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.
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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
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
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
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
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
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
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
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
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
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
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
Chatonnet P, Dubourdieu D, Boidron JN, Pons M (1992) The origin of ethylphenols in wines. J Sci Food Agric 60:165–178
Ciani M, Comitini F (2011) Non-Saccharomyces wine yeasts have a promising role in biotechnological approaches to winemaking. Ann Microbiol 61:25–32
Ciani M, Ferraro L (1997) Role of oxygen on acetic acid production by Brettanomyces/Dekkera in winemaking. J Sci Food Agric 75:489–495
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
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
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
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
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
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
Curtin CD, Kennedy E, Henschke PA (2012) Genotype-dependent sulphite tolerance of Australian Dekkera (Brettanomyces) bruxellensis wine isolates. Lett Appl Microbiol 55:56–61
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
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
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
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
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
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
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
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
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
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
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
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
Henschke P, Curtin C, Grbin P (2007) Molecular characterization of the wine spoilage yeast Dekkera (Brettanomyces) bruxellensis. Microbiol Aust 28:76–78
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
Krumbholz G, Tauschanoff W (1933) Mycotorula intermedia n. sp., ein Beitrag zur Kenntnis der Gärungserreger im Wein. Zentralbl Bakteriol 88:366–373
Kurtzman CP, Fell JW, Boekhout T (2011) The yeasts: a taxonomic study, 5th edn. Elsevier, Amsterdam
Lachance MA (1995) Yeast communities in a natural tequila fermentation. Antonie Van Leeuwenhoek 68:151–160
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
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
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
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
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
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
Millet V, Lonvaud-Funel A (2000) The viable but non-culturable state of wine micro-organisms during storage. Lett Appl Microbiol 30:136–41
Nassereddin RA, Yamani MI (2005) Microbiological quality of sous and tamarind, traditional drinks consumed in Jordan. J Food Prot 68:773–777
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
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
Oro L, Ciani M, Comitini F (2014a) Antimicrobial activity of Metschnikowia pulcherrima on wine yeasts. J Appl Microbiol 116:1209–1217
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
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
Phister TG, Mills DA (2003) Real-Time PCR assay for detection and enumeration of Dekkera bruxellensis in wine. Appl Environ Microbiol 69:7430–7434
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
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
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
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
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
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
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
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
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
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
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
Silva P, Cardoso H, Gerós H (2004) Studies on the wine spoilage capacity of Brettanomyces/Dekkera spp. Am J Enol Vitic 55:65–72
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
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
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
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
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
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
van der Walt JP (1964) Dekkera, a new genus of the Saccharomycetaceae. Antonie Van Leeuwenhoek 30:273–280
Vanegas JM, Faller R, Longo ML (2010) Influence of ethanol on lipid/sterol membranes: phase diagram construction from AFM imaging. Langmuir 26:10415–10418
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
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
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
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
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
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
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).
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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
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DOI: https://doi.org/10.1007/s11274-017-2345-z
Keywords
- Dekkera bruxellensis
- Wine spoilage yeasts
- Volatile phenols
- Sulphur dioxide
- VBNC