Skip to main content

Brettanomyces bruxellensis yeasts: impact on wine and winemaking

Abstract

Yeasts belonging to the Brettanomyces/Dekkera genus are non-conventional yeasts, which affect winemaking by causing wine spoilage all over the world. This mini-review focuses on recent results concerning the presence of Brettanomyces bruxellensis throughout the wine processing chain. Here, culture-dependent and independent methods to detect this yeast on grapes and at the very early stage of wine production are encompassed. Chemical, physical and biological tools, devised for the prevention and control of such a detrimental species during winemaking are also presented. Finally, the mini-review identifies future research areas relevant to the improvement of wine safety and sensory profiles.

This is a preview of subscription content, access via your institution.

References

  • Agnolucci M, Scarano S, Rea F, Toffanin A, Nuti M (2007) Detection of Dekkera/Brettanomyces bruxellensis in pressed sangiovese grapes by real time PCR. Ital J Food Sci 19:153–164

    CAS  Google Scholar 

  • Agnolucci M, Vigentini I, Capurso G, Merico A, Tirelli A, Compagno C, Foschino R, Nuti M (2009) Genetic diversity and physiological traits of Brettanomyces bruxellensis strains isolated from Tuscan Sangiovese wines. Int J Food Microbiol 130:238–244

    Article  CAS  Google Scholar 

  • Agnolucci M, Rea F, Sbrana C, Cristani C, Fracassetti D, Tirelli A, Nuti M (2010) Sulphur dioxide affects culturability and volatile phenol production by Brettanomyces/Dekkera bruxellensis. Int J Food Microbiol 143:76–80

    Article  CAS  Google Scholar 

  • Agnolucci M, Cristani C, Maggini S, Rea F, Cossu A, Tirelli A, Nuti M (2014) Impact of sulphur dioxide on the viability, culturability, and volatile phenol production of Dekkera bruxellensis in wine. Ann Microbiol 64:653–659

    Article  CAS  Google Scholar 

  • Andorrà I, Esteve-Zarzoso B, Guillamón JM, Mas A (2010) Determination of viable wine yeast using DNA binding dyes and quantitative PCR. Int J Food Microbiol 144:257–262

    Article  Google Scholar 

  • Barata A, Pagliara D, Piccininno T, Tarantino F, Ciardulli W, Malfeito Ferreira M, Loureiro V (2008) The effect of sugar concentration and temperature on growth and volatile phenol production by Dekkera bruxellensis in wine. FEMS Yeast Res 8:1097–1102

    Article  CAS  Google Scholar 

  • Campolongo S, Rantsiou K, Giordano M, Gerbi V, Cocolin L (2010) Prevalence and biodiversity of Brettanomyces bruxellensis in wine from northwestern Italy. Am J Enol Vitic 61:486–491

    Article  CAS  Google Scholar 

  • Caruso M, Fiore C, Contrusi M, Salzano G, Paparella A, Romano P (2002) Formation of biogenic amines as criteria for the selection of wine yeasts. World J Microbiol Biotechnol 18:159–163

    Article  CAS  Google Scholar 

  • Cecchini F, Manzano M, Mandabi Y, Perelman E, Marks RS (2012) Chemiluminescent DNA optical fibre sensor for Brettanomyces bruxellensis detection. J Biotechnol 157:25–30

    Article  CAS  Google Scholar 

  • Cecchini F, Iacumin L, Fontanot M, Comuzzo P, Comi G, Manzano M (2013) Dot blot and PCR for Brettanomyces bruxellensis detection in red wine. Food Control 34:40–46

    Article  CAS  Google Scholar 

  • Chandra M, Oro I, Ferreira-Dias S, Malfeito-Ferreira M (2015) Effect of ethanol, sulfur dioxide and glucose on the growth of wine spoilage yeasts using response surface methodology. PLoS ONE 10(6):e0128702. doi:10.1371/journal.pone.0128702

    Article  Google Scholar 

  • Chatonnet P, Dubourdieu D, Boidron JN, Pons M (1992) The origin of ethylphenols in wines. J Sci Food Agric 60:165–178

    Article  CAS  Google Scholar 

  • Ciani M, Comitini F (2011) Non-Saccharomyces wine yeasts have a promising role in biotechnological approaches to winemaking. Ann Microbiol 61:25–32

    Article  Google Scholar 

  • Ciani M, Ferraro L (1997) Role of oxygen on acetic acid production by Brettanomyces/Dekkera in winemaking. J Sci Food Agric 75:489–495

    Article  CAS  Google Scholar 

  • Cocolin L, Rantsiou K, Iacumin L, Zironi R, Comi G (2004) Molecular detection and identification of Brettanomyces/Dekkera bruxellensis and Brettanomyces/Dekkera anomalus in spoiled wines. Appl Environ Microbiol 70:1347–1355

    Article  CAS  Google Scholar 

  • Conterno L, Joseph CML, Arvik TJ, Henick-Kling T, Bisson LF (2006) Genetic and physiological characterization of Brettanomyces bruxellensis strains isolated from wines. Am J Enol Vitic 57:139–147

    CAS  Google Scholar 

  • Couto JA, Barbosa A, Hogg T (2005a) A simple cultural method for the presumptive detection of the yeasts Brettanomyces/Dekkera in wines. Lett Appl Microbiol 41:505–510

    Article  CAS  Google Scholar 

  • Couto JA, Neves F, Campos F, Hogg T (2005b) Thermal inactivation of the wine spoilage yeasts Dekkera/Brettanomyces. Int J Food Microbiol 104:337–344

    Article  CAS  Google Scholar 

  • Crauwels S, Assche A van, Jonge R de, Borneman AR, Verreth C, Troels P, Samblanx G de, Marchal K, Peer Y van de, Willems KA, Verstrepen KJ, Curtin CD, Lievens B (2015) Comparative phenomics and targeted use of genomics reveals variation in carbon and nitrogen assimilation among different Brettanomyces bruxellensis strains. Appl Microbiol Biotechnol 99:9123–9134

    Article  CAS  Google Scholar 

  • Curtin CD, Bellon JR, Henschke PA, Godden PW, de Barros Lopes MA (2007) Genetic diversity of Dekkera bruxellensis yeasts isolated from Australian wineries. FEMS Yeast Res 7:471–481

    Article  CAS  Google Scholar 

  • Curtin CD, Kennedy E, Henschke PA (2012) Genotype-dependent sulphite tolerance of Australian Dekkera (Brettanomyces) bruxellensis wine isolates. Lett Appl Microbiol 55:56–61

    Article  CAS  Google Scholar 

  • Curtin CD, Langhans G, Henschke PA, Grbin PR (2013) Impact of Australian Dekkera bruxellensis strains grown under oxygen-limited conditions on model wine composition and aroma. Food Microbiol 36:241–247

    Article  CAS  Google Scholar 

  • Curtin CD, Varela C, Borneman A (2015) Harnessing improved understanding of Brettanomyces bruxellensis biology to mitigate the risk of wine spoilage. Aust J Grape Wine Res 21:680–692

    Article  Google Scholar 

  • Custers MTJ (1940) Onderzoekingen over het gistgeslacht Brettanomyces. Thesis, Delft

  • Delaherche A, Claisse O, Lonvaud-Funel A (2004) Detection and quantification of Brettanomyces bruxellensis and ‘ropy’ Pediococcus damnosus strains in wine by real-time polymerase chain reaction. J Appl Microbiol 97:910–915

    Article  CAS  Google Scholar 

  • Du Toit WJ, Pretorius IS, Lonvaud-Funel A (2005) The effect of sulphur dioxide and oxygen on the viability and culturability of a strain of Acetobacter pasteurianus and a strain of Brettanomyces bruxellensis isolated from wine. J Appl Microbiol 98:862–871

    Article  CAS  Google Scholar 

  • Egli CM, Henick-Kling T (2001) Identification of Brettanomyces/Dekkera species based on polymorphism in the rRna internal transcribed spacer region. Am J Enol Vitic 52:241–246

    CAS  Google Scholar 

  • Fabrizio V, Vigentini I, Parisi N, Picozzi C, Compagno C, Foschino R (2015) Heat inactivation of wine spoilage yeast Dekkera bruxellensis by hot water treatment. Lett Appl Microbiol 61:186–191

    Article  CAS  Google Scholar 

  • Gonzalez-Arenzana L, Santamaria P, Lopez R, Garijo P, Gutierrez AR, Garde-Cerdan T, Lopez-Alfaro I (2013) Microwave technology as a new tool to improve microbiological control of oak barrels: a preliminary study. Food Control 30:536–539

    Article  Google Scholar 

  • Gonzalez-Arenzana L, Sevenich R, Rauh C, Lopez R, Knorr D, Lopez-Alfaro I (2016) Inactivation of Brettanomyces bruxellensis by high hydrostatic pressure technology. Food Control 59:188–195

    Article  CAS  Google Scholar 

  • Gray S, Rawsthorne H, Dirks B, Phister T (2011) Detection and enumeration of Dekkera anomala in beer, cola, and cider using real-time PCR. Lett Appl Microbiol 52:352–359

    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, mawè, gowé and tchoukoutou by using culture-dependent and -independent methods. Int J Food Microbiol 165:84–88

    Article  CAS  Google Scholar 

  • Guzzon R, Nardin T, Micheletti O, Nicolini G, Larcher R (2013) Antimicrobial activity of ozone. Effectiveness against the main wine spoilage microorganisms and evaluation of impact on simple phenols in wine. Aust J Grape Wine Res 19:180–188

    Article  CAS  Google Scholar 

  • Hayashi N, Arai R, Tada S, Taguchi H, Ogawa Y (2007) Detection and identification of Brettanomyces/Dekkera sp. yeasts with a loop-mediated isothermal amplification method. Food Microbiol 24:778–785

    Article  CAS  Google Scholar 

  • Henschke P, Curtin C, Grbin P (2007) Molecular characterization of the wine spoilage yeast Dekkera (Brettanomyces) bruxellensis. Microbiol Aust 28:76–78

    Google Scholar 

  • Joseph CL, Gorton LW, Ebeler SE, Bisson LF (2013) Production of volatile compounds by wine strains of Brettanomyces bruxellensis grown in the presence of different precursor substrates. Am J Enol Vitic 64:231–240

    Article  CAS  Google Scholar 

  • Krumbholz G, Tauschanoff W (1933) Mycotorula intermedia n. sp., ein Beitrag zur Kenntnis der Gärungserreger im Wein. Zentralbl Bakteriol 88:366–373

    Google Scholar 

  • Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam

    Google Scholar 

  • Lachance MA (1995) Yeast communities in a natural tequila fermentation. Antonie Van Leeuwenhoek 68:151–160

    Article  CAS  Google Scholar 

  • Laforgue R, Lonvaud-Funel A (2012) Hydroxycinnamic acid decarboxylase activity of Brettanomyces bruxellensis involved in volatile phenol production: relationship with cell viability. Food Microbiol 32:230–234

    Article  CAS  Google Scholar 

  • Leaute B, Giboulot M (2013) Study of the distribution of the contamination of the inner surface of a new wine barrel by Brettanomyces bruxellensis. Revue des Oenologues 146:29–30

    Google Scholar 

  • Loureiro V, Malfeito-Ferreira M (2006) Dekkera/Brettanomyces spp. In: C de W Blackburn (ed) Food spoilage microorganisms. Woodhead Publishing Ltd, Abington, pp 353–398

    Google Scholar 

  • Lustrato G, Alfano G, De Leonardis A, Macciola M, Ranalli G (2015) Inactivation of Dekkera bruxellensis yeasts in wine storage in brand new oak barrels using low electric current technology. Ann Microbiol 65:2091–2098

    Article  CAS  Google Scholar 

  • Malfeito-Ferreira M, Laureano P, Barata A, D’Antuono I, Stender H, Loureiro V (2004) Effect of different barrique sanitation procedures on yeasts isolated from the inner layers of wood. Abstr Am J Enol Vitic 55:304A

    Google Scholar 

  • Manzano M, Vizzini P, Jia K, Adam P-M, Ionescu RE (2016) Development of localized surface plasmon resonance biosensors for the detection of Brettanomyces bruxellensis in wine. Sens Actuators B 223:295–300

    Article  CAS  Google Scholar 

  • Millet V, Lonvaud-Funel A (2000) The viable but non-culturable state of wine micro-organisms during storage. Lett Appl Microbiol 30:136–41

    Article  Google Scholar 

  • Nassereddin RA, Yamani MI (2005) Microbiological quality of sous and tamarind, traditional drinks consumed in Jordan. J Food Prot 68:773–777

    Article  Google Scholar 

  • Oelofse A, Pretorius IS, du Toit M (2008) Significance of Brettanomyces and Dekkera during winemaking: a synoptic review. South Afr J Enol Vitic 29:128–144

    CAS  Google Scholar 

  • Oelofse A, Malherbe S, Pretorius IS, Du Toit M (2010) Preliminary evaluation of infrared spectroscopy for the differentiation of Brettanomyces bruxellensis strains isolated from red wines. Int J Food Microbiol 143:136–142

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Oro L, Zara S, Fancellu F, Mannazzu I, Budroni M, Ciani M, Comitini F (2014b) TpBGL2 codes for a Tetrapisispora phaffii killer toxin active against wine spoilage yeasts. FEMS Yeast Res 14:464–471

    Article  CAS  Google Scholar 

  • Palacios A, Borinaga I, Carrillo D (2012) Comparative study on wine barrel disinfection systems and their use as alternatives to sulfur treatment. Enologos 14:46–54

    CAS  Google Scholar 

  • Phister TG, Mills DA (2003) Real-Time PCR assay for detection and enumeration of Dekkera bruxellensis in wine. Appl Environ Microbiol 69:7430–7434

    Article  CAS  Google Scholar 

  • Portugal C, Ruiz-Larrea F (2013) Comparison of specific real-time PCR and conventional culture for detection and enumeration of Brettanomyces in red wines. Am J Enol Vitic 64:139–145

    Article  CAS  Google Scholar 

  • Pozo-Bayon MA, Monagas M, Polo MC, Gomez-Cordoves C (2004) Occurrence of pyranoanthocyanins in sparkling wines manufactured with red grape varieties. J Agric Food Chem 52:1300–1306

    Article  CAS  Google Scholar 

  • Renouf V, Lonvaud-Funel A (2007) Development of an enrichment medium to detect Dekkera/Brettanomyces bruxellensis, a spoilage wine yeast, on the surface of grape berries. Microbiol Res 162:154–167

    Article  CAS  Google Scholar 

  • Renouf V, Falcou M, Miot-Sertier C, Perello MC, De Revel G, Lonvaud-Funel A (2006) Interactions between Brettanomyces bruxellensis and other yeast species during the initial stages of winemaking. J Appl Microbiol 100:1208–1219

    Article  CAS  Google Scholar 

  • Rizzotti L, Levav N, Fracchetti F, Felis GE, Torriani S (2015) Effect of UV-C treatment on the microbial population of white and red wines, as revealed by conventional plating and PMA-qPCR methods. Food Control 47:407–412

    Article  CAS  Google Scholar 

  • Röder C, König H, Fröhlich J (2007) Species-specific identification of Dekkera/Brettanomyces yeasts by fluorescently labeled DNA probes targeting the 26S rRNA. FEMS Yeast Res 7:1013–1026

    Article  Google Scholar 

  • Rodriguez SB, Thornton MA, Thornton RJ (2013) Raman spectroscopy and chemometrics for identification and strain discrimination of the wine spoilage yeasts Saccharomyces cerevisiae, Zygosaccharomyces bailii, and Brettanomyces bruxellensis. Appl Environ Microbiol 79:6264–6270

    Article  CAS  Google Scholar 

  • Romano A, Perello MC, de Revel G, Lonvaud-Funel A (2008) Growth and volatile compound production by Brettanomyces/Dekkera bruxellensis in red wine. J Appl Microbiol 104:1577–1585

    Article  CAS  Google Scholar 

  • Rozpędowska E, Hellborg L, Ishchuk OP, Orhan F, Galafassi S, Merico A, Woolfit M, Compagno C, Piškur J (2011) Parallel evolution of the make–accumulate–consume strategy in Saccharomyces and Dekkera yeasts. Nat Commun 2:302. doi:10.1038/ncomms1305

    Article  Google Scholar 

  • Scheffers WA, Wiken TO (1969) The Custer effect (negative Pasteur effect) as a diagnostic criterion for the genus Brettanomyces. Antonie van Leeuwenhoek 35:31–32

    Google Scholar 

  • Serpaggi V, Remize F, Recorbet G, Gaudot-Dumas E, Sequeira-LeGrand A, Alexandre H (2012) Characterization of the “Viable but non culturable” (VBNC) state in the wine spoilage yeast Brettanomyces. Food Microbiol 30:438–447

    Article  CAS  Google Scholar 

  • Silva P, Cardoso H, Gerós H (2004) Studies on the wine spoilage capacity of Brettanomyces/Dekkera spp. Am J Enol Vitic 55:65–72

    CAS  Google Scholar 

  • Stender H, Kurtzman C, Hyldig-Nielsen JJ, Sørensen D, Broomer A, Oliveira K, Perry-O’Keefe H, Sage A, Young B, Coull J (2001) Identification of Dekkera bruxellensis (Brettanomyces) from wine by fluorescence in situ hybridization using peptide nucleic acid probes. Appl Environ Microbiol 67:938–941

    Article  CAS  Google Scholar 

  • Sturm ME, Arroyo-Lopez FN, Garrido-Fernandez A, Querol A, Mercado LA, Ramirez ML, Combina M (2014) Probabilistic model for the spoilage wine yeast Dekkera bruxellensis as a function of pH, ethanol and free SO2 using time as a dummy variable. Int J Food Microbiol 170:83–90

    Article  CAS  Google Scholar 

  • Tessonnière H, Vidal S, Barnavon L, Alexandre H, Remize F (2009) Design and performance testing of a real-time PCR assay for sensitive and reliable direct quantification of Brettanomyces in wine. Int J Food Microbiol 129:237–243

    Article  Google Scholar 

  • Tofalo R, Schirone M, Corsetti A, Suzzi G (2012) Detection of Brettanomyces spp. in red wines using real-time PCR. J Food Sci 77:M545-M549

    Article  Google Scholar 

  • Usseglio-Tomasset L (1992) Properties and use of sulphur dioxide. International symposium on current issues with food preservatives. Chemico-technical, nutritional and safety in use aspects. Food Addit Contam 9:399–404

    Article  CAS  Google Scholar 

  • Usseglio-Tomasset L, Ciolfi G, Di Stefano R (1982) Influence of anthocyanins on inhibitory action of SO2 in yeasts. Vini d’Italia 24:86–94

    Google Scholar 

  • van der Walt JP (1964) Dekkera, a new genus of the Saccharomycetaceae. Antonie Van Leeuwenhoek 30:273–280

    Article  Google Scholar 

  • Vanegas JM, Faller R, Longo ML (2010) Influence of ethanol on lipid/sterol membranes: phase diagram construction from AFM imaging. Langmuir 26:10415–10418

    Article  CAS  Google Scholar 

  • Vendrame M, Manzano M, Comi G, Bertrand J, Iacumin L (2014) Use of propidium monoazide for the enumeration of viable Brettanomyces bruxellensis in wine and beer by quantitative PCR. Food Microbiol 42:196–204

    Article  CAS  Google Scholar 

  • Vigentini I, Romano A, Compagno C, Merico A, Molinari F, Tirelli A, Foschino R, Volonterio G (2008) Physiological and oenological traits of different Dekkera/Brettanomyces bruxellensis strains under wine-model conditions. FEMS Yeast Res 8:1087–1096

    Article  CAS  Google Scholar 

  • Vigentini I, Joseph CL, Picozzi C, Foschino R, Bisson LF (2013) Assessment of the Brettanomyces bruxellensis metabolome during sulphur dioxide exposure. FEMS Yeast Res 13:597–608

    Article  CAS  Google Scholar 

  • Villalba ML, Saez JS, del Monaco S, Lopes CA, Sangorrin 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  Google Scholar 

  • Willenburg E, Divol B (2012) Quantitative PCR: An appropriate tool to detect viable but not culturable Brettanomyces bruxellensis in wine. Int J Food Microbiol 160:131–136

    Article  CAS  Google Scholar 

  • Zuehlke JM, Edwards CG (2013) Impact of sulfur dioxide and temperature on culturability and viability of Brettanomyces bruxellensis in wine. J Food Protection 76:2024–2030

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We apologize to the colleagues whose work has not been cited due to space limitations. This work was funded by a University of Pisa grant (Progetti di Ateneo).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Monica Agnolucci.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Agnolucci, M., Tirelli, A., Cocolin, L. et al. Brettanomyces bruxellensis yeasts: impact on wine and winemaking. World J Microbiol Biotechnol 33, 180 (2017). https://doi.org/10.1007/s11274-017-2345-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-017-2345-z

Keywords

  • Dekkera bruxellensis
  • Wine spoilage yeasts
  • Volatile phenols
  • Sulphur dioxide
  • VBNC