Microbiological, biochemical, physicochemical surface properties and biofilm forming ability of Brettanomyces bruxellensis
- 94 Downloads
Brettanomyces bruxellensis is a serious source of concern for winemakers. The production of volatile phenols by the yeast species confers to wine unpleasant sensory characteristics which are unacceptable by the consumers and inevitably provoke economic loss for the wine industry. This ubiquitous yeast is able to adapt to all winemaking steps and to withstand various environmental conditions. Moreover, the ability of B. bruxellensis to adhere and colonize inert materials can be the cause of the yeast persistence in the cellars and thus recurrent wine spoilage. We therefore investigated the surface properties, biofilm formation capacity, and the factors which may affect the attachment of the yeast cells to surfaces with eight strains representative of the genetic diversity of the species.
The eight strains of B. bruxellensis were isolated from different geographical and industrial fermentation origins. The cells were grown in synthetic YPD medium containing 1% (w/v) yeast extract (Difco Laboratories, Detroit), 2% (w/v) bacto peptone (Difco), and 1% (w/v) glucose. Surface physicochemical properties as electrophoretic mobility and adhesion to hydrocarbon of the cells were studied. The ability of the strains to form biofilm was quantified using a colorimetric microtiter 96-well polystyrene plate. Biochemical characteristics were examined by colorimetric methods as well as by chemical analysis.
Our results show that the biofilm formation ability is strain-dependent and suggest a possible link between the physicochemical properties of the studied strains and their corresponding genetic group.
The capacity to detect and identify the strains of the spoilage yeast based on their biofilm formation abilities may help to develop more efficient cleaning procedures and preventing methods.
KeywordsBrettanomyces bruxellensis Wine spoilage Biochemical properties Physico-chemical surface properties Biofilm formation
This work was supported by funds from FranceAgriMer. Lipids analysis was performed at the lipidomic plateform of Bordeaux University.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
This work does not contain any studies with human participants or animals performed by any of the authors.
Informed consent was obtained from all individual participants included in the study. The study has been also published as a preprint version with doi https://doi.org/10.1101/579144.
- Agnolucci M, Tirelli A, Cocolin L, Toffanin A (2017) Brettanomyces bruxellensis yeasts: impact on wine and winemaking. World J Microbiol Biotechnol 33(10):180Google Scholar
- Albertin W, Panfili A, Miot-Sertier C, Goulielmakis A, Delcamp A, Salin F, Lonvaud-Funel A, Curtin C, Masneuf-Pomarede I (2014) Development of microsatellite markers for the rapid and reliable genotyping of Brettanomyces bruxellensis at strain level. Food Microbiol 42:188–195Google Scholar
- Albertin W, Masneuf-Pomarede I, Peltier E (2017) Method for analysing a sample to detect the presence of sulphite-resistant yeasts of the Brettanomyces bruxellensis species and kit for implementing same. France patent no. PCT/FR2016/052701Google Scholar
- Avramova M, Cibrario A, Peltier E, Coton M, Coton E, Schacherer J, Spano G, Capozzi V, Blaiotta G, Salin F, Dols-Lafargue M, Grbin P, Curtin C, Albertin W, Masneuf-Pomarede I (2018a) Brettanomyces bruxellensis population survey reveals a diploid-triploid complex structured according to substrate of isolation and geographical distribution. Sci Rep 8(1):4136Google Scholar
- Avramova M, Vallet-Courbin A, Maupeu J, Masneuf-Pomarède I, Albertin W (2018b) Molecular diagnosis of Brettanomyces bruxellensis sulfur dioxide sensitivity through genotype specific method. Front Microbiol 9:1260Google Scholar
- Barata A, Caldeira J, Botelheiro R, Pagliara D, Malfeito-Ferreira M, Loureiro V (2008) Survival patterns of Dekkera bruxellensis in wines and inhibitory effect of Sulphur dioxide. Int J Food Microbiol 121:201–207Google Scholar
- Belda I, Zarraonaindia I, Perisin M, Palacios A, Acedo A (2017) From vineyard soil to wine fermentation: microbiome approximations to explain the “terroir” concept. Front Microbiol 8:821Google Scholar
- Bellon-Fontaine MN, Rault J, Van Oss C (1996) Microbial adhesion to solvents: a novel method to determine the electron-donor/electron-acceptor or Lewis acid-base properties of microbial cells. Colloids Surf B: Biointerfaces 7:47–53Google Scholar
- Borneman AR, Zeppel R, Chambers PJ, Curtin CD (2014) Insights into the Dekkera bruxellensis genomic landscape: comparative genomics reveals variations in ploidy and nutrient utilisation potential amongst wine isolates. PLoS Genet 13(2):10Google Scholar
- Capozzi V, Di Toro MR, Grieco F, Michelotti V, Salma M, Lamontanara A, Russo P, Orrù L, Alexandre H, Spano G (2016) Viable but not Culturable (VBNC) state of Brettanomyces bruxellensis in wine: new insights on molecular basis of VBNC behaviour using a transcriptomic approach. Food Microbiol 59:196–204Google Scholar
- Carpentier and Cerf (1993) Biofilms and their consequences with particular reference to hygiene in the food industry, J Appl Bacteriol 75:499–511Google Scholar
- Chatonnet P, Dubourdieu D, Boidron JN (1992) Incidence des conditions de fermentation et d’élevage des vins blancs secs en barriques sur leur composition en substances cédées par le bois de chêne. Sci Aliment 12:665–685Google Scholar
- Chatonnet P, Dubourdieu D, Boidron JN (1995) The influence of Brettanomyces/Dekkera sp. yeasts and lactic acid Bacteria on the Ethylphenol content of red wines. Am J Enol Vitic 46:463–468Google Scholar
- Conterno L, Fondazione E, Henick-Kling T (2010) Brettanomyces/Dekkera off-flavours and other wine faults associated with microbial spoilage, in: Reynolds, a.G. (Ed.), managing wine quality, Woodhead publishing series in food science, technology and nutrition. Reynolds, Andrew G. managing wine quality. Am J Enol Vitic 57:139–147Google Scholar
- Curtin C, Kennedy E, Henschke PA (2012) Genotype-dependent sulphite tolerance of Australian Dekkera (Brettanomyces) bruxellensis wine isolates. Lett Appl Microbiol 55:56–61Google Scholar
- Delsart C, Grimi N, Boussetta N, Miot Sertier C, Ghidossi R, Vorobiev E, Mietton PM (2016) Impact of pulsed-electric field and high-voltage electrical discharges on red wine microbial stabilization and quality characteristics. J Appl Microbiol 120:152–164Google Scholar
- Di Toro MR, Capozzi V, Beneduce L, Alexandre H, Tristezza M, Durante M, Spano G (2015) Intraspecific biodiversity and ‘spoilage potential’ of Brettanomyces bruxellensis in Apulian wines LWT-Food Science and Technology 60(1):102–108Google Scholar
- Dimopoulou M, Bardeau T, Ramonet PY, Miot-Certier C, Claisse O, Doco T, Petrel M, Lucas P, Dols-Lafargue M (2016) Exopolysaccharides produced by Oenococcus oeni: from genomic and phenotypic analysis to technological valorization. Food Microbiol 53:10–17Google Scholar
- Dimopoulou M, Hatzikamari M, Masneuf-Pomarede I, Albertin W (2019) Sulfur dioxide response of Brettanomyces bruxellensis strains isolated from Greek wine. Food Microbiol 78:155–163Google Scholar
- Fournier T, Gounot JS, Freel K, Cruaud C, Lemainque A, Aury JM, Wincker P, Schacherer J, Friedrich A (2017) High-Quality de Novo Genome Assembly of the Dekkera bruxellensis Yeast Using Nanopore MinION Sequencing. G3 (Bethesda) 7(10):3243–3250Google Scholar
- Gagiano M, van Dyk D, Bauer F, Lambrechts MG, Pretorius IS (1999) Msn1p/Mss10p, Mss11p and Muc1p/Flo11p are part of a signal transduction pathway downstream of Mep2p regulating invasive growth and pseudohyphal differentiation in Saccharomyces cerevisiae. Mol Microbiol 31:103–116Google Scholar
- Garde-Cerdán T, Ancín-Azpilicueta C (2006) Review of quality factors on wine ageing in oak barrels. Trends Food Sci Technol 17:438–447Google Scholar
- Ghafoor A, Hay ID, Rehm BHA (2011) Role of exopolysaccharides in Pseudomonas aeruginosa biofilm formation and architecture. Appl Environ Microbiol 77:5238–5246Google Scholar
- González-Arenzana L, Santamaría P, López R, Garijo P, Gutiérrez AR, Garde-Cerdán T, López-Alfaro I (2013) Microwave technology as a new tool to improve microbiological control of oak barrels: a preliminary study. Food Control 30:536–539Google Scholar
- Grangeteau C, Gerhards D, von Wallbrunn C, Alexandre H, Rousseaux S, Guilloux-Benatier M (2016) Persistence of two non-Saccharomyces yeasts (Hanseniaspora and Starmerella) in the cellar. Front Microbiol 7:268Google 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 19:180–188Google Scholar
- Guzzon R, Larcher R, Guarcello R, Francesca N, Settanni L, Moschetti G (2018) Spoilage potential of brettanomyces bruxellensis strains isolated from Italian wines. Food Res Int 105:668–677Google Scholar
- Joseph L, Kumar G, Su E, Bisson LF (2007) Adhesion and biofilm production by wine isolates of Brettanomyces bruxellensis. Am J Enol Vitic 58:373–378Google Scholar
- Kang S, Choi H (2005) Effect of surface hydrophobicity on the adhesion of S. cerevisiae onto modified surfaces by poly (styrene-ran-sulfonic acid) random copolymers. Colloids Surf B: Biointerfaces 46:70–77Google Scholar
- Legras JL, Moreno-Garcia J, Zara S, Zara G, Garcia-Martinez T, Mauricio JC, Mannazzu I, Coi AL, Bou Zeidan M, Dequin S, Moreno J, Budroni M (2016) Flor yeast: new perspectives beyond wine aging. Front Microbiol 7:503Google Scholar
- Liu Y, Rousseaux S, Tourdot-Maréchal R, Sadoudi M, Gougeon R, Schmitt-Kopplin P, Alexandre H (2017) Wine microbiome: a dynamic world of microbial interactions. Crit Rev Food Sci Nutr 57:856–873Google Scholar
- Longin C, Degueurce C, Julliat F, Guilloux-Benatier M, Rousseaux S, Alexandre H (2016) Efficiency of population-dependent sulfite against Brettanomyces bruxellensis in red wine. Food Res Int 89:620–630Google Scholar
- Ludwig TG, Goldberg HJV (1956) The Anthrone method for the determination of carbohydrates in foods and in Oral rinsing. J Dent Res 35(1):90–94Google Scholar
- O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79Google Scholar
- Redón M, Guillamón JM, Mas A, Rozès N (2009) Effect of lipid supplementation upon Saccharomyces cerevisiae lipid composition and fermentation performance at low temperature. Eur Food Res Technol 228:833–840Google Scholar
- Renouf V, Falcou M, Miot-Sertier C, Perello MC, De Revel G, Lonvaud-Funel A (2006) Interactions between Brettanomyces bruxellensis and the other yeast species during the first steps of winemaking. J Appl Microbiol 100:1208–1219Google Scholar
- Reynolds T, Fink GR (2001) Bakers' yeast, a model for fungal biofilm formation. Science 291:878–881Google 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(6):1577–1585Google Scholar
- Rozès N, Garcìa-Jares C, Larue F, Lonvaud-Funel A (1992) Differentiation between fermenting and spoilage yeasts in wine by total free fatty acid analysis. J Sci Food Agric 59:351–357Google Scholar
- Rubio P, Garijo P, Santamaria P, Lopez R, Martinez J, Gutierrez A (2015) Influence of oak origin and ageing on wine spoilage by Brettanomyces yeasts. Food Control 54:176–180Google Scholar
- Sheppard DC, Howell PL (2016) Biofilm exopolysaccharides of pathogenic Fungi: lessons from Bacteria. J Biol Chem 291:12529–12537Google Scholar
- 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 206:24–38Google Scholar
- Tek EL, Sundstrom JF, Gardner JM, Oliver SG, Jiranek V (2018) Evaluation of the ability of commercial wine yeasts to form biofilms (mats) and adhere to plastic: implications for the microbiota of the winery environment. FEMS Microbiol Ecol 94(2):fix188Google Scholar
- Tempère S, Marchal A, Barbe JC, Bely M, Masneuf-Pomarede I, Marullo P, Albertin W (2018) The complexity of wine: clarifying the role of microorganisms. Appl Microbiol Biotechnol 102:3995–4007Google Scholar
- Tronchoni J, Rozès N, Querol A, Guillamón JM (2012) Lipid composition of wine strains of Saccharomyces kudriavzevii and Saccharomyces cerevisiae grown at low temperature. Int J Food Microbiol 155:191–198Google Scholar
- Verstrepen KJ, Klis FM (2006) Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol 60:5–15Google Scholar
- Woolfit M, Rozpedowska E, Piskur J, Wolfe KH (2007) Genome survey sequencing of the wine spoilage yeast Dekkera (Brettanomyces) bruxellensis. Eukaryot Cell 6:721–733Google Scholar