Exploring adaptation routes to low temperatures in the Saccharomyces genus

Abstract

The identification of traits that affect adaptation of microbial species to external abiotic factors, such as temperature, is key for our understanding of how biodiversity originates and can be maintained in a constantly changing environment. The Saccharomyces genus, which includes eight species with different thermotolerant profiles, represent an ideal experimental platform to study the impact of adaptive alleles in different genetic backgrounds. Previous studies identified a group of genes important for maintenance of growth at lower temperatures. Here, we carried out a genus-wide functional analysis in all eight Saccharomyces species for six candidate genes. We showed that the cold tolerance trait of S. kudriavzevii and S. eubayanus is likely to be evolved from different routes, involving genes important for the conservation of redox-balance, and for the long-chain fatty acid metabolism, respectively. For several loci, temperature- and species-dependent epistasis was detected, underlying the plasticity and complexity of the genetic interactions. The natural isolates of S. kudriavzevii, S. jurei and S. mikatae had a significantly higher expression of the genes involved in the redox balance compared to S. cerevisiae, raising the question of what proportion of the trait is accounted for solely due to transcriptional strength. To tease apart the role of gene expression from that of allelic variation, for two genes we independently replaced in four yeast species either the promoters or the alleles with those derived from S. kudriavzevii. Our data consistently showed a significant fitness improvement at cold temperatures in the strains carrying the S. kudriavzevii promoter, while growth was lower upon allele swapping. These results suggest that transcriptional strength plays a bigger role in growth maintenance at cold over the allele type and supports a model of adaptation centred on stochastic tuning of the expression network. Author summaryThe decline in biodiversity due to environmental changes influences the stability of ecosystems by altering the geographic distribution of several microbial and fungal species. Temperature is one of the leading factors that drive adaptation and different organisms share the same habitat because of their different thermal profiles. It is therefore important to study the genes that affect the fitness of microorganisms at different temperatures in order to understand both how biodiversity originated and how can be maintained. The Saccharomyces genus, which includes species with different thermotolerant profiles, represent an ideal experimental platform to investigate the impact of adaptive alleles in response to temperature changes. Here, we carried out a functional analysis for putative cold-tolerant genes and showed that this trait is likely to be evolved from different routes in different species, involving the conservation of redox-balance and alteration of membrane fluidity. Furthermore, for several species, genetic interactions display fitness tradeoffs in different environments. Finally, by unravelling the interplay between gene expression, allele variation, genetic background and environment, this study shed light on the intricate nature of transcriptional regulation and its pivotal role in facilitating cold adaptation in Saccharomyces species.