Genetic background shapes the transcriptional activity and phenotypic contribution of a horizontally acquired region in yeast

Horizontal gene transfer is the movement of genetic material across species. In Saccharomyces cerevisiae, a DNA segment known as Region B was acquired horizontally from a distant yeast species. This region (∼17 Kb) encodes five genes and is present in the genomes of yeast strains from different phylogenetic clades. Interestingly, the presence of Region B is not restricted to yeast strains isolated from fermentative environments, leaving its contribution to yeast niche-specific adaptation unclear. In this work, the genomic structure of Region B was analyzed in yeast strains from the ScRAP (S. cerevisiae Reference Assembly Panel) collection, identifying ten structural variants that maintain a circular continuity. To assess the role of Region B in yeast adaptation, we performed a high-throughput phenotyping of the ScRAP collection under different growth conditions, identifying that Region B is associated with higher tolerance to oxidative stress. Then, we characterized the transcriptional activity of each gene within Region B using a fluorescent reporter. The results revealed that gene expression depends on the host's genetic background and transcription factors encoded within Region B. To identify the genetic determinants involved in Region B expression within different genetic backgrounds, three expression quantitative trait loci were mapped and validated. Finally, by performing the deletion of Region B in two different strains, we determined a background-dependent contribution of this region to various fermentative phenotypes. Altogether, our results suggest a complex regulatory interaction between the horizontally acquired genes and the host genome that contributes to yeast adaptation under fermentation conditions.