Abstract

Exposure to long-term environmental changes across >100s of generations results in adapted phenotypes, but little is known about how metabolic and transcriptional responses are optimized in these processes. Here, we show that thermotolerant yeast strains selected by adaptive laboratory evolution to grow at increased temperature, activated a constitutive heat stress response when grown at the optimal ancestral temperature, and that this is associated with a reduced growth rate. This preventive response was perfected by additional transcriptional changes activated when the cultivation temperature is increased. Remarkably, the sum of global transcriptional changes activated in the thermotolerant strains when transferred from the optimal to the high temperature, corresponded, in magnitude and direction, to the global changes observed in the ancestral strain exposed to the same transition. This demonstrates robustness of the yeast transcriptional program when exposed to heat, and that the thermotolerant strains streamlined their path to rapidly and optimally reach post-stress transcriptional and metabolic levels. Thus, long-term adaptation to heat improved yeasts ability to rapidly adapt to increased temperatures, but this also causes a trade-off in the growth rate at the optimal ancestral temperature.

Highlights

  • Changes in signaling networks to adjust gene expression programs and metabolic fluxes according to environmental change is a concomitant homeostatic response of cells when getting exposed to agents which can damage their macromolecules and desynchronize their metabolism[1,2,3]

  • Earlier we found that seven thermotolerant S. cerevisiae strains (TTSs) isolated from independent adaptive laboratory evolution (ALE) experiments at high temperature (39.5 °C), acquired single nucleotide variations (SNVs) in ATP2/3 and ERG3 genes[18]

  • These observations suggested that the TTSs could display very different gene expression and metabolic programs compared to the wild type strain (WTS) in cultivations at the ancestral and high temperatures, allowing the TTSs to robustly control heat stress

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Summary

Introduction

Changes in signaling networks to adjust gene expression programs and metabolic fluxes according to environmental change is a concomitant homeostatic response of cells when getting exposed to agents which can damage their macromolecules and desynchronize their metabolism[1,2,3]. In S. cerevisiae, changes in the membrane lipid composition affected the expression of the HSP70 family and the HSP82 gene which is a negative regulator of the heat-shock transcription factor HSF1, modifying the threshold of the heat shock response[24,25] These observations suggested that the TTSs could display very different gene expression and metabolic programs compared to the WTS in cultivations at the ancestral and high temperatures, allowing the TTSs to robustly control heat stress. To test this hypothesis, we here studied transcriptional, metabolic and physiological responses of the TTSs and the WTS in cultivations at 30 °C and 40 °C

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