The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae

Int J Mol Sci. 2021 Nov 14;22(22):12293. doi: 10.3390/ijms222212293.

Abstract

The cell central metabolism has been shaped throughout evolutionary times when facing challenges from the availability of resources. In the budding yeast, Saccharomyces cerevisiae, a set of duplicated genes originating from an ancestral whole-genome and several coetaneous small-scale duplication events drive energy transfer through glucose metabolism as the main carbon source either by fermentation or respiration. These duplicates (~a third of the genome) have been dated back to approximately 100 MY, allowing for enough evolutionary time to diverge in both sequence and function. Gene duplication has been proposed as a molecular mechanism of biological innovation, maintaining balance between mutational robustness and evolvability of the system. However, some questions concerning the molecular mechanisms behind duplicated genes transcriptional plasticity and functional divergence remain unresolved. In this work we challenged S. cerevisiae to the use of lactic acid/lactate as the sole carbon source and performed a small adaptive laboratory evolution to this non-fermentative carbon source, determining phenotypic and transcriptomic changes. We observed growth adaptation to acidic stress, by reduction of growth rate and increase in biomass production, while the transcriptomic response was mainly driven by repression of the whole-genome duplicates, those implied in glycolysis and overexpression of ROS response. The contribution of several duplicated pairs to this carbon source switch and acidic stress is also discussed.

Keywords: acidic stress; heat-shock proteins; metabolic distance; phenotypic response; reactive oxygen response; small-scale duplicates; whole-genome duplicates.

MeSH terms

  • Adaptation, Physiological / genetics*
  • Carbon / metabolism*
  • Evolution, Molecular
  • Gene Duplication*
  • Gene Expression Profiling / methods
  • Gene Expression Regulation, Developmental
  • Gene Expression Regulation, Fungal
  • Gene Ontology
  • Genome, Fungal / genetics
  • Glycolysis / genetics
  • Lactic Acid / metabolism*
  • RNA-Seq / methods
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / growth & development
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / genetics*
  • Saccharomyces cerevisiae Proteins / metabolism

Substances

  • Saccharomyces cerevisiae Proteins
  • Lactic Acid
  • Carbon