Dominance of wine Saccharomyces cerevisiae strains over S. kudriavzevii in industrial fermentation competitions is related to an acceleration of nutrient uptake and utilization

Abstract

Summary Grape must is a sugar‐rich habitat for a complex microbiota which is replaced by Saccharomyces cerevisiae strains during the first fermentation stages. Interest on yeast competitive interactions has recently been propelled due to the use of alternative yeasts in the wine industry to respond to new market demands. The main issue resides in the persistence of these yeasts due to the specific competitive activity of S. cerevisiae. To gather deeper knowledge of the molecular mechanisms involved, we performed a comparative transcriptomic analysis during fermentation carried out by a wine S. cerevisiae strain and a strain representative of the cryophilic S. kudriavzevii, which exhibits high genetic and physiological similarities to S. cerevisiae, but also differences of biotechnological interest. In this study, we report that transcriptomic response to the presence of a competitor is stronger in S. cerevisiae than in S. kudriavzevii. Our results demonstrate that a wine S. cerevisiae industrial strain accelerates nutrient uptake and utilization to outcompete the co‐inoculated yeast, and that this process requires cell‐to‐cell contact to occur. Finally, we propose that this competitive phenotype evolved recently, during the adaptation of S. cerevisiae to man‐manipulated fermentative environments, since a non‐wine S. cerevisiae strain, isolated from a North American oak, showed a remarkable low response to competition.

Nitrogen Preferences during Alcoholic Fermentation of Different Non-Saccharomyces Yeasts of Oenological Interest

“…Later, some studies have revealed that non-Saccharomyces yeasts have specific profiles for amino acid consumption, concluding that the different nitrogen composition of the media strongly influences the assimilation order of each compound, both in natural [19] and synthetic must [12,35,37]. Different studies have analyzed the possible competition for nutrients between Saccharomyces and non-Saccharomyces yeasts [11,12,[40][41][42]. Rollero et al [12] observed different consumption profiles of S. cerevisiae depending on the non-Saccharomyces yeasts used in the sequential culture, suggesting that this behavior could be explained by the competition for nutrients.…”

“…Moreover, recent studies have demonstrated that under conditions of co-cultivation with some non-Saccharomyces species, S. cerevisiae partially relieves the nitrogen and glucose catabolite repression, in order to increase the flux of nutrients and reduce their availability for other yeast species [12,40]. Indeed, the presence of other Saccharomyces species, such as Saccharomyces kudriavzevii, can also produce metabolic stimulation in S. cerevisiae [41].…”

Proteomic characterization of extracellular vesicles produced by several wine yeast species

“…Considering the short response time, transcriptional reprogramming was likely mediated by specific recognition mechanisms. Recently, similar results have been reported by other authors (Shekhawat et al ., 2019; Alonso del Real et al ., 2019).…”

Transcriptomics provides a genetic signature of vineyard site with insight into vintage-independent regional wine characteristics

“…Microbial biogeography of wine has been documented in globally distributed appellations (4,7,8,(14)(15)(16)(17)(18)(19)(20)(21), and has been correlated with wine fermentation outcomes (15,22). In inoculated co-cultures, non-Saccharomyces microorganisms both contribute to fermentation and change the behavior of the dominant fermenter S. cerevisiae, leading to measurable differences in wine aroma and composition (36)(37)(38). Here, we show that grape must ribosomal DNA profiles do not correlate with detected eukaryotic gene expression patterns during primary fermentation.…”

“…How these altered fermentation outcomes occur remains a difficult question to address, as a given outcome may be the direct result of metabolism by the non-Saccharomyces organism, or the result of the organism altering S. cerevisiae metabolism via direct or indirect interactions (35)(36)(37). In support of the latter, the presence of non-Saccharomyces organisms has been shown to increase the rate and diversity of resource uptake by S. cerevisiae in early fermentation (36)(37)(38). In controlled steady-state bioreactor fermentations, the presence of Lachancea thermotolerans was found to increase the expression of S. cerevisiae genes important for iron and copper acquisition (39).…”