Subpopulation-specific gene expression in Lachancea thermotolerans uncovers distinct metabolic adaptations to wine fermentation

Gene expression is the first step in translating genetic information into quantifiable traits. This study analysed gene expression in 23 strains across six subpopulations of Lachancea thermotolerans, shaped by anthropization, under winemaking conditions to understand the impact of adaptation on transcriptomic profiles and fermentative performance, particularly regarding lactic acid production. Understanding the gene expression differences linked to lactic acid production could allow a more rational address of biological acidification while optimizing yeast-specific nutritional requirements during fermentation. By sequencing mRNA during exponential growth and fermentation in synthetic grape must, we identified unique expression patterns linked to the strains originated from wine-related environments. Global expression analysis revealed that anthropized subpopulations, particularly Europe/Domestic-2 and Europe-Mix, exhibited distinct gene expression profiles related to fermentation processes such as glycolysis and pyruvate metabolism. These processes were differentially expressed, along with other important biological processes during fermentation, such as nitrogen and fatty acid metabolism. This study highlights that anthropization has driven metabolic specialization in L. thermotolerans, enhancing traits like lactic acid production, which is a trait of interest in modern winemaking. Correlation analysis further linked lactic acid dehydrogenase genes with key metabolic pathways, indicating adaptive gene expression regulation. Additionally, differences in other metabolites of oenological interest as glycerol or aroma compounds production are highlighted. Here, we provide insights into the evolutionary processes shaping the transcriptomic diversity of L. thermotolerans, emphasizing the impact of winemaking environments on driving specific metabolic adaptations, including lactic acid production.