • Alexander M, Jeffries T (1990) Respiratory efficiency and metabolite partitioning as regulatory phenomena in yeasts. Enzym Microb Technol 12:2–19

    Article  CAS  Google Scholar 

  • Aung MT, Lee PR, Yu B, Liu SQ (2015) Cider fermentation with three Williopsis saturnus yeast strains and volatile changes. Ann Microbiol 65:921–928

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Baidya D, Chakraborty I, Saha J (2016) Table wine from tropical fruits utilizing natural yeast isolates. J Food Sci Tech Mys 53:1663–1669

    Article  CAS  Google Scholar 

  • Baker E, Wang B, Bellora N, Peris D, Hulfachor AB, Koshalek JA, Adams M, Libkind D, Hittinger CT (2015) The genome sequence of Saccharomyces eubayanus and the domestication of lager-brewing yeasts. Mol Biol Evol 32:2818–2831

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartowsky EJ, Costello PJ, Chambers PJ (2015) Emerging trends in the application of malolactic fermentation. Aust J Grape Wine Res 21:663–669

    Article  Google Scholar 

  • Basso RF, Alcarde AR, Portugal CB (2016) Could non-Saccharomyces yeasts contribute on innovative brewing fermentations? Food Res Int 86

  • Belda I, Conchillo LB, Ruiz J, Navascues E, Marquina D, Santos A (2016a) Selection and use of pectinolytic yeasts for improving clarification and phenolic extraction in winemaking. Int J Food Microbiol 223:1–8

    Article  CAS  PubMed  Google Scholar 

  • Belda I, Navascues 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 Biot 99:1911–1922

    Article  CAS  Google Scholar 

  • Belda I, Ruiz J, Navascues E, Marquina D, Santos A (2016b) Improvement of aromatic thiol release through the selection of yeasts with increased beta-lyase activity. Int J Food Microbiol 225:1–8

    Article  CAS  PubMed  Google Scholar 

  • Benito A, Calderon F, Palomero F, Benito S (2015a) Combine use of selected Schizosaccharomyces pombe and Lachancea thermotolerans yeast strains as an alternative to the traditional malolactic fermentation in red wine production. Molecules 20:9510–9523

    Article  CAS  PubMed  Google Scholar 

  • Benito S, Hofmann T, Laier M, Lochbuehler B, Schuettler A, Ebert K, Fritsch S, Roecker 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

    Article  CAS  Google Scholar 

  • Bokulich NA, Mills DA (2012) Microbial terroir of wine: deep insight into site-specific winery and vineyard microbial communities. Am J Enol Viticult 63:435a–435a

    Article  CAS  Google Scholar 

  • Bokulich NA, Bamforth CW, Mills DA (2012) Brewhouse-resident microbiota are responsible for multi-stage fermentation of American coolship ale. PLoS One 7:e35507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bovo B, Fontana F, Giacomini A, Corich V (2011) Effects of yeast inoculation on volatile compound production by grape marcs. Ann Microbiol 61:117–124

    Article  CAS  Google Scholar 

  • Brady M (2008) The first taste of alcohol. Alcohol Education & Rehabilitation Foundation Ltd, Deakin

    Google Scholar 

  • Canonico L, Agarbati A, Comitini F, Ciani M (2016a) Torulaspora delbrueckii in the brewing process: a new approach to enhance bioflavour and to reduce ethanol content. Food Microbiol 56:45–51

    Article  CAS  PubMed  Google Scholar 

  • Canonico L, Comitini F, Ciani M (2015) Influence of vintage and selected starter on Torulaspora delbrueckii/Saccharomyces cerevisiae sequential fermentation. Eur Food Res Technol 241:827–833

    Article  CAS  Google Scholar 

  • Canonico L, Comitini F, Oro L, Ciani M (2016b) Sequential fermentation with selected immobilized non-Saccharomyces yeast for reduction of ethanol content in wine. Front Microbiol 7

  • Capece A, Pietrafesa R, Romano P (2011) Experimental approach for target selection of wild wine yeasts from spontaneous fermentation of "Inzolia" grapes. World J Microbiol Biotechnol 27:2775–2783

    Article  CAS  Google Scholar 

  • Cavalieri D, McGovern P, Hartl D, Mortimer R, Polsinelli M (2003) Evidence for S. cerevisiae fermentation in ancient wine. J Mol Evol 57:S226–S232

    Article  CAS  PubMed  Google Scholar 

  • Chen D, Liu SQ (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

    Article  CAS  Google Scholar 

  • Chen D, Liu S-Q (2014) Chemical and volatile composition of lychee wines fermented with four commercial Saccharomyces cerevisiae yeast strains. Int J Food Sci Tech 49:521–530

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ciani M, Comitini F, Mannazzu I, Domizio P (2010) Controlled mixed culture fermentation: a new perspective on the use of non-Saccharomyces yeasts in winemaking. FEMS Yeast Res 10:123–133

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Contreras A, Curtin C, Varela C (2015a) Yeast population dynamics reveal a potential 'collaboration' between Metschnikowia pulcherrima and Saccharomyces uvarum for the production of reduced alcohol wines during Shiraz fermentation. Appl Microbiol Biot 99:1885–1895

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Contreras A, Hidalgo C, Schmidt S, Henschke PA, Curtin C, Varela C (2015b) The application of non-Saccharomyces yeast in fermentations with limited aeration as a strategy for the production of wine with reduced alcohol content. Int J Food Microbiol 205:7–15

    Article  CAS  PubMed  Google Scholar 

  • Cordero-Bueso G, Esteve-Zarzoso B, Mariano Cabellos J, Gil-Diaz 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

    Article  CAS  Google Scholar 

  • Cus F, Jenko M (2013) The influence of yeast strains on the composition and sensory quality of Gewurztraminer wine. Food Technol Biotech 51:547–553

    CAS  Google Scholar 

  • Daenen L, Saison D, Sterckx F, Delvaux FR, Verachtert H, Derdelinckx G (2008a) Screening and evaluation of the glucoside hydrolase activity in Saccharomyces and Brettanomyces brewing yeasts. J Appl Microbiol 104:478–488

    CAS  PubMed  Google Scholar 

  • Daenen L, Sterckx F, Delvaux FR, Verachtert H, Derdelinckx G (2008b) Evaluation of the glycoside hydrolase activity of a Brettanomyces strain on glycosides from sour cherry (Prunus cerasus L.) used in the production of special fruit beers. FEMS Yeast Res 8:1103–1114

    Article  CAS  PubMed  Google Scholar 

  • Dashko S, Zhou N, Tinta T, Sivilotti P, Lemut MS, Trost K, Gamero A, Boekhout T, Butinar L, Vrhovsek U, Piskur J (2015) Use of non-conventional yeast improves the wine aroma profile of Ribolla Gialla. J Ind Microbiol Biot 42:997–1010

    Article  CAS  Google Scholar 

  • De Francesco G, Turchetti B, Sileoni V, Marconi O, Perretti G (2015) Screening of new strains of Saccharomycodes ludwigii and Zygosaccharomyces rouxii to produce low-alcohol beer. J I Brewing 121:113–121

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Duarte WF, Amorim JC, Schwan RF (2013) The effects of co-culturing non-Saccharomyces yeasts with S. cerevisiae on the sugar cane spirit cachaca fermentation process. Anton Leeuw Int J G 103:175–194

    Article  CAS  Google Scholar 

  • Easingwood C, Lockshin L, Spawton A (2011) The drivers of wine regionality. J Wine Res 22:19–33

    Article  Google Scholar 

  • Englezos V, Rantsiou K, Cravero F, Torchio F, Ortiz-Julien A, Gerbi V, Rolle L, Cocolin L (2016a) Starmerella bacillaris and Saccharomyces cerevisiae mixed fermentations to reduce ethanol content in wine. Appl Microbiol Biot 100:5515–5526

    Article  CAS  Google Scholar 

  • Englezos V, Torchio F, Cravero F, Marengo F, Giacosa S, Gerbi V, Rantsiou K, Rolle L, Cocolin L (2016b) Aroma profile and composition of Barbera wines obtained by mixed fermentations of Starmerella bacillaris (synonym Candida zemplinina) and Saccharomyces cerevisiae. LWT–Food Science and Technology

  • Garavaglia J, de Souza Schneider RC, Camargo Mendes SD, Welke JE, Zini CA, Caramao EB, Valente P (2015) Evaluation of Zygosaccharomyces bailii BCV 08 as a co-starter in wine fermentation for the improvement of ethyl esters production. Microbiol Res 173:59–65

    Article  CAS  PubMed  Google Scholar 

  • Garofalo C, Tristezza M, Grieco F, Spano G, Capozzi V (2016) From grape berries to wine: population dynamics of cultivable yeasts associated to “Nero di Troia” autochthonous grape cultivar. World J Microbiol Biotechnol 32

  • Gobbi M, Comitini F, Domizio P, Romani C, Lencioni L, Mannazzu I, Ciani M (2013) Lachancea thermotolerans and Saccharomyces cerevisiae in simultaneous and sequential co-fermentation: a strategy to enhance acidity and improve the overall quality of wine. Food Microbiol 33:271–281

    Article  CAS  PubMed  Google Scholar 

  • Gobbi M, De Vero L, Solieri L, Comitini F, Oro L, Giudici P, Ciani M (2014) Fermentative aptitude of non-Saccharomyces wine yeast for reduction in the ethanol content in wine. Eur Food Res Technol 239:41–48

    CAS  Google Scholar 

  • Gonzalez R, Quiros M, Morales P (2013) Yeast respiration of sugars by non-Saccharomyces yeast species: a promising and barely explored approach to lowering alcohol content of wines. Trends Food Sci Tech 29:55–61

    Article  CAS  Google Scholar 

  • Gonzalez SS, Barrio E, Querol A (2007) Molecular identification and characterization of wine yeasts isolated from Tenerife (Canary Island, Spain). J Appl Microbiol 102:1018–1025

    CAS  PubMed  Google Scholar 

  • Gonzalez-Royo E, Pascual O, Kontoudakis N, Esteruelas M, Esteve-Zarzoso B, Mas A, Miquel Canals J, 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

    Article  CAS  Google Scholar 

  • Greppi A, Rantsiou K, Padonou W, Hounhouigan J, Jespersen L, Jakobsen M, Cocolin L (2013) Determination of yeast diversity in ogi, mawe, gowe and tchoukoutou by using culture-dependent and -independent methods. Int J Food Microbiol 165:84–88

    Article  CAS  PubMed  Google Scholar 

  • Hu K, Qin Y, Tao Y-S, Zhu X-L, Peng C-T, Ullah N (2016a) Potential of glycosidase from non-Saccharomyces isolates for enhancement of wine aroma. J Food Sci 81:M935–M943

    Article  CAS  PubMed  Google Scholar 

  • Hu K, Zhu XL, Mu H, Ma Y, Ullah N, Tao YS (2016b) A novel extracellular glycosidase activity from Rhodotorula mucilaginosa: its application potential in wine aroma enhancement. Lett Appl Microbiol 62:169–176

    Article  CAS  PubMed  Google Scholar 

  • Izquierdo-Canas PM, Garcia-Romero E, Heras Manso JM, Fernandez-Gonzalez M (2014) Influence of sequential inoculation of Wickerhamomyces anomalus and Saccharomyces cerevisiae in the quality of red wines. Eur Food Res Technol 239:279–286

    Article  CAS  Google Scholar 

  • Jolly N, Augustyn O, Pretorius IS (2003) The occurrence of non-Saccharomyces cerevisiae yeast species over three vintages in four vineyards and grape musts from four production regions of the Western Cape, South Africa. S Afr J Enol Vitic 24:35–42

    Google Scholar 

  • Jolly NP, Varela C, Pretorius IS (2014) Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res 14:215–237

    Article  CAS  PubMed  Google Scholar 

  • Kemsawasd V, Viana T, Ardo Y, Arneborg N (2015) Influence of nitrogen sources on growth and fermentation performance of different wine yeast species during alcoholic fermentation. Appl Microbiol Biot 99:10191–10207

    Article  CAS  Google Scholar 

  • Kim HR, Kim J-H, Bai D-H, Ahn B (2012) Feasibility of brewing Makgeolli using Pichia anomala Y197-13, a non-Saccharomyces cerevisiae. J Microbiol Biotechn 22:1749–1757

    Article  CAS  Google Scholar 

  • Kutyna DR, Varela C, Henschke PA, Chambers PJ, Stanley GA (2010) Microbiological approaches to lowering ethanol concentration in wine. Trends Food Sci Tech 21:293–302

    Article  CAS  Google Scholar 

  • Lage P, Barbosa C, Mateus B, Vasconcelos I, Mendes-Faia A, Mendes-Ferreira A (2014) H. guilliermondii impacts growth kinetics and metabolic activity of S. cerevisiae: the role of initial nitrogen concentration. Int J Food Microbiol 172:62–69

    Article  CAS  PubMed  Google Scholar 

  • Lappe-Oliveras P, Moreno-Terrazas R, Arrizón-Gaviño J, Herrera-Suárez T, García-Mendoza A, Gschaedler-Mathis A (2008) Yeasts associated with the production of Mexican alcoholic nondistilled and distilled agave beverages. FEMS Yeast Res 8:1037–1052

    Article  CAS  PubMed  Google Scholar 

  • Lasekan O, Abbas KA (2012) Distinctive exotic flavor and aroma compounds of some exotic tropical fruits and berries: a review. Crit Rev Food Sci Nutr 52:726–735

    Article  CAS  PubMed  Google Scholar 

  • Lee PR, Ong YL, Yu B, Curran P, Liu SQ (2010) Evolution of volatile compounds in papaya wine fermented with three Williopsis saturnus yeasts. Int J Food Sci Tech 45:2032–2041

    Article  CAS  Google Scholar 

  • Lee P-R, Chong IS-M, Yu B, Curran P, Liu S-Q (2012) Effects of sequentially inoculated Williopsis saturnus and Saccharomyces cerevisiae on volatile profiles of papaya wine. Food Res Int 45:177–183

    Article  CAS  Google Scholar 

  • Legras JL, Merdinoglu D, Cornuet JM, Karst F (2007) Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history. Mol Ecol 16:2091–2102

    Article  CAS  PubMed  Google Scholar 

  • Lencioni L, Romani C, Gobbi M, Comitini F, Ciani M, Domizio P (2016) Controlled mixed fermentation at winery scale using Zygotorulaspora florentina and Saccharomyces cerevisiae. Int J Food Microbiol

  • Li X, Chan LJ, Yu B, Curran P, Liu SQ (2012a) Fermentation of three varieties of mango juices with a mixture of Saccharomyces cerevisiae and Williopsis saturnus var. mrakii. Int J Food Microbiol 158:28–35

    Article  CAS  PubMed  Google Scholar 

  • Li X, Yu B, Curran P, Liu SQ (2011) Chemical and volatile composition of mango wines fermented with different Saccharomyces cerevisiae yeast strains. S Afr J Enol Vitic 32:117–128

    Google Scholar 

  • Li X, Yu B, Curran P, Liu SQ (2012b) Impact of two Williopsis yeast strains on the volatile composition of mango wine. Int J Food Sci Tech 47:808–815

    Article  CAS  Google Scholar 

  • Liu SQ, Aung MT, Lee PR, Yu B (2016) Yeast and volatile evolution in cider co-fermentation with Saccharomyces cerevisiae and Williopsis saturnus. Ann Microbiol 66:307–315

    Article  CAS  Google Scholar 

  • Lleixa J, Martin V, Portillo MC, Carrau F, Beltran G, Mas A (2016) Comparison of fermentation and wines produced by inoculation of Hanseniaspora vineae and Saccharomyces cerevisiae. Front Microbiol 7

  • Loira I, Morata A, Comuzzo P, Jesus Callejo M, Gonzalez C, Calderon F, Antonio Suarez-Lepe J (2015) Use of Schizosaccharomyces pombe and Torulaspora delbrueckii strains in mixed and sequential fermentations to improve red wine sensory quality. Food Res Int 76:325–333

    Article  CAS  Google Scholar 

  • Lopandic K, Gangl H, Wallner E, Tscheik G, Leitner G, Querol A, Borth N, Breitenbach M, Prillenger H, Tiefenbrunner W (2007) Genetically different wine yeasts isolated from Austrian vine-growing regions influence wine aroma differently and contain putative hybrids between Saccharomyces cerevisiae and Saccharomyces kudriavzevii. FEMS Yeast Res 7:953–965

  • Lopez MC, Mateo JJ, Maicas S (2015) Screening of β-glucosidase and β-xylosidase activities in four non-Saccharomyces yeast isolates. J Food Sci 80:C1696–C1704

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Alvarez A, Laura Diaz-Perez A, Sosa-Aguirre C, Macias-Rodriguez L, Campos-Garcia J (2012) Ethanol yield and volatile compound content in fermentation of agave must by Kluyveromyces marxianus UMPe-1 comparing with Saccharomyces cerevisiae baker's yeast used in tequila production. J Biosci Bioeng 113:614–618

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Huang D, Lee P-R, Liu S-Q (2016) Assessment of volatile and non-volatile compounds in durian wines fermented with four commercial non-Saccharomyces yeasts. J Sci Food Agr 96:1511–1521

    Article  CAS  Google Scholar 

  • Masneuf-Pomarede I, Bely M, Marullo P, Albertin W (2016) The genetics of non-conventional wine yeasts: current knowledge and future challenges. Front Microbiol 6

  • Masneuf-Pomarede I, Juquin E, Miot-Sertier C, Renault P, Laizet Y, Salin F, Alexandre H, Capozzi V, Cocolin L, Colonna-Ceccaldi B, Englezos V, Girard P, Gonzalez B, Lucas P, Mas A, Nisiotou A, Sipiczki M, Spano G, Tassou C, Bely M, Albertin W (2015) The yeast Starmerella bacillaris (synonym Candida zemplinina) shows high genetic diversity in winemaking environments. FEMS Yeast Res 15:11

    Article  Google Scholar 

  • Maturano YP, Assof M, Fabani MP, Nally MC, Jofre V, Rodriguez Assaf LA, Toro ME, Castellanos de Figueroa LI, Vazquez F (2015) Enzymatic activities produced by mixed Saccharomyces and non-Saccharomyces cultures: relationship with wine volatile composition. Anton Leeuw Int J G 108:1239–1256

    Article  CAS  Google Scholar 

  • McGovern P, Hartung U, Badler V, Glusker D, Exner L (1997) The beginnings of winemaking and viniculture in the ancient Near East and Egypt. Expedition 39:3–21

    Google Scholar 

  • McGovern PE, Zhang JH, Tang JG, Zhang ZQ, Hall GR, Moreau RA, Nunez A, Butrym ED, Richards MP, Wang CS, Cheng GS, Zhao ZJ, Wang CS (2004) Fermented beverages of pre- and proto-historic China. P Natl Acad Sci USA 101:17593–17598

    Article  CAS  Google Scholar 

  • Medina K, Boido E, Dellacassa E, Carrau F (2012) Growth of non-Saccharomyces yeasts affects nutrient availability for Saccharomyces cerevisiae during wine fermentation. Int J Food Microbiol 157:245–250

    Article  CAS  PubMed  Google Scholar 

  • Medina K, Boido E, Farina L, Gioia O, Gomez ME, Barquet M, Gaggero C, Dellacassa E, Carrau F (2013) Increased flavour diversity of Chardonnay wines by spontaneous fermentation and co-fermentation with Hanseniaspora vineae. Food Chem 141:2513–2521

    Article  CAS  PubMed  Google Scholar 

  • Mehlomakulu NN, Setati ME, Divol B (2014) Characterization of novel killer toxins secreted by wine-related non-Saccharomyces yeasts and their action on Brettanomyces spp. Int J Food Microbiol 188:83–91

    Article  CAS  PubMed  Google Scholar 

  • Meinhardt F, Klassen R (2009) Yeast killer toxins: fundamentals and applications. In: Anke T, Weber D (eds) Physiology and genetics: selected basic and applied aspects. Springer, Berlin, Heidelberg, pp. 107–130

    Chapter  Google Scholar 

  • Merin MG, Morata de Ambrosini VI (2015) Highly cold-active pectinases under wine-like conditions from non-Saccharomyces yeasts for enzymatic production during winemaking. Lett Appl Microbiol 60:467–474

    Article  CAS  PubMed  Google Scholar 

  • Merin MG, Martin MC, Rantsiou K, Cocolin L, Morata de Ambrosini V (2015) Characterization of pectinase activity for enology from yeasts occurring in Argentine Bonarda grape. Braz J Microbiol 46:815–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Michel M, Kopecka J, Meier-Doernberg T, Zarnkow M, Jacob F, Hutzler M (2016) Screening for new brewing yeasts in the non-Saccharomyces sector with Torulaspora delbrueckii as model. Yeast 33:129–144

    Article  CAS  PubMed  Google Scholar 

  • Mingorance-Cazorla L, Clemente-Jimenez JM, Martinez-Rodriguez S, Las Heras-Vazquez FJ, Rodriguez-Vico F (2003) Contribution of different natural yeasts to the aroma of two alcoholic beverages. World J Microbiol Biotechnol 19:297–304

    Article  CAS  Google Scholar 

  • del Monaco SM, Barda NB, Rubio NC, Caballero AC (2014) Selection and characterization of a Patagonian Pichia kudriavzevii for wine deacidification. J Appl Microbiol 117:451–464

    Article  PubMed  CAS  Google Scholar 

  • Morales P, Rojas V, Quiros M, Gonzalez R (2015) The impact of oxygen on the final alcohol content of wine fermented by a mixed starter culture. Appl Microbiol Biot 99:3993–4003

    Article  CAS  Google Scholar 

  • Nunez-Guerrero ME, Paez-Lerma JB, Rutiaga-Quinones OM, Gonzalez-Herrera SM, Soto-Cruz NO (2016) Performance of mixtures of Saccharomyces and non-Saccharomyces native yeasts during alcoholic fermentation of Agave duranguensis juice. Food Microbiol 54:72–78

    Article  CAS  Google Scholar 

  • Oliveira ES, Cardello H, Jeronimo EM, Souza ELR, Serra GE (2005) The influence of different yeasts on the fermentation, composition and sensory quality of cachaca. World J Microbiol Biotechnol 21:707–715

    Article  CAS  Google Scholar 

  • Oro L, Ciani M, Comitini F (2014) Antimicrobial activity of Metschnikowia pulcherrima on wine yeasts. J Appl Microbiol 116:1209–1217

    Article  CAS  PubMed  Google Scholar 

  • Parapouli M, Hatziloukas E, Drainas C, Perisynakis A (2010) The effect of Debina grapevine indigenous yeast strains of Metschnikowia and Saccharomyces on wine flavour. J Ind Microbiol Biot 37:85–93

    Article  CAS  Google Scholar 

  • Parente DC, Vidal EE, Leite FCB, Pita WD, de Morais MA (2015) Production of sensory compounds by means of the yeast Dekkera bruxellensis in different nitrogen sources with the prospect of producing cachaca. Yeast 32:77–87

    Google Scholar 

  • Peng B, Yue T, Yuan Y (2008) A fuzzy comprehensive evaluation for selecting yeast for cider making. Int J Food Sci Tech 43:140–144

    Article  CAS  Google Scholar 

  • Petruzzi L, Rosaria Corbo M, Sinigaglia M, Bevilacqua A (2016) Brewer’s yeast in controlled and uncontrolled fermentations, with a focus on novel, nonconventional, and superior strains. Food Rev Int 32:341–363

    Article  CAS  Google Scholar 

  • Pinto C, Pinho D, Cardoso R, Custodio V, Fernandes J, Sousa S, Pinheiro M, Egas C, Gomes AC (2015) Wine fermentation microbiome: a landscape from different Portuguese wine appellations. Front Microbiol 6

  • Pires EJ, Teixeira JA, Branyik T, Brandao T, Vicente AA (2015) Continuous beer fermentation–diacetyl as a villain. J I Brewing 121:55–61

    Article  CAS  Google Scholar 

  • Pires EJ, Teixeira JA, Branyik T, Vicente AA (2014) Yeast: the soul of beer's aroma-a review of flavour-active esters and higher alcohols produced by the brewing yeast. Appl Microbiol Biot 98:1937–1949

    Article  CAS  Google Scholar 

  • Portugal CB, Alcarde A, Bortoletto A, de Silva A (2016) The role of spontaneous fermentation for the production of cachaça: a study of case. Eur Food Res Technol 242:1587–1597

    Article  CAS  Google Scholar 

  • Quiros M, Rojas V, Gonzalez R, Morales P (2014) Selection of non-Saccharomyces yeast strains for reducing alcohol levels in wine by sugar respiration. Int J Food Microbiol 181:85–91

    Article  CAS  PubMed  Google Scholar 

  • 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

  • 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

  • Ribeiro LS, Duarte WF, Dias DR, Schwan RF (2015) Fermented sugarcane and pineapple beverage produced using Saccharomyces cerevisiae and non-Saccharomyces yeast. J I Brewing 121:262–272

    Article  CAS  Google Scholar 

  • Rodriguez-Lerma GK, Gutierrez-Moreno K, Cardenas-Manriquez M, Botello-Alvarez E, Jimenez-Islas H, Rico-Martinez R, Navarrete-Bolanos JL (2011) Microbial ecology studies of spontaneous fermentation: starter culture selection for prickly pear wine production. J Food Sci 76:M346–M352

    Article  CAS  PubMed  Google Scholar 

  • Rossouw D, Bauer FF (2016) Exploring the phenotypic space of non-Saccharomyces wine yeast biodiversity. Food Microbiol 55:32–46

    Article  CAS  PubMed  Google Scholar 

  • Rossouw D, Bagheri B, Setati ME, Bauer FF (2015) Co-flocculation of yeast species, a new mechanism to govern population dynamics in microbial ecosystems. PLoS One 10

  • 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

    Article  CAS  Google Scholar 

  • Satora P, Tarko T, Sroka P, Blaszczyk U (2014) The influence of Wickerhamomyces anomalus killer yeast on the fermentation and chemical composition of apple wines. FEMS Yeast Res 14:729–740

    Article  CAS  PubMed  Google Scholar 

  • Segura-Garcia LE, Taillandier P, Brandam C, Gschaedler A (2015) Fermentative capacity of Saccharomyces and non-Saccharomyces in agave juice and semi-synthetic medium. LWT-Food Sci Technol 60:284–291

    Article  CAS  Google Scholar 

  • Sohrabvandi S, Razavi SH, Mousavi SM, Mortazavian A, Rezaei K (2009) Application of Saccharomyces rouxii for the production of non-alcoholic beer. Food Sci Biotechnol 18:1132–1137

    CAS  Google Scholar 

  • Spitaels F, Wieme AD, Janssens M, Aerts M, Daniel HM, Van Landschoot A, De Vuyst L, Vandamme P (2014) The microbial diversity of traditional spontaneously fermented lambic beer. PLoS One 9

  • Steensels J, Daenen L, Malcorps P, Derdelinckx G, Verachtert H, Verstrepen KJ (2015) Brettanomyces yeasts–from spoilage organisms to valuable contributors to industrial fermentations. Int J Food Microbiol 206:24–38

    Article  CAS  PubMed  Google Scholar 

  • Sun SY, Che CY, Sun TF, Lv ZZ, He SX, Gu HN, Shen WJ, Chi DC, Gao Y (2013) Evaluation of sequential inoculation of Saccharomyces cerevisiae and Oenococcus oeni strains on the chemical and aromatic profiles of cherry wines. Food Chem 138:2233–2241

    Article  CAS  PubMed  Google Scholar 

  • Sun SY, Gong HS, Jiang XM, Zhao YP (2014) Selected non-Saccharomyces wine yeasts in controlled multistarter fermentations with Saccharomyces cerevisiae on alcoholic fermentation behaviour and wine aroma of cherry wines. Food Microbiol 44:15–23

    Article  CAS  PubMed  Google Scholar 

  • Sun SY, Gong HS, Zhao YP, Liu WL, Jin C (2016) Sequential culture with Torulaspora delbrueckii and Saccharomyces cerevisiae and management of fermentation temperature to improve cherry wine quality. J Sci Food Agr 96:1880–1887

    Article  CAS  Google Scholar 

  • Tapsoba F, Legras JL, Savadogo A, Dequin S, Traore AS (2015) Diversity of Saccharomyces cerevisiae strains isolated from Borassus akeassii palm wines from Burkina Faso in comparison to other African beverages. Int J Food Microbiol 211:128–133

    Article  PubMed  Google Scholar 

  • Tofalo R, Patrignani F, Lanciotti R, Perpetuini G, Schirone M, Di Gianvito P, Pizzoni D, Arfelli G, Suzzi G (2016) Aroma profile of Montepulciano d'Abruzzo wine fermented by single and co-culture starters of autochthonous Saccharomyces and non-saccharomyces yeasts. Front Microbiol 7

  • Tristezza M, Tufariello M, Capozzi V, Spano G, Mita G, Grieco F (2016) The oenological potential of Hanseniaspora uvarum in simultaneous and sequential co-fermentation with Saccharomyces cerevisiae for industrial wine production. Front Microbiol 7

  • Ugliano M, Henschke PA (2009) Yeast and wine flavour. In: Moreno-Arribas MV, Polo C (eds) Wine chemistry and biochemistry. Springer, New York, pp. 313–392

    Chapter  Google Scholar 

  • Vanbeneden N, Gils F, Delvaux F, Delvaux FR (2008) Formation of 4-vinyl and 4-ethyl derivatives from hydroxycinnamic acids: occurrence of volatile phenolic flavour compounds in beer and distribution of Pad1-activity among brewing yeasts. Food Chem 107:221–230

    Article  CAS  Google Scholar 

  • Varela C, Borneman AR (2016) Yeasts of vineyards and wineries. Yeast.

  • Varela C, Dry PR, Kutyna DR, Francis IL, Henschke PA, Curtin CD, Chambers PJ (2015) Strategies for reducing alcohol concentration in wine. Aust J Grape Wine Res 21:670–679

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Varela C, Siebert T, Cozzolino D, Rose L, McLean H, Henschke PA (2009) Discovering a chemical basis for differentiating wines made by fermentation with 'wild' indigenous and inoculated yeasts: role of yeast volatile compounds. Aust J Grape Wine Res 15:238–248

    Article  CAS  Google Scholar 

  • Verdugo Valdez A, Segura Garcia L, Kirchmayr M, Ramírez Rodríguez P, González Esquinca A, Coria R, Gschaedler Mathis A (2011) Yeast communities associated with artisanal mezcal fermentations from Agave salmiana. Antonie Van Leeuwenhoek 100:497–506

    Article  CAS  PubMed  Google Scholar 

  • Vila Nova X, Pereira A, Ramos B, Morais M (2009) Yeast species involved in artisanal cachaça fermentation in three stills with different technological levels in Pernambuco, Brazil. Food Microbiol 26:460–466

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Walker G (1998) Yeast physiology and biotechnology. Wiley, Chichester

    Google Scholar 

  • 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

  • Wang C, Mos A, Esteve-Zarzoso B (2015) Interaction between Hanseniaspora uvarum and Saccharomyces cerevisiae during alcoholic fermentation. Int J Food Microbiol 206:67–74

    Article  CAS  PubMed  Google Scholar 

  • Ye MQ, Yue TL, Yuan YH (2014) Effects of sequential mixed cultures of Wickerhamomyces anomalus and Saccharomyces cerevisiae on apple cider fermentation. FEMS Yeast Res 14:873–882

    Article  CAS  PubMed  Google Scholar 

  • Zara G, Mannazzu I, Del Caro A, Budroni M, Pinna MB, Murru M, Farris GA, Zara S (2014) Wine quality improvement through the combined utilisation of yeast hulls and Candida zemplinina/Saccharomyces cerevisiae mixed starter cultures. Aust J Grape Wine Res 20:199–207

    Article  CAS  Google Scholar 

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Acknowledgments

The author would like to thank Dr. Paul Chambers for discussions on this topic and reviewing the manuscript. The AWRI, a member of the Wine Innovation Cluster in Adelaide, is supported by Australia’s grapegrowers and winemakers through their investment body Wine Australia with matching funds from the Australian Government.

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    Cristian Varela

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Varela, C. The impact of non-Saccharomyces yeasts in the production of alcoholic beverages. Appl Microbiol Biotechnol 100, 9861–9874 (2016). https://doi.org/10.1007/s00253-016-7941-6

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