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Maicas, S.; Mateo, J.J. Non-Saccharomyces Yeasts in Drinking Wine. Encyclopedia. Available online: https://encyclopedia.pub/entry/44208 (accessed on 27 July 2024).
Maicas S, Mateo JJ. Non-Saccharomyces Yeasts in Drinking Wine. Encyclopedia. Available at: https://encyclopedia.pub/entry/44208. Accessed July 27, 2024.
Maicas, Sergi, José Juan Mateo. "Non-Saccharomyces Yeasts in Drinking Wine" Encyclopedia, https://encyclopedia.pub/entry/44208 (accessed July 27, 2024).
Maicas, S., & Mateo, J.J. (2023, May 12). Non-Saccharomyces Yeasts in Drinking Wine. In Encyclopedia. https://encyclopedia.pub/entry/44208
Maicas, Sergi and José Juan Mateo. "Non-Saccharomyces Yeasts in Drinking Wine." Encyclopedia. Web. 12 May, 2023.
Non-Saccharomyces Yeasts in Drinking Wine
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This entry is adapted from the peer-reviewed paper 10.3390/microorganisms11051178
Non-Saccharomyces yeasts can also contribute to the sensory characteristics of wines. For example, some non-Saccharomyces yeasts can produce volatile compounds that contribute to fruity, floral or spicy aromas in wine. Others can produce enzymes that release aroma precursors, which can lead to the development of complex and desirable aromas during aging. Non-Saccharomyces yeasts can also contribute to the mouthfeel of wine by producing polysaccharides and glycerol, which can increase the viscosity and perceived body of the wine. In addition to wine production, non-Saccharomyces yeasts are used in the production of other fermented foods and beverages, such as beer, cider, mead, and kefir. In beer production, non-Saccharomyces yeasts can contribute to the flavor, aroma, and mouthfeel of the final product.
Saccharomyces non-Saccharomyces yeasts wine fermentations enzymes

1. Schizosaccharomyces pombe

Initially considered a spoilage yeast, Schizosaccharomyces has been successfully used industrially in the fermentation of sugar cane during rum making and palm and cocoa fermentation, and there are high hopes for its use in the wine industry [1]. Malolactic fermentation is often used to reduce the malic acid content in musts and wines, especially in the production of red wines, although it is sometimes a very complicated process due to the growth requirements of the bacteria used [1]. The use of Sc. pombe could become an invaluable new tool for grapes from wine-growing regions where malic acid is present in excessive concentrations, although few commercial strains are available due to their high rate of acetic acid production (about 1 g/L). Mixed and sequential cultures with Saccharomyces have been used to reduce the negative effects of Schizosaccharomyces spp. strains [2]. However, Sc. pombe has much greater potential than just its ability to reduce malic acid content and ferment sugar. Some researchers are using Sc. pombe to decrease gluconic acid [3]. Another application is aging on lees due to the greater autolytic release of polysaccharides than with Saccharomyces [4]. The ability of Sc. pombe to reduce 4-ethylphenol in wine due to its high adsorption capacity has also been studied [5]. Furthermore, urease activity is also of great interest in relation to food safety. Urea is the main precursor of ethyl carbamate, so reducing urea content could reduce ethyl carbamate, which is one of the main food safety problems in modern oenology [6]. Furthermore, the use of Schizosaccharomyces could limit the risk of biogenic amines [2], which are notorious for causing physiological problems in humans [7]. In addition, Schizosaccharomyces produces a large amount of pyruvic acid, and the significant hydroxycinnamate decarboxylase activity of Schizosaccharomyces favors the formation of vinylphenolic pyranoanthocyanins [2][8].

2. Pichia kluyveri

The various species of Pichia are fascinating non-Saccharomyces yeasts in oenology and are typically present in must fermentations, directly linked to wine [9]. The most frequently cited species in literature are P. fermentans [10][11], Pichia membranifaciens [12], Pichia occidentalis [13], Pichia terricola, Pichia manshurica, Pichia kudriavzevii, and Pichia kluyveri. The frequency of Pichia in grapes is lower than that of S. cerevisiae (28%) and other species such as Hanseniaspora uvarum (44%). The frequency varies from 0.12% for P. occidentalis to 4.7% for Pichia anomala. Other Pichia species commonly isolated from grapes are P. manshurica (2.81%), P. membranifaciens (0.98%), and P. kudriavzevii (0.85%) [14]. As a result, there are no adequate selection methods available, mainly because of these low frequencies that do not contribute to the development of commercial strains. However, P. kluyveri is perhaps the most researched species, for which commercial preparations are available. These species are known for their abilities to enhance the composition of aromatic compounds, providing thiols, terpenes, and fruity esters. When added to the fermentation process, they enhance rose petal and floral aromas, contributing to the overall bouquet of the wine, and the varietal and thiol aromas [15][16]. Marketers of wine suggest a sequential use of starter cultures, adding P. kluyveri first and after 48 h of fermentation, S. cerevisiae, which is better adapted to high ethanol concentrations and will complete the fermentation process. Biochemically, Pichia species ferment glucose but not other sugar molecules easily. Overall, the various Pichia species are gaining increasing interest in oenology [17][18][19].

3. Torulaspora delbrueckii

Torulaspora delbrueckii is one of the most commonly used non-Saccharomyces yeasts in oenology. It is recognized for its ability to improve the quality of wine and significantly reduce volatile acidity, particularly in musts with high sugar concentrations [20]. Winemakers consider this yeast to be a good option for optimizing certain wine parameters, as compared to those produced with S. cerevisiae. Specifically, T. delbrueckii is attributed with a lower acetic acid production capacity, lower ethanol concentration, higher amounts of glycerol, increased release of mannoproteins and polysaccharides, and greater potential for malolactic fermentation. In addition, this yeast has been observed to produce a higher number of desirable aroma compounds such as fruity esters lactones, thiols, and terpenes, while reducing the production of undesirable aroma compounds such as higher alcohols [21][22][23]. From an organoleptic perspective, T. delbrueckii contributes significantly to the reduction of esters and, at the same time, increases the concentration of minor esters and lactones, making it an important factor in the production of white wine [20]. In this way, the action of T. delbrueckii reduces the intensity of the fresh fruit aromas that are characteristic of young wines. At the same time, it increases the aromas of raisined fruit and sweetness, giving the wine aromatic characteristics associated with wines that have been produced over a longer period of time [24]. For this reason, some wine producers consider that T. delbrueckii is not a recommended yeast for making young white and rosé wines, as they are less aromatic and more evolved than those produced with Saccharomyces.
The effect attributable to T. delbrueckii varies depending on its degree of involvement in fermentation. When S. cerevisiae is involved, it is usually weak. To increase its effect, killer strains of T. delbrueckii are used, thus achieving a more reproducible effect of these yeasts on the final aroma of the wine [22]. It is known that T. delbrueckii has a lower fermentation potential and a lower growth rate than S. cerevisiae when used under normal fermentation conditions. When using killer strains, the environmental conditions are modified.
On the other hand, red wine production differs in certain aspects that may affect the growth of T. delbrueckii during fermentation and the quality of the wine. Frequent punching (oxygenation of the grape skins) allows for a higher availability of oxygen in the fermentation of red wines in comparison with white wines. This may benefit T. delbrueckii, since respiration is more relevant to its metabolism than that of S. cerevisiae, so the former grows worse than the latter under strictly anaerobic conditions [25].
However, the alcohol content is usually higher in red wines than in white wines. This negatively affects the ability of T. delbrueckii to dominate and complete fermentation, especially in the presence of S. cerevisiae, which is a yeast better adapted to high ethanol levels. Nevertheless, the initial amount of wild microorganisms is usually higher in red wine fermentation than in white wine fermentation. Red wine fermentation takes place in the presence of skins, which hold together more bacteria that carry out malolactic fermentation [26]. In addition, the presence of skins in the must provides additional nutrients, which can improve the fermentative capacity of T. delbrueckii and make it more competitive with S. cerevisiae [27].

4. Wickerhamomyces anomalus

The presence of W. anomalus during the fermentation process can have both positive and negative effects on the final wine product. On one hand, research has shown that this yeast contributes to the production of desirable aromas and flavors in wine, such as floral and fruity notes [28]. However, uncontrolled growth of W. anomalus can lead to spoilage and off-flavors in the wine [21][29][30]. To prevent the growth of spoilage yeasts such as W. anomalus, sulfites (e.g., sulfur dioxide) are commonly added to the wine by winemakers [31]. The addition of sulfites helps inhibit the growth of unwanted microorganisms, preserving the wine’s freshness and flavor. Nevertheless, some individuals are sensitive to sulfites, and high levels of sulfites in wine can trigger allergic reactions [32]. As a result, winemakers are exploring alternative approaches for preventing spoilage, such as using non-sulfite antimicrobial agents or implementing more frequent monitoring and testing during wine production [33].
Enzymes produced by W. anomalus, such as glycosidases, can contribute to the release of aromatic compounds in wine by hydrolyzing glycosidic bonds that are present in grape precursors [9]. These glycosidic bonds can mask the aromatic compounds, making them less volatile and therefore less perceptible to the human nose. By releasing these compounds, W. anomalus can have a significant impact on the aroma of wine. For example, β-D-glucosidase can hydrolyze glycosides of monoterpene alcohols, which are important contributors to floral and fruity aromas in wine [34]. Strains identified as W. anomalus or its former names have been reported to produce glycosidases such as β-D-glucosidase, α-L-arabinofuranosidase, α-L-rhamnosidase, and β-D-xylosidase, which are involved in the release of compounds aromatics from grape precursors [35]. The production of these enzymes by W. anomalus can therefore enhance the aroma profile of wine, potentially making it more complex and interesting. As such, strains of W. anomalus have been studied for their potential use in the oenological industry as a source of enzymes for improving wine aroma [36].

5. Metschnikowia pulcherrima

Metschnikowia pulcherrima is a non-Saccharomyces yeast present in various ecological niches, including the surface of grapes. Morphologically, its shape is ovoid to ellipsoidal with a size of 2.5 μm × 4−10 μm. The diploid cells of this species propagate vegetatively by budding. Under certain anaerobic conditions it can form pseudohyphae. It can form one to two lance-shaped (acicular/threadlike) spores. Its colonies are cream-colored and produce a reddish-brown soluble pigment called pulcherrimina, characteristic of this species, which gives color to the colonies and diffuses towards the medium. Strains of M. pulcherrima can be identified using selective and differential media: they show positive activity of the enzyme β-glucosidase, expression indicated by the use of arbutin as carbon source in agar plates; and proteolytic activity [37]. It grows well in media such as yeast extract peptone dextrose (YPD) or L-lysine. On the other hand, it shows very weak growth on nitrate agar [38]. Regarding the metabolism of M. pulcherrima, it is known that it can use glucose, sucrose, fructose, galactose, and maltose as carbon sources. However, it seems that with lactose it shows weak or non-existent growth. On the other hand, it can grow adequately at low temperatures of 15 to 20 ∘C and with a pH between 3 and 6 [38]. M. pulcherrima is one of the non-Saccharomyces yeast species capable of expressing more extracellular hydrolytic enzymes, highlighting the following: amylase, cellulase, glucanase, β-glucosidase, β-lyase, lipase, lichenase, pectinase, protease, sulfite reductase, and xylanase [39].
M. pulcherrima is considered a promising candidate for producing wine with low ethanol content. Previous studies have demonstrated that inoculating this yeast in combination with other yeasts, such as Saccharomyces uvarum, can result in wines with lower alcohol concentrations. However, M. pulcherrima has a lower fermentation power compared to other non-Saccharomyces yeasts [38]. Moreover, the reduction in alcohol production appears to be additive when used in combination with other yeasts, but competition and interactions with the autochthonous microbiota of grapes during fermentation can limit the expected results [40].

6. Hanseniaspora/Kloeckera spp.

Yeasts belonging to the genus Hanseniaspora are ascomycetes that are easily identified by their characteristic apiculate shape under the microscope, resulting from bipolar budding. This genus is part of the non-Saccharomyces yeasts, which are frequently isolated during the initial stages of fermentation. These yeasts can also be found on the surface of grapes, in soil, and in the winery environment, including harvesting machinery and fruit processing equipment [41][42]. Apiculate yeasts belonging to the genus Hanseniaspora are prevalent on grape surfaces. While H. uvarum is known for its abundant presence on grapes and its negative impact on wine quality due to high volatile acidity production, less is known about H. vineae, which is better adapted to fermentation. Studies have reported that H. vineae has enzymatic activity [42][43] and is capable of producing high levels of desirable aromatic compounds [44][45], enhancing the sensory properties of wines produced on an industrial scale. Additionally, proteolytic activity has been observed in Hanseniaspora isolates [46].

7. Lachancea thermotolerans

Lachancea thermotolerans, which was previously known as Kluyveromyces thermotolerans, is a yeast commonly found in various natural environments, including grapes. Its elliptical shape makes it indistinguishable from S. cerevisiae under light microscopy [47]. This yeast reproduces sexually with the formation of 1–4 ascospores and has been available as an active dry yeast since 2012, marketed by Christian Hansen (CHR-Hansen) to enhance the sensory characteristics of wines. A recent review [48] highlights its effects on acidity, aromatic profile, and polyalcohol production. L. thermotolerans has a moderate fermentation power (4–10% v/v) and is recommended for mixed or sequential use with other species such as S. cerevisiae or Sc. pombe, to allow for complete fermentation of the must’s sugars. One of the most noteworthy properties of this yeast is its ability to produce lactic acid, which can effectively enhance the acidity and pH of wines in a stable manner, as this acid remains unchanged during wine aging and stabilization. Additionally, the pH modification capability is crucial, with some strains able to exceed 0.5 pH units under real vinification conditions, particularly when used in sequential fermentations on crushed red grapes, in the presence of solid parts [48]. This is due to the fact that most of the acidification by L. thermotolerans occurs during the initial stages of fermentation, making it a strong competitor against other wine yeast species, and also because of its excellent tolerance to ethanol. In addition to its enzymatic activities, L. thermotolerans also produces a range of volatile compounds that contribute to the aroma of wines. These include esters, such as isoamyl acetate and ethyl lactate, as well as higher alcohols, such as isoamyl alcohol and 2-phenylethanol [49]. It has also been reported to produce sulfur compounds, such as thiol precursors, which can contribute to the tropical and citrus fruit notes in wine [48]. Overall, L. thermotolerans is considered a promising non-Saccharomyces yeast for improving the sensory properties of wines, especially in terms of acidity and aroma. Recent studies describe that it can favor the release of terpenes and volatile thiols [50]. Various works also show a positive effect of the use of L. thermotolerans on glycerol contents [22]. Glycerol is the second quantitatively most important fermentative metabolite after ethanol and has a certain effect on wine smoothness and structure [51].
Further studies have aimed to explore the biocompatibilities between L. thermotolerans and Hanseniaspora spp. in co-inoculation, using different types of nutrients and considering the effect on yeast assimilable nitrogen at low (16 °C) and medium temperatures SO2 (50 mg/L) for improving the sensory profile [52].The behavior of these yeasts was evaluated, and significant results were obtained on the population count, with higher populations of Hanseniaspora spp. with respect to L. thermotolerans. Not surprisingly, fermentations with L. thermotolerans/H. vineae, showed inhibition of acidification, generating up to 0.41 g/L of lactic acid. On the contrary, a synergistic effect was observed when L. thermotolerans/H. opuntiae was used, achieving 2.44 g/L of lactic acid and a pH reduction of up to 0.16 [52].

8. Candida stellata

Non-Saccharomyces yeasts, such as Candida spp., are becoming increasingly important in the industry due to their unique fermentative behavior. Candida species have been identified as potential candidates for the fermentation of wine and beer [53]. In particular, C. stellata is frequently isolated from grape must and can survive throughout spontaneous wine fermentation for extended periods of time [54]. Studies on the fermentative activity of C. stellata have shown that it can have a positive impact on the taste and flavor of alcoholic beverages [55]. In addition to its ability to positively affect the taste and flavor of alcoholic beverages, C. stellata also exhibits unique metabolic characteristics. It is known to have a strong preference for fructose and high osmotic pressure environments. Under anaerobic conditions or limited oxygen supply, it undergoes alcoholic fermentation, but under completely aerobic conditions, a mixed respiro-fermentative metabolism is observed. This metabolic behavior is influenced by the concentration of oxygen and glucose in the fermentation medium. When conditions are conducive to sugar fermentation, major fermentative compounds such as ethanol, acetic acid, and glycerol are produced, along with small amounts of higher alcohols, esters, volatile fatty acids and carbonyl compounds. Despite these metabolic losses, the complete fermentation of hexose by yeast can still produce 94–96% of the theoretical yield of ethanol [56][57][58][59].

9. Limitations in the Research Field and Future Perspectives

While the use of non-Saccharomyces yeasts in winemaking shows great potential, there are still some limitations in the research field that need to be addressed. One of the biggest limitations is the lack of understanding of how non-Saccharomyces yeasts interact with S. cerevisiae during co-fermentation. While it is known that non-Saccharomyces yeasts can contribute to wine flavor and aroma complexity, more research is needed to determine the specific mechanisms involved in this process [60][61]. Another limitation is the lack of commercial availability of non-Saccharomyces yeasts. While some non-Saccharomyces yeasts are available commercially, there is still a limited selection compared to the vast diversity of non-Saccharomyces yeasts present in nature. This limitation has led to a lack of standardization in the use of non-Saccharomyces yeasts in winemaking, making it difficult to compare the effects of different yeasts on wine quality [62][63].
Despite the limitations in the research field, the use of non-Saccharomyces yeasts in winemaking shows great potential for the future. With advances in molecular biology and genetic engineering, it may be possible to develop new non-Saccharomyces yeasts with specific traits that are desirable for winemaking. For example, it may be possible to develop non-Saccharomyces yeasts that are better able to survive in the harsh conditions of winemaking, or that are better able to compete with S. cerevisiae during co-fermentation. The use of these new yeasts will be conditioned to legal aspects in some countries [64][65].
Another potential avenue for research is the use of mixed cultures of non-Saccharomyces yeasts. While much of the current research focuses on the use of non-Saccharomyces yeasts in combination with S. cerevisiae, it may be possible to develop mixed preparations [25][66].

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Subjects: Microbiology
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Sergi Maicas
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José Juan Mateo
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Update Date: 15 May 2023
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