Whole-Genome Sequencing and Phenotyping Reveal Specific Adaptations of Lachancea thermotolerans to the Winemaking Environment.

Abstract

Adaptation to the environment plays an essential role in yeast evolution as a consequence of selective pressures. Lachancea thermotolerans, a yeast related to fermentation and one of the current trends in wine technology research, has undergone an anthropisation process, leading to a notable genomic and phenomic differentiation. Using whole-genome sequencing, of 145 L. thermotolerans strains, we identified six well-defined groups primarily delineated by their ecological origin and exhibiting high levels of genetic diversity. Anthropised strains showed lower genetic diversity due to the selective pressure imposed by the winemaking environment. Strong evidence of anthropisation and adaptation to the wine environment through modification of gene content was also found. Differences in genes involved in the assimilation of alternative carbon and nitrogen sources, such as the MAL31 and DAL5 genes, which confer greater fitness in the winemaking environment, were observed. Additionally, we found that phenotypic traits considered domestication hallmarks are present in anthropised strains. Among these, increased fitness in the presence of ethanol and sulphites, assimilation of non-fermentable carbon sources, and lower levels of residual fructose under fermentative conditions highlight. We hypothesise that lactic acid production in the Saccharomyces-Lachancea lineage is an anthropisation signature linked to winemaking, resulting from the loss of respiratory chain complex I and the evolutionary preference for fermentation over respiration, even in the presence of oxygen. Overall, the results of this work provide valuable insight into the anthropisation process in L. thermotolerans and demonstrate how fermentation environments give rise to similar adaptations in different yeast species.