Interspecific hybridization and aneuploidy as adaptive mechanisms in Saccharomyces yeasts

With the explosion of genome sequencing technologies, mechanisms such as aneuploidy, polyploidy, and hybridization are emerging as being more frequent and relevant in genomes evolution than what was considered earlier. An interesting model to study such mechanisms are Saccharomyces yeasts as much data is available on its genome structure and evolution and they are easily manipulated in laboratory. Yeast from this genus have small and compact genomes that make them an interesting model for genomics studies on eukaryotic organisms. Moreover, hybrids between the different species of the genus are known and relevant for industrial processes. In this doctoral thesis, we aimed to investigate different aspects of the adaptive value of aneuploidy and interspecific hybridization in Saccharomyces. In the first chapter, we were interested in studying what genomic differences were underlying the different ethanol tolerance observed in S. cerevisiae strains. The most interesting genomic change we observed was a shared polysomy of chromosome III in the highest ethanol tolerant strains. We could determine that this correlation between ethanol tolerance and chromosome III copy number also appeared in different background and we confirmed it was an adaptive mechanism on ethanol stress. In the second chapter of this work, we asked how S. cerevisiae x S. kudriavzevii hybrids mate and how this mechanism would influence the genomic and adaptability outcome of these hybrids. We found that rare-mating was the most frequent but not the only mechanism use. As most of the hybrid were triploid and had a diploid heterozygous contribution of S. cerevisiae, this mating mechanism was the most probable. However, two hybrids were tetraploid. One had an extreme reduction of the S. kudriavzevii subgenome and heterozygous S. cerevisiae. This structure seemed more compatible with the outcome of artificial crossing in strain improvement programs. The last strain had a diploid homozygous contribution of each subgenome what indicates a spore to spore mating followed by whole-genome duplication. An interesting point of the ploidy outcome is that it influenced the phenotype of the strain and its evolvability. In chapter 3, we studied in detail the genome of the hybrid VIN7 and showed that its genome was unstable. The instability influenced the stress resistance of the strain suggesting that genomic instability, probably triggered by hybridization, is an important factor of phenotypic variability, and therefore to adaptability. We aimed to investigate the factors that influenced polysomy frequency for each chromosome and found that the least interacting chromosomes and the smallest were the most frequent polysomic ones. The fourth chapter of this work deals with short-term evolution of artificial hybrids between S. cerevisiae and S. kudriavzevii. We wanted to know how the genome content changed in conditions in which the species that form the hybrid had different phenotypes: ethanol, were S. cerevisiae is better fit, and cold temperature, where the best species is S. kudriavzevii. We showed that recombination between subgenome was less frequent than between the two copies of the S. cerevisiae subgenome. This suggests that the distance between the genome sequence influences the recombination rate in hybrid cells. We found that ploidy was strongly influencing transcription and the evolution mechanisms available for the hybrids. The hybrids evolved at cold temperature showed an aneuploidy on chromosome XII. At the transcriptomic level, these were the only ones showing a modification of the global transcriptome after the evolution process. We determined also that the selection on transcriptional rewiring during the evolution occurred at process level instead of genes or subgenomes.