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QS in wine fermentation is a cell to cell communication between wine microbial consortiums, which is a mechanism of creation, synthesis, and detection of QSMs, and the concentration depends on the presence of related microorganisms in the wine[52]. This mechanism mediates the beginning of competence and the synthesis of secondary metabolites like ammonia, bicarbonate, farnesol, acetaldehyde, tryptophol, and phenylethanol which are the significant yeast QSMs[53]. In the yeast QS process, alcohols, small peptides, volatile compounds, lipids, and small molecules act as messengers in intraspecies communication, and aromatic alcohols are the only acting bodies of QSMs[54]. QS systems were first observed in a dimorphic fungus called C. albicans, and it regulated the transition of filamentous growth from yeast cells. Farnesol is one of the QSMs secreted during the development of C. albicans cultures. When the culture reaches a specific density, accumulated farnesol prevents the development of germ tubes[55]. Tyrosol is another QSM in C. albicans that induces cell growth and germ tube formations even in low density[56]. The QS system of C. albicans is different from S. cerevisiae. Anyhow, according to previous studies, S. cerevisiae plays a major role in the secretion of QSMs, affecting the aromatic profile of the wine. Especially, it converts phenylalanine and tryptophan into aromatic alcohols like 2-phenyl-ethanol and tryptophol, respectively, through the Ehrlich pathway[57]. These molecules could act as QSMs; hence they induce the phase shifting into the stationary phase. At the same time, they promote pseudohypha generation and rapid growth of cells. Like this QS controls wine's microbial population and organoleptic properties during winemaking concerning regions and available microbial consortium. There is no evidence available for the function of QSMs like tyrosol, tryptophol, or 2-phenylethanol by S. cerevisiae during AF. QSMs are synthesized when the phase change from exponential to stationary in the alcoholic fermentation process[58]. For instance, the mini fermentation results of Zupan et al.[58], further revealed that tyrosol, tryptophol, or 2-phenylethanol production of S. cerevisiae is high in the exponential phase of the fermentation and rapidly declined just before the stationary phase of alcoholic fermentation. Furthermore, the whole-genome microarray analysis results of Chen & Fink[59] showed tryptophol and 2-phenylethanol regulate the transcription of a set of genes that manipulate the entrance to the stationary phase. Furthermore, tryptophol stimulates the production of aromatic alcohol. Yeast like S. cerevisiae exhibits higher fermentative capacity and higher ethanol tolerance under the availability of quorum sensing molecule tyrosol. Furthermore, aromatic alcohols derived from amino acids mediate QS-type yeast regulations[60]. All these results showed that QS molecules control the correct entrance of S. cerevisiae cells to the stationary phase. Other than, S. cerevisiae some non-Saccharomyces species, H. uvarum, T. pretoriensis, and Z. bailii were able to produce phenylethanol, tryptophol, and tyrosol like quorum sensing molecules[58]. It has been postulated by a recent study that S. cerevisiae, Candida zemplinina, Hanseniaspora uvarum, Torulaspora pretoriensis, Zygosaccharomyces bailii, and Dekkera bruxellensis expressed species-specific mechanisms for the synthesis of tyrosol, 2-phenylethanol, and tryptophol (Fig. 2). At the same time, no QSMs were observed after one day of wine fermentation of C. zemplinina and D. bruxellensis[58]. Further, this research revealed that Zygosaccharomyces bailii were able to produce tryptophol at a similar rate to S. cerevisiae, which could be because both belong to the same family Saccharomycetaceae. Further, the results revealed, secondly, the highest phenylethanol and tyrosol production capability after S. cerevisiae was shown by this yeast species. The aromatic alcohol 2-phenylethanol has a significant impact on the aroma profile of a wine. On the other hand, Hanseniaspora uvarum has different QS kinetics, showing the early tyrosol synthesis initiation and the late start of tryptophol synthesis compared to H. uvarum. Furthermore, it showed a meager rate of production of phenylethanol without any peaks in the kinetics curve. All in all, these analyses revealed the heterogeneity of QSMs and their kinetics in all tested species. Therefore, further studies on the kinetics of QSMs and mechanisms may open new avenues in wine fermentation, facilitating the better quality of the wine[58]. Therefore, the combination of wine microbial consortium through various indigenous microorganisms for wine fermentation leads to the development of specific organoleptic qualities of the final wine product. In Gram-positive bacteria, QS-mediated signaling is coordinated by small peptides due to the intracellular mechanism detected by a sensory protein called histidine-kinase[61]. Lactones, terpenes, alcohols, and peptides are the prominent families of QSMs[62]. No scientific proofs are available on how S. cerevisae communicates signals, and it was stated that S. cerevisiae synthesized and released QSMs at a specific microbial density like C. albicans[55]. Tryptophols and 2-phenylethanol are present in C. albicans, but they do not express any density-dependent responses. Debaryomyces hansenii also secreted QSMs like tyrosols, 2-phenylethanol, and tryptophols to communicate with the other microorganisms in the environment.
Figure 2.
Synthesis of QSMs of different wine yeast species in MS300 medium at 22 °C for 29 h in 2 mL microcentrifuge tubes (mini fermentation)[58].
Further, the study of Nissen et al.[43] revealed that, when S. cerevisiae and non-Saccharomyces are in a co-culture, yeast-yeast interactions are mediated by QSMs to reduce the early growth of non-Saccharomyces. Furthermore, this research revealed that it might be due to the cell to cell contact process of yeast in mixed cultures, and it demonstrated that the cell to cell contact process is not a single mechanism responsible for the early growth arrest non-Saccharomyces. Several other factors and mechanisms also involve the inhibition of growth of non-Saccharomyces in early fermentation. Acetaldehyde is a major QSM that mediates the cell to cell signaling process and regulates biomass synthesis, fermentation kinetics, and by-product formation[63]. Flocculation is a significant cell-to-cell associative mechanism in which colloidal cells come out of the medium to accumulate in a flake form. The effective yeast flocculation regulates the formation of compacted sediments and initiates the clarification mechanism in post AF[64]. An individual cell does not carry out the flocculation process[65]. A flocculent of K. apiculata communicates with a non-flocculent S. cerevisiae strain in mixed fermentation and facilitates co-flocculation in both strains. It has been revealed that S. cerevisiae, Dekkera spp., and K. apiculata are involved in co-flocculation with various bacterial strains[66]. A lectin-carbohydrate binding system regulates these types of co-flocculation mechanisms[65,66]. Due to this mechanism, the indigenous non-Saccharomyces species involved in early AF of spontaneous fermentation are controlled by S. cerevisiae, and as a result, regional wine varieties obtained different organoleptic qualities[65,66]. However, there have been no records for the QS mechanism and cell to cell contact of bacterial cells in the wine medium, and many kinds of research need to be carried out to clear this area. Hence different wine microbes have different QS systems, and this opens an avenue to conduct much research to identify some yeast genera specific QS systems. Further different region-specific grape microbiome also shows diversity in their QS systems. As a result of QS variations, they generate different metabolites in different stages of alcohol fermentation. This may lead to the region-specific organoleptic property development of the final wine product. Therefore, this is a highly blind area to be investigated through many kinds of research.
The quorum sensing capability of wine microbial consortium varies from region to region. Geographical features and climatic conditions of vineyards and wineries determine the grape microbial consortium, quorum sensing, and, eventually, the quality of the wine. Specifically, climatic features, training systems, soil types, and cultural behaviors interact, which determines the terroir and growth of different grape varieties[67]. Five regions of the world are considered the top five wine regions; hence more than 80% of wine exports took place from these regions. France, Italy, the United States of America, Australia, and Chile are the top five wine regions globally. Several well-known wine varieties from specific regions of these countries use selective grape varieties (Table 1)[11]. Other than these countries, Spain, Germany, Argentina, Portugal, South Africa, and New Zealand are also significant wine producers globally. Likewise, according to the information from the Fruit Crops Research and Development Centre, Department of Agriculture (Horana, Sri Lanka); Israel blue, Cardinal, Black muscat, Muscat MI, and French MI are the major grape varieties cultivated in Sri Lanka. Among these Muscat MI (red wine) and French MI (white wine) are used for winemaking, while others are used as table varieties. In Sri Lanka, better grape harvest can be obtained from well drained, deep soils in the dry zone under irrigation. In Sri Lanka, farmers use the pandol system, Geneva double curtain system (GDC), and other fence systems as training systems. Jaffna and Dambulla are some of the significant grape-cultivating regions in Sri Lanka. Similarly, worldwide, the climatic conditions, fertility of soil, geology, pH, and training systems determine the growth of specific types of grape varieties and the microbial consortium of grapes[67]. Not only grapes, other fruits like apples, pears, berries, peaches, kiwis, bananas, pineapples, lemons, limes, passion fruits, and oranges are also used to make wine where we can analyse QS with both spontaneous and inoculated fermentation[68]. Eventually, this microbial consortium affects wine fermentation, secretion of quorum sensing molecules, and quality of the wine. This is how the quality of wine varies from region to region.
Table 1. Significant regional grape varieties and their respective wine types all over the world[11].
Region Well known wine type Grape variety France Haut-Médoc Château Cantemerle, AC Cabernet Sauvignon blended with
Cabernet Franc and MerlotChÍteau Lafite – Rothschild, Latour Mouton-Rothschild Upper Loire Sancerre Rouge, AC Pinot Noir Bordeaux fringe country Bergerac, AC Merlot, Cabernet Càte de Beaune Aloxe-Corton, AC Pinot Noir Italy Tuscany Brunello di Montalcino, DOCG Sangiovese Vernaccia Di San Gimignano Vernaccia Veneto Soave, DOC Garganega Breganze, DOC Rondinella and Molinara United States of America California Mondavi Chardonnay(white), Cabernet Sauvignon Merlot Berringer SonomaCutrer Cabernet Sauvignon/Chardonnay Oregon Adelsheim Pinot Noir Australia Victoria Lindemans Chardonnay ChÍteau Tahbilk Cabernet, Shiraz South Australia Adams Chardonnay (white) Henschke Sauvignon (red) Wynns Cabernet Chile Central valley Santa Rita Cabernet Sauvignon Concha y Toro Merlot (red) Terra Noble Carmenieres Several research teams have showcased the finding of artificial communication within and between species by employing synthetic circuits that incorporate elements of quorum sensing systems. Engineered quorum sensing (QS)-based circuits find diverse applications, including the synthesis of biochemicals, tissue culture engineering, and the facilitation of co-culture fermentations. Moreover, they play a crucial role in the development of microbial biosensors for discerning and monitoring microbial species within the environment and microorganisms[52]. The biofilm formation, acid stress tolerance, bacteriocin production, competence, adhesion, morphological switches, and oriented growth are some of the traits directed by QS in foodborne microorganisms. Moreover, QS has been identified in fermented food producing microorganisms. So, it can be applied to small-scale processing of fermented foods like dairy products, sourdough, fermented vegetables, and wine[69].
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These data were derived from the following resources in the reference section and were analyzed during this study.
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Cite this article
Thivijan S, Undugoda LJS, Nugara RN, Manage PM, Thambulugala KM, et al. 2023. Quorum sensing capability of wine microbial consortium involved in spontaneous fermentation of regional wine production. Studies in Fungi 8:20 doi: 10.48130/SIF-2023-0020
Quorum sensing capability of wine microbial consortium involved in spontaneous fermentation of regional wine production
- Received: 26 July 2023
- Accepted: 29 November 2023
- Published online: 21 December 2023
Abstract: Quorum sensing (QS) is an intercellular communication process in which wine microbial consortium collectively adapts their metabolism by secreting quorum sensing molecules (QSM) into their environment. These QSMs continuously diffuse into the medium until approaching the threshold level, which stimulates the microbial cell population. Moreover, these molecules bind with their target sensory proteins and stimulate the transcription and translation of genes responsible for aromatic alcohol production. The research findings revealed that ARO genes regulate the synthesis of quorum sensing molecules like tyrosol, 2-phenylethanol, and tryptophol. For instance, ARO8, ARO9, and ARO10 present in Saccharomyces cerevisiae are the significant genes regulating the above QSMs and other aromatic alcohols, which determine the organoleptic qualities of wine. Another essential gene that affects the quality of wine is FLO11. Hence, different grape cultivars harbor different types of wine fermenting microbes with unique quorum sensing systems, leading to the unique organoleptic qualities in regional wine. Since we could still find the quorum sensing system of S. cerevisiae, this may open avenues to conduct much research to discover the unique quorum sensing systems of different wine microbes. These findings will lead to novel wine starter cultures with many specific genes developed through recombinant DNA technology. Therefore, this review focuses on quorum sensing of wine microbial consortium involved in the fermentation process of spontaneous wine fermentation through the chemistry of QSMs and how these signaling processes are genetically manipulated. Furthermore, this focus reviews the organoleptic quality development of regional wine products due to different quorum sensing abilities.
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Key words:
- Wine /
- Yeast /
- Fermentation /
- Recombinant DNA technology /
- Microbial consortium /
- Quorum sensing