Applied Microbiology and Biotechnology

, Volume 102, Issue 9, pp 3995–4007 | Cite as

The complexity of wine: clarifying the role of microorganisms

  • Sophie Tempère
  • Axel Marchal
  • Jean-Christophe Barbe
  • Marina Bely
  • Isabelle Masneuf-Pomarede
  • Philippe Marullo
  • Warren AlbertinEmail author


The concept of wine complexity has gained considerable interest in recent years, both for wine consumers and wine scientists. As a consequence, some research programs concentrate on the factors that could improve the perceived complexity of a wine. Notably, the possible influence of microbiological factors is particularly investigated. However, wine complexity is a multicomponent concept not easily defined. In this review, we first describe the actual knowledge regarding wine complexity, its perception, and wine chemical composition. In particular, we emphasize that, contrary to expectations, the perception of wine complexity is not related to wine chemical complexity. Then, we review the impact of wine microorganisms on wine complexity, with a specific focus on publications including sensory analyses. While microorganisms definitively can impact wine complexity, the underlying mechanisms and molecules are far from being deciphered. Finally, we discuss some prospective research fields that will help improving our understanding of wine complexity, including perceptive interactions, microbial interactions, and other challenging phenomena.


Wine complexity perception Sensorial analysis Yeast Bacteria 


Author contributions statement

All authors wrote the paper.

Compliance with ethical standards

Conflict of interest

Sophie Tempère, Axel Marchal, Jean-Chistophe Barbe, Marina Bely, Isabelle Masneuf-Pomarede, and Warren Albertin declare that they have no conflict of interest. Philippe Marullo is affiliated with Biolaffort Company.

Informed consent

This article does not contain any studies with human participants or animals performed by any of the authors.


  1. Albertin W, Zimmer A, Miot-Sertier C, Bernard M, Coulon J, Moine V, Colonna-Ceccaldi B, Bely M, Marullo P, Masneuf-Pomarede I (2017) Combined effect of the Saccharomyces cerevisiae lag phase and the non-Saccharomyces consortium to enhance wine fruitiness and complexity. Appl Microbiol Biotechnol 101:7603–7620. PubMedCrossRefGoogle Scholar
  2. 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. PubMedCrossRefGoogle Scholar
  3. Antalick G, Perello M-C, de Revel G (2012) Characterization of fruity aroma modifications in red wines during malolactic fermentation. J Agric Food Chem 60:12371–12383. PubMedCrossRefGoogle Scholar
  4. Atanasova B, Thomas-Danguin T, Langlois D, Nicklaus S, Etievant P (2004) Perceptual interactions between fruity and woody notes of wine. Flavour and Fragrance J 19:476–482. CrossRefGoogle Scholar
  5. 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. PubMedCrossRefGoogle Scholar
  6. Balint G, Reynolds AG (2017) Irrigation level and time of imposition impact vine physiology, yield components, fruit composition and wine quality of Ontario chardonnay. Sci Hortic 214:252–272. CrossRefGoogle Scholar
  7. Beckner Whitener ME, Carlin S, Jacobson D, Weighill D, Divol B, Conterno L, Du Toit M, Vrhovsek U (2015) Early fermentation volatile metabolite profile of non-Saccharomyces yeasts in red and white grape must: a targeted approach. Food Sci Technol 64:412–422. Google Scholar
  8. Beckner Whitener ME, Stanstrup J, Panzeri V, Carlin S, Divol B, Du Toit M, Vrhovsek U (2016) Untangling the wine metabolome by combining untargeted SPME–GCxGC-TOF-MS and sensory analysis to profile Sauvignon Blanc co-fermented with seven different yeasts. Metabolomics 12:53. CrossRefGoogle Scholar
  9. 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. PubMedCrossRefGoogle Scholar
  10. Belda I, Ruiz J, Esteban-Fernández A, Navascués E, Marquina D, Santos A, Moreno-Arribas M (2017) Microbial contribution to wine aroma and its intended use for wine quality improvement. Molecules 22:189. CrossRefGoogle Scholar
  11. Benito S, Hofmann T, Laier M, Lochbühler B, Schüttler A, Ebert K, Fritsch S, Röcker J, Rauhut D (2015) 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. CrossRefGoogle Scholar
  12. Blanco P, Mirás-Avalos JM, Pereira E, Fornos D, Orriols I (2014) Modulation of chemical and sensory characteristics of red wine from Mencía by using indigenous Saccharomyces cerevisiae yeast strains. OENO One 48:63–74. CrossRefGoogle Scholar
  13. Blanco P, Miras-Avalos JM, Suarez V, Orriols I (2013a) Inoculation of Treixadura musts with autochthonous Saccharomyces cerevisiae strains: fermentative performance and influence on the wine characteristics. Food Sci Technol Int 19:177–186. PubMedCrossRefGoogle Scholar
  14. Blanco P, Mirás-Avalos JM, Pereira E, Orriols I (2013b) Fermentative aroma compounds and sensory profiles of Godello and Albariño wines as influenced by Saccharomyces cerevisiae yeast strains. J Sci Food Agric 93:2849–2857. PubMedCrossRefGoogle Scholar
  15. Blein-Nicolas M, Albertin W, da Silva T, Valot B, Balliau T, Masneuf-Pomarede I, Bely M, Marullo P, Sicard D, Dillmann C, de Vienne D, Zivy M (2015) A systems approach to elucidate Heterosis of protein abundances in yeast. Mol Cell Proteomics 14:2056–2071. PubMedPubMedCentralCrossRefGoogle Scholar
  16. Budić-Leto I, Zdunić G, Banović M, Tomić-Potrebuješ I, Lovrić T (2010) Fermentative aroma compounds and sensory descriptors of traditional Croatian dessert wine Prošek from Plavac mali cv. Food Technol Biotechnol 48:530–537Google Scholar
  17. Callejon R, Clavijo A, Ortigueira P, Troncoso A, Paneque P, Morales M (2010) Volatile and sensory profile of organic red wines produced by different selected autochthonous and commercial Saccharomyces cerevisiae strains. Anal Chim Acta 660:68–75. PubMedCrossRefGoogle Scholar
  18. Cameleyre M, Lytra G, Tempere S, Barbe JC (2015) Olfactory impact of higher alcohols on red wine fruity Ester aroma expression in model solution. J Agric Food Chem 63:9777–9788. PubMedCrossRefGoogle Scholar
  19. Cañas PMI, Pérez-Martín F, Romero EG, Prieto SS, Herreros MLP (2012) Influence of inoculation time of an autochthonous selected malolactic bacterium on volatile and sensory profile of Tempranillo and Merlot wines. Int J Food Microbiol 156:245–254. CrossRefGoogle Scholar
  20. Carvalho E, Mateus N, Plet B, Pianet I, Dufourc E, De Freitas V (2006) Influence of wine pectic polysaccharides on the interactions between condensed tannins and salivary proteins. J Agric Food Chem 54:8936–8944. PubMedCrossRefGoogle Scholar
  21. Charters S, Pettigrew S (2007) The dimensions of wine quality. Food Qual Prefer 18:997–1007. CrossRefGoogle Scholar
  22. Chasseriaud L (2015) Interactions entre levures Saccharomyces cerevisiae et non-Saccharomyces en vinification: Incidence de facteurs de l’environnement. Univeristé de BordeauxGoogle Scholar
  23. Chasseriaud L, Coulon J, Marullo P, Albertin W, Bely M (2018) Effect of grape must saturation with carbon dioxide at the beginning of alcoholic fermentation: valorisation of species of interest. Appl Microbiol BiotechnolGoogle Scholar
  24. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  25. Costello P, Francis I, Bartowsky E (2012) Variations in the effect of malolactic fermentation on the chemical and sensory properties of Cabernet Sauvignon wine: interactive influences of Oenococcus oeni strain and wine matrix composition. Aust J Grape Wine Res 18:287–301. CrossRefGoogle Scholar
  26. Cretin BN, Dubourdieu D, Marchal A (2018) Influence of ethanol content on sweetness and bitterness perception in dry wines. LWT Food Sci Technol 87:61–66. CrossRefGoogle Scholar
  27. da Silva T, Albertin W, Dillmann C, Bely M, la Guerche S, Giraud C, Huet S, Sicard D, Masneuf-Pomarede I, de Vienne D, Marullo P (2015) Hybridization within Saccharomyces genus results in homoeostasis and phenotypic novelty in winemaking conditions. PLoS One 10:e0123834. PubMedPubMedCentralCrossRefGoogle Scholar
  28. Darriet P, Nikolantonaki M, Schuttler A, Rauhut D, Pons A, Stamatopoulos P (2013) From compounds to sensory perception: what affects complexity and uniqueness of wine aromas? In: AWITC15, SydneyGoogle Scholar
  29. Dashko S, Zhou N, Tinta T, Sivilotti P, Lemut MS, Trost K, Gamero A, Boekhout T, Butinar L, Vrhovsek U (2015) Use of non-conventional yeast improves the wine aroma profile of Ribolla Gialla. J Ind Microbiol Biotechnol 42:997–1010. PubMedCrossRefGoogle Scholar
  30. Day MP, Schmidt SA, Smith PA, Wilkes EN (2015) Use and impact of oxygen during winemaking. Aust J Grape Wine Res 21:693–704. CrossRefGoogle Scholar
  31. de Ovalle S, Cavello I, Brena BM, Cavalitto S, González-Pombo P (2018) Production and characterization of a β-glucosidase from Issatchenkia terricola and its use for hydrolysis of aromatic precursors in Cabernet Sauvignon wine. LWT Food Sci Technol 87:515–522. CrossRefGoogle Scholar
  32. del Barrio-Galan R, Caceres-Mella A, Medel-Maraboli M, Pena-Neira A (2015) Effect of selected Saccharomyces cerevisiae yeast strains and different aging techniques on the polysaccharide and polyphenolic composition and sensorial characteristics of Cabernet Sauvignon red wines. J Sci Food Agric 95:2132–2144. PubMedCrossRefGoogle Scholar
  33. Del Mónaco SM, Curilen Y, Maturano RDC, Bravo SME, Simes AB, Caballero AC (2016) The use of indigenous yeast to develop high-quality Patagonian wines. In: Grape and wine biotechnology. InTech,Google Scholar
  34. Di Maro E, Ercolini D, Coppola S (2007) Yeast dynamics during spontaneous wine fermentation of the Catalanesca grape. Int J Food Microbiol 117:201–210. PubMedCrossRefGoogle Scholar
  35. Domizio P, Lencioni L, Ciani M, Di Blasi S, Pontremolesi CD, Sabatelli M (2007) Spontaneous and inoculated yeast populations dynamics and their effect on organoleptic characters of Vinsanto wine under different process conditions. Int J Food Microbiol 115:281–289. PubMedCrossRefGoogle Scholar
  36. Drewnowski A (2001) The science and complexity of bitter taste. Nutr Rev 59:163–169PubMedCrossRefGoogle Scholar
  37. Dubourdieu D (2011) La valeur du vin entre nature et culture, réflexions sur le goût mondial et la typicité. In: Oeno2011, Bordeaux, France, DunodGoogle Scholar
  38. Dubourdieu D, Tominaga T, Masneuf-Pomarede I, Peyrot des Gachons C, Murat ML (2006) The role of yeasts in grape flavor development during fermentation: the example of Sauvignon Blanc. Am J Enol Vitic 57:81–88Google Scholar
  39. Escot S, Feuillat M, Dulau L, Charpentier C (2001) Release of polysaccharides by yeasts and the influence of released polysaccharides on colour stability and wine astringency. Aust J Grape Wine Res 7:153–159. CrossRefGoogle Scholar
  40. Etievant PX, Marie S, Issanchou SN (1989) Sensory impact of volatile phenols on red wine aroma: influence of carbonic maceration and time of storage. Sonoma County Wine Library. Sciences des AlimentsGoogle Scholar
  41. Fernández O, Martínez O, Hernández Z, Guadalupe Z, Ayestarán B (2011) Effect of the presence of lysated lees on polysaccharides, color and main phenolic compounds of red wine during barrel ageing. Food Res Int 44:84–91. CrossRefGoogle Scholar
  42. Fleet GH (2003) Yeast interactions and wine flavour. Int J Food Microbiol 86:11–22PubMedCrossRefGoogle Scholar
  43. Fontoin H, Saucier C, Teissedre P-L, Glories Y (2008) Effect of pH, ethanol and acidity on astringency and bitterness of grape seed tannin oligomers in model wine solution. Food Qual Prefer 19:286–291. CrossRefGoogle Scholar
  44. Frost R, Quinones I, Veldhuizen M, Alava JI, Small D, Carreiras M (2015) What can the brain teach us about winemaking? An fMRI study of alcohol level preferences. PLoS One 10:e0119220. PubMedPubMedCentralCrossRefGoogle Scholar
  45. Gammacurta M, Marchand S, Albertin W, Moine V, de Revel G (2014) Impact of yeast strain on Ester levels and fruity aroma persistence during aging of Bordeaux red wines. J Agric Food Chem 62:5378–5389. PubMedCrossRefGoogle Scholar
  46. Gammacurta M, Marchand S, Moine V, de Revel G (2017) Influence of different yeast/lactic acid bacteria combinations on the aromatic profile of red Bordeaux wine. J Sci Food Agric 97:4046–4057. PubMedCrossRefGoogle Scholar
  47. García M, Esteve-Zarzoso B, Crespo J, Cabellos JM, Arroyo T (2017) Yeast monitoring of wine mixed or sequential fermentations made by native strains from D.O. “Vinos de Madrid” using real-time quantitative PCR. Front Microbiol 8.
  48. Gawel R, Van Sluyter SC, Smith PA, Waters EJ (2013) Effect of pH and alcohol on perception of phenolic character in white wine. Am J Enol Vitic 64:425–429. CrossRefGoogle Scholar
  49. Gerbaux V, Vincent B (2001) Effects of volatile phenols on sensory quality of red wines from different cultivars. Revue des Oenologues 99:15–18Google Scholar
  50. Grieco F, Tristezza M, Vetrano C, Bleve G, Panico E, Mita G, Logrieco A (2011) Exploitation of autochthonous micro-organism potential to enhance the quality of Apulian wines. Ann Microbiol 61:67–73CrossRefGoogle Scholar
  51. Grigorica L-G, Niculaua M, Nechita CB, Nistor A-M, Cotea VV (2017) The impact of some commercial yeast strains on aroma compounds and sensorial analysis on two white wine varieties made in PGI Dealurile Olteniei, Romania. In: BIO Web of Conferences, EDP Sciences, p 02006Google Scholar
  52. Harzing AWK, van der Wal R (2008) Google Scholar as a new source for citation analysis. Ethics in Science and Environmental Politics 8:61–73CrossRefGoogle Scholar
  53. Henick-Kling T, Edinger W, Daniel P, Monk P (1998) Selective effects of sulfur dioxide and yeast starter culture addition on indigenous yeast populations and sensory characteristics of wine. J Appl Microbiol 84:865–876. CrossRefGoogle Scholar
  54. Howell KS, Cozzolino D, Bartowsky EJ, Fleet GH, Henschke PA (2006) Metabolic profiling as a tool for revealing Saccharomyces interactions during wine fermentation. FEMS Yeast Res 6:91–101. PubMedCrossRefGoogle Scholar
  55. Hranilovic A, Li S, Boss PK, Bindon K, Ristic R, Grbin PR, Van der Westhuizen T, Jiranek V (2018, 2018) Chemical and sensory profiling of Shiraz wines co-fermented with commercial non-Saccharomyces inocula. Aust J Grape Wine Res.
  56. Hu K, Qin Y, Tao YS, Zhu XL, Peng CT, Ullah N (2016) Potential of glycosidase from non-Saccharomyces isolates for enhancement of wine aroma. J Food Sci 81:M935–M943. PubMedCrossRefGoogle Scholar
  57. Jackson RS (2017) Wine tasting. A professional handbook. Third edition. Academic Press. doi:
  58. Jarosz DF, Brown JC, Walker GA, Datta MS, Ung WL, Lancaster AK, Rotem A, Chang A, Newby GA, Weitz DA, Bisson LF, Lindquist S (2014) Cross-kingdom chemical communication drives a heritable, mutually beneficial prion-based transformation of metabolism. Cell 158:1083–1093. PubMedPubMedCentralCrossRefGoogle Scholar
  59. Jellinek JS, Köster EP (1979) Perceived fragrance complexity and its relation to familiarity and pleasantness. J Soc Cosmet Chem 30:253–262Google Scholar
  60. Jones PR, Gawel R, Francis IL, Waters EJ (2008) The influence of interactions between major white wine components on the aroma, flavour and texture of model white wine. Food Qual Prefer 19:596–607. CrossRefGoogle Scholar
  61. Kemsawasd V, Branco P, Almeida MG, Caldeira J, Albergaria H, Arneborg N (2015) Cell-to-cell contact and antimicrobial peptides play a combined role in the death of Lachanchea thermotolerans during mixed-culture alcoholic fermentation with Saccharomyces cerevisiae. FEMS Microbiol Lett 362.
  62. King ES, Swiegers JH, Travis B, Francis IL, Bastian SEP, Pretorius IS (2008) Coinoculated fermentations using Saccharomyces yeasts affect the volatile composition and sensory properties of Vitis vinifera L. cv. Sauvignon Blanc wines. J Agric Food Chem 56:10829–10837. PubMedCrossRefGoogle Scholar
  63. Kramer M (2012) How to really taste wine. The six most important words in wine tasting, Wine SpectatorGoogle Scholar
  64. Laing DG, Francis GW (1989) The capacity of humans to identify odors in mixtures. Physiol Behav 46:809–814PubMedCrossRefGoogle Scholar
  65. Léger A, Hocquellet A, Dieryck W, Moine V, Marchal A, Marullo P, Josseaume A, Cabanne C (2017) Production and purification of the native Saccharomyces cerevisiae Hsp12 in Escherichia coli. J Agric Food Chem 65:8154–8161. PubMedCrossRefGoogle Scholar
  66. Lévy CM, Köster EP (1999) The relevance of initial hedonic judgements in the prediction of subtle food choices. Food Qual Prefer 10:185–200. CrossRefGoogle Scholar
  67. Liu N, Qin Y, Song Y, Ye D, Yuan W, Pei Y, Xue B, Liu Y (2015) Selection of indigenous Saccharomyces cerevisiae strains in Shanshan County (Xinjiang, China) for winemaking and their aroma-producing characteristics. World J Microbiol Biotechnol 31:1781–1792. PubMedCrossRefGoogle Scholar
  68. Livermore A, Laing DG (1996) Influence of training and experience on the perception of multicomponent odor mixtures. J Exp Psychol Hum Percep Perform 22:267–277CrossRefGoogle Scholar
  69. 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. CrossRefGoogle Scholar
  70. Loira I, Vejarano R, Morata A, Ricardo-da-Silva JM, Laureano O, Gonzalez MC, Suarez-Lepe JA (2013) Effect of Saccharomyces strains on the quality of red wines aged on lees. Food Chem 139:1044–1051. PubMedCrossRefGoogle Scholar
  71. Lonvaud-Funel A (1999) Lactic acid bacteria in the quality improvement and depreciation of wine. Antonie Van Leeuwenhoek 76:317–331. PubMedCrossRefGoogle Scholar
  72. Lopes CA, Rodriguez ME, Sangorrin M, Querol A, Caballero AC (2007) Patagonian wines: implantation of an indigenous strain of Saccharomyces cerevisiae in fermentations conducted in traditional and modern cellars. J Ind Microbiol Biotechnol 34:139–149. PubMedCrossRefGoogle Scholar
  73. López R, López-Alfaro I, Gutiérrez AR, Tenorio C, Garijo P, González-Arenzana L, Santamaría P (2011) Malolactic fermentation of Tempranillo wine: contribution of the lactic acid bacteria inoculation to sensory quality and chemical composition. Int J Food Sci Technol 46:2373–2381. CrossRefGoogle Scholar
  74. Lytra G, Franc C, Cameleyre M, Barbe JC (2017) Study of substituted Ester formation in red wine by the development of a new method for quantitative determination and enantiomeric separation of their corresponding acids. J Agric Food Chem 65:5018–5025. PubMedCrossRefGoogle Scholar
  75. Lytra G, Tempere S, de Revel G, Barbe JC (2014) Distribution and organoleptic impact of ethyl 2-methylbutanoate enantiomers in wine. J Agric Food Chem 62:5005–5010. PubMedCrossRefGoogle Scholar
  76. Lytra G, Tempere S, Le Floch A, de Revel G, Barbe JC (2013) Study of sensory interactions among red wine fruity esters in a model solution. J Agric Food Chem 61:8504–8513. PubMedCrossRefGoogle Scholar
  77. Lytra G, Tempere S, Revel GD, Barbe J-C (2012) Impact of perceptive interactions on red wine fruity aroma. J Agric Food Chem 60:12260–12269. PubMedCrossRefGoogle Scholar
  78. Mahaney P, Frey S, Henry T, Paris P Influence of the barrel on the growth of Brettanomyces yeast in barreled red wine. In: Proceedings from the 5th Intervitis Interfructa International Symposium, Stuttgart, Germany, 1998. pp 260–269Google Scholar
  79. Majdak A, Herjavec S, Orlic S, Redzepovic S, Mirosevic N (2002) Comparison of wine aroma compounds produced by Saccharomyces paradoxus and Saccharomyces cerevisiae strain. Food Technol Biotechnol 40:103–110Google Scholar
  80. Marchal A, Marullo P, Durand C, Moine V, Dubourdieu D (2015) Fermentative conditions modulating sweetness in dry wines: genetics and environmental factors influencing the expression level of the Saccharomyces cerevisiae HSP12 gene. J Agric Food Chem 63:304–311. PubMedCrossRefGoogle Scholar
  81. Marchal A, Marullo P, Moine V, Dubourdieu D (2011) Influence of yeast macromolecules on sweetness in dry wines: role of the Saccharomyces cerevisiae protein Hsp12. J Agric Food Chem 59:2004–2010. PubMedCrossRefGoogle Scholar
  82. 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. PubMedCrossRefGoogle Scholar
  83. Mendoza LM, Manca de Nadra MC, Farías ME (2007) Kinetics and metabolic behavior of a composite culture of Kloeckera apiculata and Saccharomyces cerevisiae wine related strains. Biotechnol Lett 29:1057–1063. PubMedCrossRefGoogle Scholar
  84. Moreno J, Moreno-García J, López-Muñoz B, Mauricio JC, García-Martínez T (2016) Use of a flor velum yeast for modulating colour, ethanol and major aroma compound contents in red wine. Food Chem 213:90–97. PubMedCrossRefGoogle Scholar
  85. Moskowitz HR, Barbe CD (1977) Profiling of odor components and their mixtures. Sens Processes 1:212–226PubMedGoogle Scholar
  86. Nikolaou E, Soufleros EH, Bouloumpasi E, Tzanetakis N (2006) Selection of indigenous Saccharomyces cerevisiae strains according to their oenological characteristics and vinification results. Food Microbiol 23:205–211. PubMedCrossRefGoogle Scholar
  87. 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. PubMedCrossRefGoogle Scholar
  88. OIV (2015) Review document on sensory analysis of wineGoogle Scholar
  89. 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. PubMedPubMedCentralGoogle Scholar
  90. Parr WV, Mouret M, Blackmore S, Pelquest-Hunt T, Urdapilleta I (2011) Representation of complexity in wine: influence of expertise. Food Qual Prefer 22:647–660. CrossRefGoogle Scholar
  91. Patrignani F, Montanari C, Serrazanetti DI, Braschi G, Vernocchi P, Tabanelli G, Parpinello GP, Versari A, Gardini F, Lanciotti R (2017) Characterisation of yeast microbiota, chemical and sensory properties of organic and biodynamic Sangiovese red wines. Ann Microbiol 67:99–109CrossRefGoogle Scholar
  92. Perez-Torrado R, Barrio E, Querol A (2017) Alternative yeasts for winemaking: Saccharomyces non-cerevisiae and its hybrids. Crit Rev Food Sci Nutr:1–11.
  93. Pineau B, Barbe J-C, Van Leeuwen C, Dubourdieu D (2011) Contribution of grape skin and fermentation microorganisms to the development of red-and black-berry aroma in Merlot wines. OENO One 45:27–37. CrossRefGoogle Scholar
  94. Pineau B, Barbe JC, Van Leeuwen C, Dubourdieu D (2009) Examples of perceptive interactions involved in specific “red-” and “black-berry” aromas in red wines. J Agric Food Chem 57:3702–3708. PubMedCrossRefGoogle Scholar
  95. Ramakrishnan V, Walker GA, Fan Q, Ogawa M, Luo Y, Luong P, Joseph CML, Bisson LF (2016) Inter-kingdom modification of metabolic behavior: [GAR+] prion induction in Saccharomyces cerevisiae mediated by wine ecosystem Bacteria. Front Ecol Evol 4.
  96. 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. PubMedCrossRefGoogle Scholar
  97. Renault P, Coulon J, de Revel G, Barbe JC, 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. PubMedCrossRefGoogle Scholar
  98. 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. PubMedPubMedCentralCrossRefGoogle Scholar
  99. Renault P, Miot-Sertier C, Marullo P, Hernandez-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. PubMedCrossRefGoogle Scholar
  100. Renault PE, Albertin W, Bely M (2013) An innovative tool reveals interaction mechanisms among yeast populations under oenological conditions. Appl Microbiol Biotechnol 97:4105–4119. PubMedCrossRefGoogle Scholar
  101. Ribéreau-Gayon P, Dubourdieu D, Donèche B, Lonvaud A (2006) Handbook of enology: the microbiology of wine and vinifications, vol 1. John Wiley & Sons, Ltd.
  102. Rivero D, Berná L, Stefanini I, Baruffini E, Bergerat A, Csikász-Nagy A, De Filippo C, Cavalieri D (2015) Hsp12p and PAU genes are involved in ecological interactions between natural yeast strains. Environ Microbiol 17:3069–3081. PubMedCrossRefGoogle Scholar
  103. Rodriguez SB, Amberg E, Thornton R, McLellan M (1990) Malolactic fermentation in chardonnay: growth and sensory effects of commercial strains of Leuconostoc oenos. J Appl Microbiol 68:139–144Google Scholar
  104. Sáenz-Navajas M-P, Fernández-Zurbano P, Ferreira V (2012) Contribution of nonvolatile composition to wine flavor. Food Rev Int 28:389–411. CrossRefGoogle Scholar
  105. San-Juan F, Ferreira V, Cacho J, Escudero A (2011) Quality and aromatic sensory descriptors (mainly fresh and dry fruit character) of Spanish red wines can be predicted from their aroma-active chemical composition. J Agric Food Chem 59:7916–7924. PubMedCrossRefGoogle Scholar
  106. Sannino C (2013) Influence of autochthonous microbiota on the SICILIAN wine production. Universita degli Studi di PalermoGoogle Scholar
  107. Schlich P, Medel Maraboli M, Urbano C, Parr WV (2015) Perceived complexity in Sauvignon Blanc wines: influence of domain-specific expertise. Aust J Grape Wine Res 21:168–178. CrossRefGoogle Scholar
  108. Schreier P, Jennings WG (1979) Flavor composition of wines: a review. C R C Crit Rev Food Sci Nutr 12:59–111. CrossRefGoogle Scholar
  109. Segurel MA, Razungles AJ, Riou C, Salles M, Baumes RL (2004) Contribution of dimethyl sulfide to the aroma of Syrah and Grenache Noir wines and estimation of its potential in grapes of these varieties. J Agric Food Chem 52:7084–7093. PubMedCrossRefGoogle Scholar
  110. Singleton VL, Ough CS (1962) Complexity of flavor and blending of wines. J Food Sci 27:189–196. CrossRefGoogle Scholar
  111. Smith B (2012) Perspective: complexities of flavour. Nature 486:S6. PubMedCrossRefGoogle Scholar
  112. Soden A, Francis I, Oakey H, Henschke P (2000) Effects of co-fermentation with Candida stellata and Saccharomyces cerevisiae on the aroma and composition of Chardonnay wine. Aust J Grape Wine Res 6:21–30CrossRefGoogle Scholar
  113. Swiegers JH, Pretorius IS (2005) Yeast modulation of wine flavor. Adv Appl Microbiol 57:131–175. PubMedCrossRefGoogle Scholar
  114. Takush D, Osborne J (2012) Impact of yeast on the aroma and flavour of Oregon Pinot Noir wine. Aust J Grape Wine Res 18:131–137. CrossRefGoogle Scholar
  115. Tempere S, Schaaper MH, Cuzange E, de Lescar R, de Revel G, Sicard G (2016) The olfactory masking effect of ethylphenols: characterization and elucidation of its origin. Food Qual Prefer 50:135–144. CrossRefGoogle Scholar
  116. Thomas-Danguin T, Sinding C, Romagny S, El Mountassir F, Atanasova B, Le Berre E, Le Bon AM, Coureaud G (2014) The perception of odor objects in everyday life: a review on the processing of odor mixtures. Front Psychol 5:504. PubMedPubMedCentralCrossRefGoogle Scholar
  117. 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.
  118. Tristezza M, Vetrano C, Bleve G, Grieco F, Tufariello M, Quarta A, Mita G, Spano G (2012) Autochthonous fermentation starters for the industrial production of Negroamaro wines. J Ind Microbiol Biotechnol 39:81–92. PubMedCrossRefGoogle Scholar
  119. Tronchoni J, Curiel JA, Morales P, Torres-Pérez R, Gonzalez R (2017) Early transcriptional response to biotic stress in mixed starter fermentations involving Saccharomyces cerevisiae and Torulaspora delbrueckii. Int J Food Microbiol 241:60–68. PubMedCrossRefGoogle Scholar
  120. Ugliano M, Travis B, Francis IL, Henschke PA (2010) Volatile composition and sensory properties of shiraz wines as affected by nitrogen supplementation and yeast species: rationalizing nitrogen modulation of wine aroma. J Agric Food Chem 58:12417–12425. PubMedCrossRefGoogle Scholar
  121. Varela C, Barker A, Tran T, Borneman A, Curtin C (2017) Sensory profile and volatile aroma composition of reduced alcohol Merlot wines fermented with Metschnikowia pulcherrima and Saccharomyces uvarum. Int J Food Microbiol 252:1–9. PubMedCrossRefGoogle Scholar
  122. Versari A, Patrizi C, Parpinello GP, Mattioli AU, Pasini L, Meglioli M, Longhini G (2016) Effect of co-inoculation with yeast and bacteria on chemical and sensory characteristics of commercial cabernet franc red wine from Switzerland. J Chem Technol Biotechnol 91:876–882. CrossRefGoogle Scholar
  123. Vidal S, Courcoux P, Francis L, Kwiatkowski M, Gawel R, Williams P, Waters E, Cheynier V (2004) Use of an experimental design approach for evaluation of key wine components on mouth-feel perception. Food Qual Prefer 15:209–217. CrossRefGoogle Scholar
  124. Vigentini I, Maghradze D, Petrozziello M, Bonello F, Mezzapelle V, Valdetara F, Failla O, Foschino R (2016) Indigenous Georgian wine-associated yeasts and grape cultivars to edit the wine quality in a precision oenology perspective. Front Microbiol 7:352. PubMedPubMedCentralCrossRefGoogle Scholar
  125. Volschenk H, Van Vuuren HJJ, Viljoen-Bloom M (2006) Malic acid in wine: origin, function and metabolism during vinification. South African Journal of Enology & Viticulture 27:123–136Google Scholar
  126. Wang X-C, Li A-H, Dizy M, Ullah N, Sun W-X, Tao Y-S (2017) Evaluation of aroma enhancement for “Ecolly” dry white wines by mixed inoculation of selected Rhodotorula mucilaginosa and Saccharomyces cerevisiae. Food Chem 228:550–559. PubMedCrossRefGoogle Scholar
  127. Zimmer A, Durand C, Loira N, Durrens P, Sherman DJ, Marullo P (2014) QTL dissection of lag phase in wine fermentation reveals a new translocation responsible for Saccharomyces cerevisiae adaptation to sulfite. PLoS One 9:e86298. PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Unité de recherche Œnologie EA 4577, USC 1366 INRA, Bordeaux INP, Univ. BordeauxISVVVillenave d’OrnonFrance
  2. 2.Bordeaux Sciences AgroGradignanFrance
  3. 3.BiolaffortBordeauxFrance
  4. 4.ENSCBPBordeaux INPPessacFrance

Personalised recommendations