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 the fermentative process and one of the current trends in wine technology research, has undergone an anthropization process that has led to a strong differentiation both from a genomic and phenomic perspective. Using whole-genome sequencing, we have investigated the genomic diversity of 145 L. thermotolerans strains, identifying six well-defined groups primarily delineated by their ecological origin and exhibiting high levels of genetic diversity. Anthropized strains showed lower genetic diversity due to the purifying selection imposed by the winemaking environment. Strong evidence of anthropization 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 MAL1 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 anthropized strains. Among these, increased fitness in the presence of ethanol and sulphites, assimilation of non-fermentable carbon sources such as glycerol, and lower levels of residual fructose under fermentative conditions highlight. We hypothesize that lactic acid production by wine-related strains is an anthropization signature consequence of the adaption of early Crabtree-positive yeasts to the fermentative environment. Overall, the results of this work provide valuable insight into the anthropization process in L. thermotolerans and demonstrate how fermentation environments give rise to similar adaptations in different yeast species.