Over the last decade, several non-Saccharomyces species have been used as an alternative yeast for producing wines with sensorial properties that are distinctive in comparison to those produced using only Saccharomyces cerevisiae as the classical inoculum. Among the non-Saccharomyces wine yeasts, Metschnikowia is one of the most investigated genera due to its widespread occurrence and its impact in winemaking, and it has been found in grapevine phyllospheres, fruit flies, grapes, and wine fermentations as being part of the resident microbiota of wineries and wine-making equipment. The versatility that allows some Metschnikowia species to be used for winemaking relies on an ability to grow in combination with other yeast species, such as S. cerevisiae, during the first stages of wine fermentation, thereby modulating the synthesis of secondary metabolites during fermentation in order to improve the sensory profile of the wine. Metschnikowia exerts a moderate fermentation power, some interesting enzymatic activities involving aromatic and color precursors, and potential antimicrobial activity against spoilage yeasts and fungi, resulting in this yeast being considered an interesting tool for use in the improvement of wine quality. The abovementioned properties have mostly been determined from studies on Metschnikowia pulcherrima wine strains. However, M. fructicola and M. viticola have also recently been studied for winemaking purposes.

The adaptation to the different biotic and abiotic factors of wine fermentation has led to the accumulation of numerous genomic hallmarks in Saccharomyces cerevisiae wine strains. IRC7, a gene encoding a cysteine-S-β-lyase enzyme related volatile thiols production in wines, has two alleles: a full-length allele (IRC7 F ) and a mutated one (IRC7 S ), harbouring a 38 bp-deletion. Interestingly, IRC7 S -encoding a less active enzymeappears widespread amongst wine populations. Studying the global distribution of the IRC7 S allele in different yeast lineages, we confirmed its high prevalence in the Wine clade and demonstrated a minority presence in other domesticated clades (Wine-PDM, Beer and Bread) while it is completely missing in wild clades. Here, we show that IRC7 S -homozygous (HS) strains exhibited both fitness and competitive advantages compared with IRC7 F -homozygous (HF) strains. There are some pieces of evidence of the direct contribution of the IRC7 S allele to the outstanding behaviour of HS strains (i.e., improved response to oxidative stress conditions and higher tolerance to high copper levels); however, we also identified a set of sequence variants with significant co-occurrence patterns with the IRC7 S allele, which can be co-contributing to the fitness and competitive advantages of HS strains in wine fermentations.

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SummaryBiotic and abiotic factors of wine fermentations have led to the accumulation of numerous genomic hallmarks of domestication in Saccharomyces cerevisiae wine strains. Here we have studied the paradoxical distribution of a dominant allele of IRC7 in wine yeast strains. This gene encodes a cysteine-S-β-lyase and presents two alleles: a wild full-length allele (IRC7F) and a mutated one (IRC7S), harboring a 38bp-deletion. Interestingly, IRC7S-coding for a less active enzyme-appears in the great majority of wine strains. Studying its global distribution among phylogenetic clades, we observed that IRC7S allele is dominant just in wine strains, having a moderate presence in other domesticated clades (Beer, Bread and Wine-PDM), but being completely absent in wild clades, appearing as a new hallmark of domestication. To explain this paradoxical distribution, we performed an IRC7-rooted phenotypic-wide survey, demonstrating that IRC7S-homozygous (HS) wine strains have both fitness (lower lag phases and higher growth rates) and competitive (killer toxin resistance, pseudohyphal growth) advantages. Hence, we performed a genome-wide survey across domesticated clades, finding a set of mutations that are conserved among wine strains and potentially associated to IRC7S allele, which can help to explain the outstanding phenotype of HS strains and their dominant distribution in wines.Originality-Significance StatementS. cerevisiae is one of the best studied microbes due to its industrial importance and its use as a eukaryotic model organism. S. cerevisiae is also an interesting model for studying the effects of domestication in yeast genomic, phenotype and ecology. The study of how wild S. cerevisiae strains evolved into a greatly adapted domesticated strains and changed its lifestyle drastically is still of great interest. In the case of wine populations, strains have accumulated numerous hallmarks of domestication in their genome, related with their great phenotypic adaptation to this environment. Here, we report a new hallmark of domestication in wine strains; the IRC7 deleted allele (IRC7S) and present the first insights about its unexpected global distribution among phylogenetic clades, understanding the genomic context and the phenotypic implications of this allele in wine strains.