Transcriptional rewiring, adaptation, and the role of gene duplication in the metabolism of ethanol of Saccharomyces cerevisiae

Ethanol is the main by-product of yeast sugar fermentation that affects microbial growth parameters, being considered a dual molecule, a nutrient and a stressor. Previous works demonstrated that the budding yeast arose after an ancient hybridization process resulted in a tier of duplicated genes within its genome, many of them with implications in this ethanol “produce-accumulate-consume” strategy. The evolutionary link between ethanol production, consumption, and tolerance versus ploidy and stability of the hybrids is an ongoing debatable issue. The implication of ancestral duplicates in this metabolic rewiring, and how these duplicates differ transcriptionally, remains unsolved. Here, we study the transcriptomic adaptive signatures to ethanol as a nonfermentative carbon source to sustain clonal yeast growth by experimental evolution, emphasizing the role of duplicated genes in the adaptive process. As expected, ethanol was able to sustain growth but at a lower rate than glucose. Our results demonstrate that in asexual populations a complete transcriptomic rewiring was produced, strikingly by downregulation of duplicated genes, mainly whole-genome duplicates, whereas small-scale duplicates exhibited significant transcriptional divergence between copies. Overall, this study contributes to the understanding of evolution after gene duplication, linking transcriptional divergence with duplicates’ fate in a multigene trait as ethanol tolerance.

This work was supported by grants BFU2015-66073-P from the Spanish Ministry of Economy and Competitiveness (MINECO-FEDER) to M.A.F. and SEJI/2018/046 from the Generalitat Valenciana, Programa a la excelencia cientifica de investigadores juniors, to C.T. F.M. was supported by an FPI grant from the Spanish Ministry of Economy and Competitiveness (BES-2016-076677).

Peer reviewed