Elsevier

Food Microbiology

Volume 59, October 2016, Pages 161-175
Food Microbiology

Brettanomyces bruxellensis, a survivalist prepared for the wine apocalypse and other beverages

https://doi.org/10.1016/j.fm.2016.06.008Get rights and content

Highlights

  • The history and literature concerning Brettanomyces bruxellensis is reviewed.

  • The ecological niches associated with B. bruxellensis are discussed.

  • The nutrient composition of each niche is outlined.

  • The nutritional requirements of B. bruxellensis are reviewed.

Abstract

Brettanomyces bruxellensis is a common red wine spoilage yeast. Yet, in addition to wine, it has been isolated from other ecological niches that are just as nutritionally deficient as wine. B. bruxellensis can therefore be regarded as a survivor, well adapted to colonise harsh environments not often inhabited by other yeasts. This review is focused on the nutritional requirements of B. bruxellensis and the relevance thereof for its adaptation to the different matrices within which it occurs. Furthermore, the environmental conditions necessary (e.g. aerobic or anaerobic conditions) for the assimilation of the carbon or nitrogenous sources are discussed in this review. From literature, several confusing inconsistencies, regarding nutritional sources necessary for B. bruxellensis survival, in these specialist ecological niches are evidenced. The main focus of this review is wine but other products and niches that B. bruxellensis inhabits namely beer, cider, fruit juices and bioethanol production plants are also considered. This review highlights the lack of knowledge regarding B. bruxellensis when considering its nutritional requirements in comparison to Saccharomyces cerevisiae. However, there is a large enough body of evidence showing that the nutritional needs of B. bruxellensis are meagre, explaining its ability to colonise harsh environments.

Introduction

Wine is the final product of multiple biotic and abiotic interactions that occur in a complex medium (i.e. grape juice). The former are facilitated by microorganisms of which some are beneficial and others detrimental to wine quality. Certain abiotic factors, which include temperature and the initial chemical composition, play a major role in the composition of the resulting wine. The aforementioned detrimental microorganisms are referred to as spoilage microorganisms. Amongst these, yeasts of the genus Brettanomyces, or their teleomorphs known as Dekkera, have been found to negatively alter the chemical composition of wine by producing by-products detrimental to the organoleptic properties of the final product (Loureiro and Malfeito-Ferreira, 2003). Of this genus, the species Brettanomyces bruxellensis is a spoilage microorganism of wine. B. bruxellensis however, not only occurs in wine but also in many other alcoholic beverages, where it is not considered as a spoilage yeast e.g. some speciality beers and cider (Davenport, 1976, Loureiro and Malfeito-Ferreira, 2006). These yeasts can persist through the harsh conditions that occur during the winemaking process, such as rising ethanol concentrations and increasing additions of sulphur dioxide; they have in recent years become a major oenological concern worldwide.

Generally, many other species of yeasts, that naturally occur on grapes in the vineyard, are present at the onset of alcoholic fermentation but are readily eliminated due to: (i) the increase in ethanol concentration, (ii) the release of toxic compounds (e.g. killer toxins, weak acids, phenolic compounds and sulphur dioxide) by the dominant yeast Saccharomyces cerevisiae, (iii) competition for space and nutrients and (iv) low oxygen conditions (Pretorius et al., 1999, Holm Hansen et al., 2001, Nissen and Arneborg, 2003, Pérez-Nevado et al., 2006). B. bruxellensis however, is commonly isolated in wine and is well suited to surviving on all surfaces in and around the winery: winery walls, presses, fermentation tanks as well as within the wood of barrels used for maturation (Fugelsang, 1997). These environments are opportune for the colonisation of B. bruxellensis while the must is fermenting but even more so when the wine is ageing in barrel. In addition, the formation of biofilms by B. bruxellensis makes disinfection challenging, as biofilms are relatively resistant to chemical cleaning agents and sanitisers (Oelofse et al., 2008). Generally, grape juice is an environment inhabited by many yeasts, including S. cerevisiae the dominant yeast during alcoholic fermentation as well as other non-Saccharomyces yeasts. Amongst these yeasts, B. bruxellensis can also persist in this medium (Renouf et al., 2006). The ability however, of B. bruxellensis to reproduce and grow in wine, as opposed to grape juice, may have resulted in its adaptation to surviving in low nutritional environments.

The aromatic profile of wines is negatively influenced by the yeast B. bruxellensis and tends to be characterised by mousy, medicinal, wet wool, burnt plastic or horse sweat smells/scents. These off-aromas are said to be a part of the “Brett” character in wine (Licker et al., 1999). This is potentially problematic for winemakers, as this can result in serious economic losses (Loureiro and Malfeito-Ferreira, 2003, Fugelsang, 1997). The contamination of wines by B. bruxellensis has increased in recent years due to winemaking techniques changing to favour the production of wines that contain more residual sugar and that may be unsulphited, unfiltered, aged on the lees or aged longer in barrels. All of these factors are considered favourable to B. bruxellensis growth (de Orduña, 2010, Alston et al., 2011).

Although there has been a lot of research on factors influencing the growth of B. bruxellensis, it is surprisingly still uncertain which nutrients (and the concentrations thereof) are required for this microorganism to proliferate in inhospitable environments such as wine. It can be assumed from its ability to proliferate in a nutrient-poor medium that unlike S. cerevisiae, B. bruxellensis displays low nutrient requirements. In this review, the many ecological niches of B. bruxellensis will be reviewed with a primary focus on the nutritional composition of the products or niches concerned, also taking into account the adaptations of this yeast allowing it to survive in these media with varying compositions. Formerly, the history and sources of isolation of B. bruxellensis will be briefly discussed as this organism has been isolated from many different industries and matrices and has been referred to by various names since its discovery. In addition, the more common niches, products and matrices that B. bruxellensis is isolated from, will be discussed with regard to the potential nutrients available to the yeast. The general carbon and nitrogen sources utilised by B. bruxellensis, and its ability to utilise the nutrient sources from the different matrices it is isolated from, will be thoroughly reviewed. Overall, this review aims to provide a systematic and argumentative summary of B. bruxellensis’ nutritional requirements in an attempt to characterise the biological adaptations connected to surviving in a harsh medium.

Section snippets

History of Brettanomyces

Brettanomyces was given its name due to its close connection to the British brewing industry, as it was first isolated in the secondary fermentation of English beers. Indeed, once the initial fermentation by Saccharomyces was completed, it was noted by Claussen, that a secondary slow fermentation occurred. Later, he identified the yeast dominating this secondary fermentation and named it Brettanomyces (Claussen, 1904). Derived from the Greek ’’Brettano’’ meaning British and ’’myces’’ meaning

The ecological niches associated with B. bruxellensis

As mentioned above, B. bruxellensis has been isolated from many ecological niches. These various products and environments display common features/characteristics. Indeed, they are characterised by high alcohol concentrations, with the exception of soft drinks, fruit juices and the initial onset of alcoholic fermentations, and tend to be harsh matrices for microorganisms to live in as they contain limited nutrients, including low residual sugar concentrations and nitrogen sources, depending on

Chemical characterisation of B. bruxellensis’ habitats and the role of B. bruxellensis therein

The major ecological niches and products that host B. bruxellensis will be discussed in detail below. A specific focus will be placed on the nutrient and chemical composition of these different media, a summary of which is outlined in Table 2, and the accommodation of these media for the growth of B. bruxellensis.

The nutritional requirements of B. bruxellensis

Like S. cerevisiae, B. bruxellensis is ethanol tolerant, facultatively anaerobic, Crabtree positive and petite positive, allowing the yeast to produce offspring without mitochondrial DNA (Hellborg and Piskur, 2009). It can therefore ferment preferentially in the presence of high glucose in oxygenated conditions (Kurtzman and Fell, 1998, Piškur et al., 2006). However, unlike S. cerevisiae, B. bruxellensis can appear in situations in which nutrients are scarce (as reviewed in the previous

Conclusion

B. bruxellensis has been isolated from many products and environmental niches. These environments can be divided into those that are poor and generally not conducive for yeast growth, for example bottled wine or beer, as nutrients are scarce (Gilliland, 1961, Shantha Kumara and Verachtert, 1991, Ibeas et al., 1996, Esteve-Zarzoso et al., 2001) and those that are rich in nutrients, such as bioethanol plants, fruit juices and cider (Morrissey et al., 2004, Souza-Liberal et al., 2007, Passoth

References (174)

  • J.D. Duerksen et al.

    Purification and properties of an inductible β-glucosidase of yeast

    J. Biol. Chem.

    (1958)
  • H.K. Dweck et al.

    Olfactory proxy detection of dietary antioxidants in Drosophila

    Curr. Biol.

    (2015)
  • T.H. Gadaga et al.

    Enumeration and identification of yeasts isolated from Zimbabwean traditional fermented milk

    Int. Dairy J.

    (2000)
  • Y.Z. Günata et al.

    The aroma of grapes. I. Extraction and determination of free and glycosidically bound fractions of some grape aroma components

    J. Chromatogr. A

    (1985)
  • J. Jimenez et al.

    Brettanomyces

  • D. Kosse et al.

    Identification of yoghurt-spoiling yeasts with 18S rRNA-targeted oligonucleotide probes

    Syst. Appl. Microbiol.

    (1997)
  • V. Loureiro et al.

    Spoilage yeasts in the wine industry

    Int. J. Food Microbiol.

    (2003)
  • V. Loureiro et al.

    Dekkera/Brettanomyces spp

  • M. Malfeito-Ferreira et al.

    Fatty acid profiling: a feasible typing system to trace yeast contamination in wine bottling plants

    Int. J. Food Microbiol.

    (1997)
  • D.A. Abbott et al.

    Growth rates of Dekkera/Brettanomyces yeasts hinder their ability to compete with Saccharomyces cerevisiae in batch corn mash fermentations

    Appl. Microbiol. Biotechnol.

    (2005)
  • D.G. Abernathy et al.

    Analysis of protein and total usable nitrogen in beer and wine using a microwell ninhydrin assay

    J. Inst. Brew.

    (2009)
  • J.M. Alston et al.

    Too much of a good thing? causes and consequences of increases in sugar content of california wine grapes

    J. Wine Econ.

    (2011)
  • P.R. Ashurst

    Chemistry and Technology of Soft Drinks and Fruit Juices

    (1998)
  • B.M. Bakker et al.

    The mitochondrial alcohol dehydrogenase Adh3p is involved in a redox shuttle in Saccharomyces cerevisiae

    J. Bacteriol.

    (2000)
  • J. Barnett et al.

    Yeasts: Characteristics and Identification

    (1990)
  • A. Barret et al.

    Sur quelques accidents de vinification dus à des levures à voile

    CR Acad. Agric.

    (1955)
  • A.C. Basílio et al.

    Detection and identification of wild yeast contaminants of the industrial fuel ethanol fermentation process

    Curr. Microbiol.

    (2008)
  • M. Beckner et al.

    Microbial contamination of fuel ethanol fermentations

    Lett. Appl. Microbiol.

    (2011)
  • L.F. Bisson

    Influence of nitrogen on yeast and fermentation of grapes

  • J. Blomqvist

    Dekkera Bruxellensis — a Competitive Yeast for Ethanol Production from Conventional and Non-conventional Substrates

    (2011)
  • J. Blomqvist et al.

    Fermentation characteristics of Dekkera bruxellensis strains

    Appl. Microbiol. Biotechnol.

    (2010)
  • J. Blomqvist et al.

    Physiological requirements for growth and competitiveness of Dekkera bruxellensis under oxygen-limited or anaerobic conditions

    Yeast

    (2012)
  • B. Blondin et al.

    Purification and properties of the β -glucosidase of a yeast capable of fermenting cellobiose to ethanol: Dekkera intermedia Van der Walt

    Eur. J. Appl. Microbiol. Biotechnol.

    (1983)
  • A.R. Borneman et al.

    Insights into the Dekkera bruxellensis genomic landscape: comparative genomics reveals variations in ploidy and nutrient utilisation potential amongst wine isolates

    PLoS Genet.

    (2014)
  • C. Brandam et al.

    Effect of temperature on Brettanomyces bruxellensis: metabolic and kinetic aspects

    Can. J. Microbiol.

    (2008)
  • T.J. Britz et al.

    The combination effect of pH, SO2, ethanol and temperature on the growth of Leuconostoc oenos

    J. Appl. Bacteriol.

    (1990)
  • A.J. Buglass

    Handbook of Alcoholic Beverages: Technical, Analytical and Nutritional Aspects

    (2011)
  • J.M. Carrascosa et al.

    Metabolism of acetaldehyde and Custers effect in the yeast Brettanomyces abstinens

    Antonie Leeuwenhoek

    (1981)
  • P. Chatonnet et al.

    The origin of ethylphenols in wines

    J. Sci. Food Agric.

    (1992)
  • P. Chatonnet et al.

    The influence of Brettanomyces/Dekkera spp. yeasts and lactic acid bacteria on the ethyl phenol content of red wines

    Am. J. Enol. Vitic.

    (1995)
  • P. Chatonnet et al.

    Synthesis of volatile phenols by Saccharomyces cerevisiae in wines

    J. Sci. Food Agric.

    (1993)
  • M. Ciani et al.

    Role of oxygen on acetic acid production by Brettanomyces/Dekkera in winemaking

    J. Sci. Food Agric.

    (1997)
  • N.H. Claussen

    On a method for the application of Hansen’s pure yeast system in the manufacturing of well-conditioned English stock beers

    J. Inst. Brew.

    (1904)
  • L. Connel et al.

    Rapid detection and identification of Brettanomyces from winery air samples based in peptide nucleic acid analysis

    Am. J. Enol. Vitic.

    (2002)
  • L. Conterno et al.

    Genetic and physiological characterization of Brettanomyces bruxellensis strains isolated from wines

    Am. J. Enol. Vitic.

    (2006)
  • T.G. Cooper

    Nitrogen metabolism in Saccharomyces cerevisiae

  • S. Crauwels et al.

    Assessing genetic diversity in Brettanomyces yeasts using DNA fingerprinting and Whole-Genome Sequencing

    Appl. Environ. Microbiol.

    (2014)
  • S. Crauwels et al.

    Comparative phenomics and targeted use of genomics reveals variation in carbon and nitrogen assimilation among different Brettanomyces bruxellensis strains

    Appl. Microbiol. Biotechnol.

    (2015)
  • C.D. Curtin et al.

    De-novo assembly and analysis of the heterozygous triploid genome of the wine spoilage yeast Dekkera bruxellensis AWRI1499

    PLoS One

    (2012)
  • C. Curtin et al.

    Genomic insights into the evolution of industrial yeast species Brettanomyces bruxellensis

    FEMS Yeast Res.

    (2014)
  • Cited by (57)

    • Storage time and temperature affect microbial dynamics of yeasts and acetic acid bacteria in a kombucha beverage

      2022, International Journal of Food Microbiology
      Citation Excerpt :

      Indeed, different species have been isolated from beer, whose pH is similar to that of kombucha. It is interesting to note that the presence of D. anomala and D. bruxellensis in fermented drinks such as wine, cider and beer was considered negatively, as these two yeast species are able to produce volatile phenols affecting drink flavours (Agnolucci et al., 2017; Buron et al., 2011, 2012; Smith and Divol, 2016). However, in other fermented beverages, like lambic beer, D. anomala and D. bruxellensis participate in the spontaneous fermentation process and are supposed to positively affect the development of the unique sensorial characteristics, by producing acetic acid, thus increasing the flavour complexity of the beer (Steensels et al., 2015).

    • Spoilage yeasts in beer and beer products

      2022, Current Opinion in Food Science
    • Lactose utilization by Brettanomyces claussenii expands potential for valorization of dairy by-products to functional beverages through fermentation

      2021, Current Opinion in Food Science
      Citation Excerpt :

      The goal of this overview is to highlight the potential for B. claussenii in the functional beverage marketplace and aid in describing its application to lactose-containing waste streams in order to foster sustainability. Brettanomyces spp. have been isolated from a variety of sources, mainly alcoholic fermentations such as beer, wine or cider; but they have also been isolated from kombucha, soft drinks, and fruit juices, as well as from some dairy products such as fermented milk, yogurt, and cheese [4,12••,13••,14,15]. Isolation sources specific to B. claussenii can be seen in Table 1.

    View all citing articles on Scopus
    View full text