Abstract
This review examines the different types of interactions between the microorganisms involved in the fermentation processes of alcoholic beverages produced all over the world from cereals or fruit juices. The alcoholic fermentation converting sugars into ethanol is usually carried out by yeasts, mainly Saccharomyces cerevisiae, which can grow directly using fruit sugars, such as those in grapes for wine or apples for cider, or on previously hydrolyzed starch of cereals, such as for beers. Some of these beverages, or the worts obtained from cereals, can be distilled to obtain spirits. Besides S. cerevisiae, all alcoholic beverages can contain other microorganisms and especially in spontaneous fermentation when starter cultures are not used. These other microbes are mostly lactic acid bacteria and other yeasts—the non-Saccharomyces yeasts. The interactions between all these microorganisms are very diverse and complex, as in any natural occurring ecosystem, including food fermentations. To describe them, we have followed a simplified ecological classification of the interactions. The negative ones are amensalism, by which a metabolic product of one species has a negative effect on others, and antagonism, by which one microbe competes directly with others. The positive interactions are commensalism, by which one species has benefits but no apparent effect on others, and synergism, by which there are benefits for all the microbes and also for the final product. The main interactions in alcoholic beverages are between S. cerevisiae and non-Saccharomyces and between yeasts and lactic acid bacteria. These interactions can be related to metabolites produced by fermentation such as ethanol, or to secondary metabolites such as proteinaceous toxins, or are feed-related, either by competition for nutrients or by benefit from released compounds during yeast autolysis. The positive or negative effects of these interactions on the organoleptic qualities of the final product are also revised. Focusing mainly on the alcoholic beverages produced by spontaneous fermentations, this paper reviews the interactions between the different yeasts and lactic acid bacteria in wine, cider, beer, and in spirits such as tequila, mezcal and cachaça.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data sharing not applicable to this article as no datasets were generated or analyzed during the current study.
References
Albergaria H, Francisco D, Gori K, Arneborg N, Gírio F (2010) Saccharomyces cerevisiae CCMI 885 secretes peptides that inhibit the growth of some non-Saccharomyces wine-related strains. Appl Microb Cell Physiol 86:965–972. https://doi.org/10.1007/s00253-009-2409-6
Alexandre H, Costello PJ, Remize F, Guzzo J, Guilloux-Benatier M (2004) Saccharomyces cerevisiae-Oenococcus oeni interactions in wine: current knowledge and perspectives. Int J Food Microbiol 93:141–154. https://doi.org/10.1016/j.ijfoodmicro.2003.10.013
Antón-Díaz MJ, Vallés BS, Mangas-Alonso JJ, Fernández-García O, Picinelli-Lobo A (2016) Impact of different techniques involving contact with lees on the volatile composition of cider. Food Chem 190:1116–1122. https://doi.org/10.1016/j.foodchem.2015.06.018
Arellano-Plaza M, Gschaedler-Mathis A, Noriega-Cisneros R, Clemente-Guerrero M, Manzo-Ávalos S, González-Hernández JC, Saavedra-Molina A (2013) Respiratory capacity of the Kluyveromyces marxianus yeast isolated from the mezcal process during oxidative stress. World J Microbiol Biotechnol 29:1279–1287. https://doi.org/10.1007/s11274-013-1291-7
Arnink K, Henick-Kling T (2005) Influence of Saccharomyces cerevisiae and Oenococcus oeni strains on successful malolactic conversion in wine. Am J Enol Vitic 56:228–237 (https://www.ajevonline.org/content/56/3/228.short)
Arrizon J, Fiore C, Acosta G, Romano P, Gschaedler A (2006) Fermentation behaviour and volatile compound production by agave and grape must yeasts in high sugar Agave tequilana and grape must fermentations. Antonie Van Leeuwenhoek 89:181–189. https://doi.org/10.1007/s10482-005-9022-1
Avbelj M, Zupan J, Raspor P (2016) Quorum-sensing in yeast and its potential in wine making. Appl Microbiol Biotechnol 100:7841–7852. https://doi.org/10.1007/s00253-016-7758-3
Azzolini M, Tosi E, Vagnoli P, Krieger S, Zapparoli G (2010) Evaluation of technological effects of yeast-bacterial co-inoculation in red table wine production. Ital J Food Sci 22:257–263 (https://www.researchgate.net/profile/Sibylle_Krieger-Weber/publication/264892324_Evaluation_of_technological_effects_of_yeast-bacterial_co-inoculation_in_red_table_wine/links/54ddc0f40cf25b09b914a7b1.pdf)
Badotti F, Moreira AP, Chimetto Tonon LA, Luckwu de Lucena BT, Gomes FCO, Kruger R, Thompson CC, de Morais MA, Rosa CA, Thompson FL (2014) Oenococcus alcoholitolerans sp. nov., a lactic acid bacteria isolated from cachaça and ethanol fermentation processes. Antonie Van Leeuwenhoek 106:1259–1267. https://doi.org/10.1007/s10482-014-0296-z
Balmaseda A, Bordons A, Reguant C, Bautista-Gallego J (2018) Non-Saccharomyces in wine: effect upon Oenococcus oeni and malolactic fermentation. Front Microbiol 9:1–8. https://doi.org/10.3389/fmicb.2018.00534
Balmaseda A, Rozès N, Leal MA, Bordons A, Reguant C (2021) Impact of changes in wine composition produced by non-Saccharomyces on malolactic fermentation. Int J Food Microbiol 337:108954. https://doi.org/10.1016/j.ijfoodmicro.2020.108954
Barbosa C, Mendes-Faia A, Lage P, Mira NP, Mendes-Ferreira, (2015) Genomic expression program of Saccharomyces cerevisiae along a mixed-culture wine fermentation with Hanseniaspora guilliermondii. Microb Cell Fact 14:124. https://doi.org/10.1186/s12934-015-0318-1
Barbosa C, Alcarde AR, Marques A, Paron A (2016) The role of spontaneous fermentation for the production of cachaça: a study of case. Eur Food Res Technol 242:1587–1597. https://doi.org/10.1007/s00217-016-2659-3
Beech FW (1972) Cider making and cider research: a review. J Inst Brewing 78:477–491. https://doi.org/10.1002/j.2050-0416.1972.tb03485.x
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
Beltran G, Torija MJ, Novo M, Ferrer N, Poblet M, Guillamón JM, Rozès N, Mas A (2002) Analysis of yeast populations during alcoholic fermentation: a six year follow-up study. Syst Appl Microbiol 25:287–293. https://doi.org/10.1078/0723-2020-00097
Benito S (2018) The impact of Torulaspora delbrueckii yeast in winemaking. Appl Microbiol Biotechnol 102:3081–3094. https://doi.org/10.1007/s00253-018-8849-0
Benito A, Calderón F, Benito S (2019) the influence of non-Saccharomyces species on wine fermentation quality parameters. Fermentation 5:54. https://doi.org/10.3390/fermentation5030054
Binati RL, Lemos WJF Jr, Luzzini G, Slaghenaufi D, Ugliano M, Torriani S (2020) Contribution of non-Saccharomyces yeasts to wine volatile and sensory diversity: a study on Lachancea thermotolerans, Metschnikowia spp. and Starmerella bacillaris strains isolated in Italy. Int J Food Microbiol 318:108470. https://doi.org/10.1016/j.ijfoodmicro.2019.108470
Boddy L, Wimpenny JWT (1992) Ecological concepts in food microbiology. J Appl Microbiol 73:S23-38. https://doi.org/10.1111/j.1365-2672.1992.tb03622.x
Bokulich NA, Bamforth CW (2013) The microbiology of malting and brewing. Microbiol Mol Biol Rev 77:157–172. https://doi.org/10.1128/MMBR.00060-12
Bovo B, Carlot M, Lombardi A, Lomolino G, Lante A, Giacomini A, Corich V (2014) Exploring the use of Saccharomyces cerevisiae commercial strain and Saccharomycodes ludwigii natural isolate for grape marc fermentation to improve sensory properties of spirits. Food Microbiol 41:33–41. https://doi.org/10.1016/j.fm.2014.01.006
Branco P, Francisco D, Chambon C, Hébraud M, Arneborg N, Almeida MG, Caldeira J, Albergaria H (2014) Identification of novel GAPDH-derived antimicrobial peptides secreted by Saccharomyces cerevisiae and involved in wine microbial interactions. Appl Microbiol Biotechnol 98:843–853. https://doi.org/10.1007/s00253-013-5411-y
Brizuela N, Tymczyszyn EE, Semorile LC, Valdes D, Valdes La Hens D, Delfederico L, Hollmann A, Bravo-Ferrada B (2019) Lactobacillus plantarum as a malolactic starter culture in winemaking: a new (old) player ? Electron J Biotechnol 38:10–18. https://doi.org/10.1016/j.ejbt.2018.12.002
Brizuela NS, Bravo-Ferrada BM, Curilén Y, Delfederico L, Caballero A, Semorile L, Pozo-Bayón MA, Tymczyszyn E (2018) Advantages of using blend cultures of native L. plantarum and O. oeni strains to induce malolactic fermentation of patagonian Malbec wine. Front Microbiol 9:1–9. https://doi.org/10.3389/fmicb.2018.02109
Capece A, Romaniello R, Pietrafesa A, Siesto G, Pietrafesa R, Zambuto M, Romano P (2018) Use of Saccharomyces cerevisiae var. boulardii in co-fermentations with S. cerevisiae for the production of craft beers with potential healthy value-added. Int J Food Microbiol 284:22–30. https://doi.org/10.1016/j.ijfoodmicro.2018.06.028
Caridi A, Corte V (1997) Inhibition of malolactic fermentation by cryotolerant yeasts. Biotechnol Lett 19:723–726. https://doi.org/10.1023/A:1018319705617
Carreté R, Vidal MT, Bordons A, Constantí M (2002) Inhibitory effect of sulfur dioxide and other stress compounds in wine on the ATPase activity of Oenococcus oeni. FEMS Microbiol Lett 211:155–159. https://doi.org/10.1016/S0378-1097(02)00687-0
Carvalho FP, Ferreira W, Ribeiro D, Hilsdorf R, Freitas R (2015) Interaction of Saccharomyces cerevisiae and Lactococcus lactis in the fermentation and quality of artisanal cachaça. Acta Sci Agron 37:51–60. https://doi.org/10.4025/actasciagron.v37i1.18397
Cheraiti N, Guezenec S, Salmon J (2005) Redox interactions between Saccharomyces cerevisiae and Saccharomyces uvarum in mixed culture under enological conditions. Appl Environ Microbiol 71:255–260. https://doi.org/10.1128/AEM.71.1.255
Clemente-Jiménez JM, Mingorance-Cazorla L, Martínez-Rodríguez S, Las Heras-Vázquez FJ, Rodríguez-Vico F (2005) Influence of sequential yeast mixtures on wine fermentation. Int J Food Microbiol 98:301–308. https://doi.org/10.1016/j.ijfoodmicro.2004.06.007
Comitini F, Ciani M (2007) The inhibitory activity of wine yeast starters on malolactic bacteria. Ann Microbiol 57:61–66. https://doi.org/10.1007/BF03175051
Comitini F, Ferretti R, Clementi F, Mannazzu I, Ciani M (2005) Interactions between Saccharomyces cerevisiae and malolactic bacteria: preliminary characterization of a yeast proteinaceous compound(s) active against Oenococcus oeni. J Appl Microbiol 99:105–111. https://doi.org/10.1111/j.1365-2672.2005.02579.x
Cordes A, Henriksen PS, Hald MM et al (2021) Identification of prehistoric malting and partial grain germination from starch granules in charred barley grains. J Archeol Sci 125:105297. https://doi.org/10.1016/j.jas.2020.105297
Costello PJ, Henschke P, Markides J (2003) Standardised methodology for testing malolactic bacteria and wine yeast compatibility. Aust J Grape Wine Res 9:127–137. https://doi.org/10.1111/j.1755-0238.2003.tb00263.x
Cousin FJ, Le Gellec R, Schlusselhuber M, Dalmasso M, Laplace JM, Cretenet M (2017) Microorganisms in fermented apple beverages: current knowledge and future directions. Microorganisms 5(3):39. https://doi.org/10.3390/microorganisms5030039
Curiel JA, Morales P, González R, Tronchoni J (2017) Different non-Saccharomyces yeast species stimulate nutrient consumption in S. cerevisiae mixed cultures. Front Microbiol 8:2121. https://doi.org/10.3389/fmicb.2017.02121
Dharmadhikari M 1996 Wines from cherries and soft fruits. Newsletter Vineyard Vintage View 11(2): 1–9. Missouri State Fruit Experiment Station. https://www.extension.iastate.edu/wine/files/page/files/winesfromcherriesandsoftfruits.pdf
De Roos J, De Vuyst L (2019) Microbial acidification, alcoholization, and aroma production during spontaneous lambic beer production. J Sci Food Agric 99:25–38. https://doi.org/10.1002/jsfa.9291
Del Campo G, Berregi I, Santos JI, Dueñas IA (2008) Development of alcoholic and malolactic fermentations in highly acidic and phenolic apple musts. Biores Technol 99:2857–2863. https://doi.org/10.1016/j.biortech.2007.06.007
Dick KJ, Molan PC, Eschembruch R (1992) The isolation from Saccharomyces cerevisiae of two antibacterial cationic proteins that inhibit malolactic bacteria. Vitis 31:105–116 (https://ojs.openagrar.de/index.php/VITIS/article/view/5273/5018)
Dierings LR, Braga CM, Marques K, Wosiacki G, Nogueira A (2013) Population dynamics of mixed cultures of yeast and lactic acid bacteria in cider conditions. Brazilian Arch Biol Technol 56:837–847. https://doi.org/10.1590/S1516-89132013000500016
Díez L, Guadalupe Z, Belen A, Ruiz-Larrea F (2010) Effect of yeast mannoproteins and grape polysaccharides on the growth of wine lactic acid and acetic acid bacteria. J Agric Food Chem 58:7731–7739. https://doi.org/10.1021/jf100199n
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
Du Plessis HW, Steger CLC, Du Toit M, Lambrechts MG (2002) The occurrence of malolactic fermentation in brandy base wine and its influence on brandy quality. J ApplMicrobiol 92:1005–1013. https://doi.org/10.1046/j.1365-2672.2002.01616.x
Du Plessis HW, Du Toit M, Nieuwoudt H, Van M, Hoff J, Jolly N (2019) Modulation of wine flavor using Hanseniaspora uvarum in combination with different Saccharomyces cerevisiae, lactic acid bacteria strains and malolactic fermentation strategies. Fermentation 5:1–17. https://doi.org/10.3390/fermentation5030064
Dysvik A, Hovde K, Myhrer K, Westereng B, Rukke EO, de Rouck G, Wicklund T (2019) Pre-fermentation with lactic acid bacteria in sour beer production. Inst Brew Distill 125:342–356. https://doi.org/10.1002/jib.569
Dysvik A, La Rosa SL, De Rouck G, Rukke EO, Westereng B, Wicklund T (2020) Microbial dynamics in traditional and modern sour beer production. Appl Environ Microbiol 86:e00566-e620. https://doi.org/10.1128/AEM.00566-20
Escalante A, López Soto DR, Velázquez Gutiérrez JE, Giles-Gómez M, Bolívar F, López-Munguía A (2016) Pulque, a traditional Mexican alcoholic fermented beverage: historical, microbiological, and technical aspects. Front Microbiol 7:1–18. https://doi.org/10.3389/fmicb.2016.01026
Fernández CL, Beaufort S, Brandam C, Taillandier P (2014) Interactions between Kluyveromyces marxianus and Saccharomyces cerevisiae in tequila must type medium fermentation. World J Microbiol Biotechnol 30:2223–2229. https://doi.org/10.1007/s11274-014-1643-y
Ferrando N, Araque I, Ortís A, Thornes G, Bautista-Gallego J, Bordons A, Reguant C (2020) Evaluating the effect of using non-Saccharomyces on Oenococcus oeni and wine malolactic fermentation. Food Res Internat 138:109779. https://doi.org/10.1016/j.foodres.2020.109779
Ferreira W, Cunha J, Freitas R (2013) The effects of co-culturing non-Saccharomyces yeasts with S. cerevisiae on the sugar cane spirit (cachaça) fermentation process. Antonie Van Leeuwenhoek 103:175–194. https://doi.org/10.1007/s10482-012-9798-8
Ferreira W, Ferreira MV, Ribeiro D, Freitas R (2011) Effect of co-inoculation of Saccharomyces cerevisiae and Lactobacillus fermentum on the quality of the distilled sugar cane beverage cachaça. J Food Sci 76:1307–1318. https://doi.org/10.1111/j.1750-3841.2011.02412.x
Fleet GH, Lafon-Lafourcade S, Ribéreau-Gayon P (1984) Evolution of yeasts and lactic acid bacteria during fermentation and storage of Bordeaux wines. Appl Environ Microbiol 48:1034–1038. https://doi.org/10.1128/aem.48.5.1034-1038.1984
Fleet GH (2003) Yeast interactions and wine flavour. Int J Food Microbiol 86:11–22. https://doi.org/10.1016/S0168-1605(03)00245-9
Freitas R, Mendonça A, Da Silva JJ, Rodrigues V, Wheals A (2001) Microbiology and physiology of cachaça (Aguardente) fermentations. Antonie Van Leeuwenhoek 79:89–96. https://doi.org/10.1023/A:1010225117654
Geddes PA, Riffkin HL (1989) Influence of lactic acid bacteria on aldehyde, ester and higher alcohol formation during Scotch whisky fermentations. In Piggot JR, Paterson A (eds) Distilled beverage flavour. Ellis Horwood, Chichester, United Kingdom, pp 193–199
Geissler A, Behr J, von Kamp K, Vogel R (2016) Metabolic strategies of beer spoilage lactic acid bacteria in beer. Int J Food Microbiol 216:60–68. https://doi.org/10.1016/j.ijfoodmicro.2015.08.016
Gomes FCO, Silva CLC, Vianna CR, Lacerda ICA, Borelli BM, Nunes CÁ, Franco GR, Mourap MM, Rosa CA (2010) Identification of lactic acid bacteria associated with traditional cachaça fermentations. Braz J Microbiol 41:486–492. https://doi.org/10.1590/S1517-83822010000200031
González-Robles IW, Estarrón-Espinoza M, Díaz-Montaño DM (2015) Fermentative capabilities and volatile compounds produced by Kloeckera/Hanseniaspora and Saccharomyces yeast strains in pure and mixed cultures during Agave tequilana juice fermentation. Antonie Van Leeuwenhoek 108:525–536. https://doi.org/10.1007/s10482-015-0506-3
González B, Vázquez J, Cullen PJ, Mas A, Beltran G, Torija M-J (2018) Aromatic amino acid-derived compounds induce morphological changes and modulate the cell growth of wine yeast species. Front Microbiol 9:1–16. https://doi.org/10.3389/fmicb.2018.00670
Grauso L, Emrick S, de Falco B, Lanzotti V, Bonanomi G (2019) Common dandelion: a review of its botanical, phytochemical and pharmacological profiles. Phytochem Rev 18:1115–1132. https://doi.org/10.1007/s11101-019-09622-2
Harding G (2005) A wine miscellany. Carkson Potter Publ, New York
Hickey CD, Sheehan JJ, Wilkinson MG, Auty MAE (2015) Growth and location of bacterial colonies within dairy foods using microscopy techniques: a review. Front Microbiol 6:1–8. https://doi.org/10.3389/fmicb.2015.00099
Hu K, Jin GJ, Mei WC, Li T, Tao YS (2018) Increase of medium-chain fatty acid ethyl ester content in mixed H. uvarum/S. cerevisiae fermentation leads to wine fruity aroma enhancement. Food Chem 239:495–501. https://doi.org/10.1016/j.foodchem.2017.06.151
Ivey M, Massel M, Phister TG (2013) Microbial interactions in food fermentations. Ann Rev Food Sci Technol 4:141–162. https://doi.org/10.1146/annurev-food-022811-101219
Izquierdo PM, Romero EG, Pérez-Martín F, Seseña S, Palop ML (2014) Sequential inoculation versus co-inoculation in Cabernet Franc wine fermentation. Food Sci Technol Int 21:203–212. https://doi.org/10.1177/1082013214524585
Jolly NP, Varela C, Pretorius IS (2014) Not your ordinary yeast: non-Saccharomyces yeasts in wine production uncovered. FEMS Yeast Res 14:215–237. https://doi.org/10.1111/1567-1364.12111
Lachance M-A (1995) Yeast communities in a natural tequila fermentation. Antonie Van Leeuwenhoek 68:151–160. https://doi.org/10.1007/BF00873100
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. https://doi.org/10.1016/j.ijfoodmicro.2013.11.031
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. https://doi.org/10.1111/j.1567-1364.2008.00430.x
Lemaresquier H (1987) Inter-relationships between strains of Saccharomyces cerevisiae from the Champagne area and lactic acid bacteria. Lett Appl Microbiol 4:91–94. https://doi.org/10.1111/j.1472-765X.1987.tb01590.x
Lerm E, Engelbrecht L, Du Toit M (2010) Malolactic fermentation: the ABC’s of MLF. S Afr J Enol Vitic 31:186–212 (http://hdl.handle.net/10019.1/8419)
Li Y-Q, Hu K, Xu YH, Mei WC, Tao YS (2020) Biomass suppression of Hanseniaspora uvarum by killer Saccharomyces cerevisiae highly increased fruity esters in mixed culture fermentation. LWT - Food Sci Technol 132:1–8. https://doi.org/10.1016/j.lwt.2020.109839
Little AEF, Robinson CJ, Peterson SB, Raffa KF, Handelsman J (2008) Rules of engagement: interspecies interactions that regulate microbial communities. Ann Rev Microbiol 62:375–401. https://doi.org/10.1146/annurev.micro.030608.101423
Liu SQ (2002) Malolactic fermentation in wine - Beyond deacidification. J Appl Microbiol 92:589–601. https://doi.org/10.1046/j.1365-2672.2002.01589.x
Liu Y, Forcisi S, Harir M, Deleris-Bou M, Krieger-Weber S, Lucio M, Longin C, Gougeon RD, Schmitt-Kopplin P, Alexandre H (2016) New molecular evidence of wine yeast-bacteria interaction unraveled by non-targeted exometabolomic profiling. Metabolomics 12:12–69. https://doi.org/10.1007/s11306-016-1001-1
Lonvaud-Funel A, Joyeux A, Desens C (1988) Inhibition of malolactic fermentation of wines by products of yeast metabolism. J Sci Food Agric 44:183–191. https://doi.org/10.1002/jsfa.2740440209
Lonvaud-Funel A (1999) Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie Van Leeuwenhoek 76:317–331. https://doi.org/10.1023/A:1002088931106
Maicas S, Ferrer S, Pardo I (2002) NAD(P)H regeneration is the key for heterolactic fermentation of hexoses in Oenococcus oeni. Microbiology 148:325–332. https://doi.org/10.1099/00221287-148-1-325
Mannazzu I, Domizio P, Carboni G, Zara S, Comitini F, Budroni M, Ciani M (2019) Yeast killer toxins: from ecological significance to application. Crit Rev Biotechnol 39:603–617. https://doi.org/10.1080/07388551.2019.1601679
Martínez-Rodriguez AJ, Carrascosa AV, Polo MC (2001) Release of nitrogen compounds to the extracellular medium by three strains of Saccharomyces cerevisiae during induced autolysis in a model wine system. Int J Food Microbiol 68:155–160. https://doi.org/10.1016/S0168-1605(01)00486-X
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. https://doi.org/10.1016/j.ijfoodmicro.2012.05.012
Mendoza LM, Manca MC, Farías ME (2010) Antagonistic interaction between yeasts and lactic acid bacteria of oenological relevance partial characterization of inhibitory compounds produced by yeasts. Food Res Int 43:1990–1998. https://doi.org/10.1016/j.foodres.2010.05.017
Mendoza LM, Neef A, Vignolo G, Belloch C (2017) Yeast diversity during the fermentation of Andean chicha: a comparison of high-throughput sequencing and culture-dependent approaches. Food Microbiol 67:1–10. https://doi.org/10.1016/j.fm.2017.05.007
Muñoz V, Beccaria B, Abreo E (2014) Simultaneous and successive inoculations of yeasts and lactic acid bacteria on the fermentation of an unsulfited Tannat grape must. Braz J Microbiol 45:59–66. https://doi.org/10.1590/S1517-83822014000100009
Narváez-Zapata JA, Rojas-Herrera RA, Rodríguez-Luna IC, Larralde-Corona CP (2010) Culture-independent analysis of lactic acid bacteria diversity associated with mezcal fermentation. Curr Microbiol 61:444–450. https://doi.org/10.1007/s00284-010-9636-z
Nehme N, Mathieu F, Taillandier P (2008) Quantitative study of interactions between Saccharomyces cerevisiae and Oenococcus oeni strains. J Ind Microbiol Biotechnol 35:685–693. https://doi.org/10.1007/s10295-008-0328-7
Nissen P, Nielsen D, Arneborg N (2003) Viable Saccharomyces cerevisiae cells at high concentrations cause early growth arrest of non-Saccharomyces yeasts in mixed cultures by a cell–cell contact-mediated mechanism. Yeast 20:331–341. https://doi.org/10.1002/yea.965
Nissen P, Arneborg N (2003) Characterization of early deaths of non-Saccharomyces yeasts in mixed cultures with Saccharomyces cerevisiae. Arch Microbiol 180:257–263. https://doi.org/10.1007/s00203-003-0585-9
Núñez-Guerrero ME, Páez-Lerma JB, Rutiaga-Quiñones OM, González-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 54:91–97. https://doi.org/10.1016/j.fm.2015.10.011
Olguín N, Champomier-Vergès M, Anglade P, Baraige F, Cordero-Otero R, Bordons A, Zagorec M, Reguant C (2015) Transcriptomic and proteomic analysis of Oenococcus oeni PSU-1 response to ethanol shock. Food Microbiol 51:87–95. https://doi.org/10.1016/j.fm.2015.05.005
Oro L, Ciani M, Comitini F (2014) Antimicrobial activity of Metschnikowia pulcherrima on wine yeasts. J Appl Microbiol 116:1209–1217. https://doi.org/10.1111/jam.12446
Osborne JP, Edwards CG (2007) Inhibition of malolactic fermentation by a peptide produced by Saccharomyces cerevisiae during alcoholic fermentation. Int J Food Microbiol 118:27–34. https://doi.org/10.1016/j.ijfoodmicro.2007.05.007
Othman N, Hamid HA, Suleiman N (2019) Physicochemical properties and sensory evaluation of yogurt nutritionally. Food Res 3:791–797. https://doi.org/10.26656/fr201736199
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
Pauley M, Maskell D (2017) Mini-review: the role of Saccharomyces cerevisiae in the production of gin and vodka. Beverages 3(13):1–11. https://doi.org/10.3390/beverages3010013
Pereira AP, Dias T, Andrade J, Ramalhosa E, Estevinho LM (2009) Mead production: selection and characterization assays of Saccharomyces cerevisiae strains. Food Chem Toxicol 47:2057–2063. https://doi.org/10.1016/j.fct.2009.05.028
Puertas AI, Arahal DR, Ibarburu I, Aznar R, Dueñas MT (2014) Lactobacillus sicerae sp. nov., a lactic acid bacterium isolated from Spanish natural cider. Int J Syst Evol Microbio 64:2949–2955. https://doi.org/10.1099/ijs.0.059980-0
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 7:1–10. https://doi.org/10.3389/fmicb.2016.00293
Rizk Z, El Y, Ghanem C, Mathieu F, Taillandier P, Nehme N (2016) Impact of inhibitory peptides released by Saccharomyces cerevisiae BDX on the malolactic fermentation performed by Oenococcus oeni Vitilactic F. Int J Food Microbiol 233:90–96. https://doi.org/10.1016/j.ijfoodmicro.2016.06.018
Rodrigo-Torres L, Yépez A, Aznar R, Arahal DR (2019) Genomic insights into five strains of Lactobacillus plantarum with biotechnological potential isolated from chicha, a traditional maize-based fermented beverage from Northwestern Argentina. Front Microbiol 10:2232. https://doi.org/10.3389/fmicb.2019.02232
Rossouw D, Du Toit M, Bauer FF (2012) The impact of co-inoculation with Oenococcus oeni on the trancriptome of Saccharomyces cerevisiae and on the flavour-active metabolite profiles during fermentation in synthetic must. Food Microbiol 29:121–131. https://doi.org/10.1016/j.fm.2011.09.006
Ruiz J, de Celis M, de Toro M, Mendes-Ferreira A, Rauhut D, Santos A, Belda I (2020) Phenotypic and transcriptional analysis of Saccharomyces cerevisiae during wine fermentation in response to nitrogen nutrition and co-inoculation with Torulaspora delbrueckii. Food Res Int 127:109663. https://doi.org/10.1016/j.foodres.2020.109663
Sadoudi M, Tourdot-Maréchal R, Rousseaux S, Steyer D, Gallardo-Chacón JJ, Ballester J, Vichi S, Guérin-Schneider R, Caixach AH (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
Sánchez A, Coton M, Coton E, Herrero M, García LA, Díaz M (2012) Prevalent lactic acid bacteria in cider cellars and efficiency of Oenococcus oeni strains. Food Microbiol 32:32–37. https://doi.org/10.1016/j.fm.2012.02.008
Silva ML, Macedo AC, Malcata FX (2000) Review: steam distilled spirits from fermented grape pomace. Food Sci Technol Int 6:285–300. https://doi.org/10.1177/108201320000600403
Son HS, Hwang GS, Park WM, Hong YS, Lee CH (2009) Metabolomic characterization of malolactic fermentation and fermentative behaviors of wine yeasts in grape wine. J Agric Food Chem 57:4801–4809. https://doi.org/10.1021/jf9005017
Spitaels F, Wieme AD, Janssens M, Aerts M, Van Landschoot A, De Vuyst L, Vandamme P (2015) The microbial diversity of an industrially produced lambic beer shares members of a traditionally produced one and reveals a core microbiota for lambic beer fermentation. Food Microbiol 49:23–32. https://doi.org/10.1016/j.fm.2015.01.008
Stanley GA, Hobley TJ, Pamment.NB, (1997) Effect of acetaldehyde on Saccharomyces cerevisiae and Zymomonas mobilis subjected to environmental shocks. Biotechnol Bioen 53:71–78. https://doi.org/10.1002/(SICI)1097-0290(19970105)53:1%3c71::AID-BIT10%3e3.0.CO;2-C
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. https://doi.org/10.1016/j.ijfoodmicro.2015.04.005
Steinkraus KH (1997) Classification of fermented foods: Worldwide review of household fermentation techniques. Food Control 8:311–317. https://doi.org/10.1016/s0956-7135(97)00050-9
Suárez-Vallés B, Pando R, Fernández N, Querol A, Rodríguez R (2007) Yeast species associated with the spontaneous fermentation of cider. Food Microbiol 24:25–31. https://doi.org/10.1016/j.fm.2006.04.001
Tamang JP, Watanabe K, Holzapfel WH (2016) Review: diversity of microorganisms in global fermented foods and beverages. Front Microbiol 7:1–28. https://doi.org/10.3389/fmicb.2016.00377
Terrade N, Mira de Orduña R (2009) Determination of the essential nutrient requirements of wine-related bacteria from the genera Oenococcus and Lactobacillus. Int J Food Microbiol 133:8–13. https://doi.org/10.1016/j.ijfoodmicro.2009.03.020
Tronchoni J, Curiel JA, Morales P, Torres-Pérez R, González R (2017) Early transcriptional response to biotic stress in mixed starter fermentations involving Saccharmoyces cerevisiae and Torulaspora delbrueckii. Int J Food Microbiol 241:60–68. https://doi.org/10.1016/j.ijfoodmicro.2016.10.017
Tufariello M, Fragasso M, Pico J, Panighel A, Castellarin SD, Flamini R, Grieco F (2021) Influence of non-Saccharomyces on wine chemistry: a focus on aroma-related compounds. Molecules 26:644. https://doi.org/10.3390/molecules26030644
Van Beek S, Priest FG (2000) Decarboxylation of substituted cinnamic acids by lactic acid bacteria isolated during malt whisky fermentation. Appl Environ Microbiol 66:5322–5328. https://doi.org/10.1128/AEM.66.12.5322-5328.2000
Van Vuuren HJJ, Jacobs CJ (1992) Killer yeasts in the wine industry a review. Am J Enol Vitic 43:119–128 (https://www.ajevonline.org/content/43/2/119)
Verdugo Valdez A, Segura García L, Kirchmayr M, Ramírez Rodríguez P, González Esquinca A, Coria R, Gschaedler M (2011) Yeast communities associated with artisanal mezcal fermentations from Agave salmiana. Antonie Van Leeuwenhoek 100:497–506. https://doi.org/10.1007/s10482-011-9605-y
Vriesekoop F, Krahl M, Hucker B, Menz G (2012) 125th Anniversary review: bacteria in brewing: the good, the bad and the ugly. J Inst Brew 118:335–345. https://doi.org/10.1002/jib.49
Wang C, Mas A, Esteve-Zarzoso B (2015) Interaction between Hanseniaspora uvarum and Saccharomyces cerevisiae during alcoholic fermentation. Int J Food Microbiol 206:67–74. https://doi.org/10.1016/j.ijfoodmicro.2015.04.022
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 7:1–11. https://doi.org/10.3389/fmicb.2016.00502
Wells A, Osborne JP (2011) Production of SO2 and SO2 binding compounds by Saccharomyces cerevisiae during the alcoholic fermentation and the impact on wine lactic acid bacteria. S Afr J Enol Vitic 32:267–279 (http://www.journals.ac.za/index.php/sajev/article/viewFile/1387/601)
Wibowo D, Eschenbruch R, Davis C, Fleet G, Lee T (1985) Occurrence and growth of lactic acid bacteria in wine a review. Am J Enol Vitic 36:302–313 (https://www.ajevonline.org/content/36/4/302.short)
Wiśniewska P, Śliwińska M, Dymerski T, Wardencki W, Namieśnik J (2016) Differentiation between spirits according to their botanical origin. Food Anal Methods 9:1029–1035. https://doi.org/10.1007/s12161-015-0280-x
Zhang B, Xu D, Duan C, Yan G (2020) Synergistic effect enhances 2-phenylethyl acetate production in the mixed fermentation of Hanseniaspora vineae and Saccharomyces cerevisiae. Process Biochem 90:44–49. https://doi.org/10.1016/j.procbio.2019.11.007
Zheng J, Wittouck S, Salvetti E et al (2020) A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae. Int J Syst Evol Microbiol 70:2782–2858. https://doi.org/10.1099/ijsem.0.004107
Zupan J, Avbelj M, Butinar B, Kosel J, Šergan M, Raspor P (2013) Monitoring of quorum-sensing molecules during minifermentation studies in wine yeast. J Agric Food Chem 61:2496–2505. https://doi.org/10.1021/jf3051363
Acknowledgements
Rafael Torres-Guardado is grateful to the predoctoral fellowship from Fundación Carolina, which includes partial stipend from Mexican Government and from University Rovira i Virgili (URV). We are grateful to the Language Service of URV for English correction of the manuscript.
Funding
This work was supported by grant PGC2018-101852-B-I00 awarded by the Spanish Research Agency.
Author information
Authors and Affiliations
Contributions
All the authors contributed equally and substantially to the work.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Torres-Guardado, R., Esteve-Zarzoso, B., Reguant, C. et al. Microbial interactions in alcoholic beverages. Int Microbiol 25, 1–15 (2022). https://doi.org/10.1007/s10123-021-00200-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10123-021-00200-1