Comparative genomic analysis of Saccharomyces cerevisiae yeasts isolated from fermentations of traditional beverages unveils different adaptive strategies

Abstract

Saccharomyces cerevisiae strains are the main responsible of most traditional alcohol fermentation processes performed around the world. The characteristics of the diverse traditional fermentations are very different according to their sugar composition, temperature, pH or nitrogen sources. During the adaptation of yeasts to these new environments provided by human activity, their different compositions likely imposed selective pressures that shaped the S. cerevisiae genome. In the present work we performed a comparative genomic hybridization analysis to explore the genome constitution of six S. cerevisiae strains isolated from different traditional fermentations (masato, mescal, cachaça, sake, wine, and sherry wine) and one natural strain. Our results indicate that gene copy numbers (GCN) are very variable among strains, and most of them were observed in subtelomeric and intrachromosomal gene families involved in metabolic functions related to cellular homeostasis, cell-to-cell interactions, and transport of solutes such as ions, sugars and metals. In many cases, these genes are not essential but they can play an important role in the adaptation to new environmental conditions. However, the most interesting result is the association observed between GCN changes in genes involved in the nitrogen metabolism and the availability of nitrogen sources in the different traditional fermentation processes. This is clearly illustrated by the differences in copy numbers not only in gene PUT1, the main player in the assimilation of proline as a nitrogen source, but also in CAR2, involved in arginine catabolism. Strains isolated from fermentations where proline is more abundant contain a higher number of PUT1 copies and are more efficient in assimilating this amino acid as a nitrogen source. A strain isolated from sugarcane juice fermentations, in which arginine is a rare amino acid, contains less copies of CAR2 and showed low efficiency in arginine assimilation. These results suggest that nitrogen metabolism has played an important role in the adaptive evolution of S. cerevisiae strains.

Keywords: GCN; Gene copy number; Gene families; Nitrogen metabolism; Saccharomyces cerevisiae; Traditional fermentations; aCGH; array Comparative Genome Hybridization; gene copy number.