Repeated heat waves trigger divergent transcriptional responses in cold- and warm-adapted yeast species

Extreme climatic events such as heat waves pose major challenges to species survival and have profound impacts on evolutionary processes. Plasticity is thought to buffer organismal stress, yet the molecular mechanisms underlying plastic responses remain poorly understood. In particular, the role of transcriptional plasticity and stress memory in responding to repeated stress events remains unresolved. Here, we experimentally exposed clonal populations of eight divergent Saccharomyces yeast species with different thermal tolerances to repeated heat waves. We compared their phenotypic and transcriptomic profiles after a few generations of mitotic growth, reflecting transcriptional changes. Warm-adapted species maintained higher growth than cold-adapted species across heat wave exposures. Thermo-generalist species showed intermediate outcomes with one species improving growth across repeated heat waves. To interpret transcriptomic results, we used a conceptual framework separating no-memory (gene expression independent from prior exposure) from memory-associated responses (expression modulated by prior exposure). No-memory responses showed conserved transcriptomic signatures of proteostasis induction, and reduced expression of ribosome biogenesis and translation upon repeated heat waves. Memory-associated responses were more rare and highly species-specific, showing opposite patterns of (de)sensitization in ribosomal and translational pathways in species at the two extremes of thermal tolerance. Together, our results show that thermal resilience can arise through alternative transcriptional changes and suggests that warm- and cold-temperature specialists adopt divergent gene regulatory strategies upon repeated heat waves. With climate change projections indicating more frequent and intense heat waves, understanding plastic responses across species with ecologically and genetically different backgrounds is crucial.