Remembering heat: How the unicellular alga Cyanidioschyzon merolae establishes a molecular stress memory that boosts its thermotolerance

While this has been extensively studied in multicellular organisms, we demonstrate that heat stress memory is also present in the unicellular red alga Cyanidioschyzon merolae. We show that, similarly to more complex organisms, thermomemory in this alga is underpinned by transcriptomic reprogramming, with the chloroplast emerging as the main site of gene trainability.

Additionally, we find a conserved small heat shock protein (sHSP)-encoding locus in the nuclear genome to be heat-trainable, likely by histone depletion and modification through the repressive mark H3K27me3. We show that of C. merolae’s two sHSPs, only CmsHSP2 is necessary for proper HS memory establishment, and that the two sHSPs localize to different cellular compartments during heat stress. Finally, comparative RNA-Sequencing of an Enhancer of zeste mutant reveals a role for the H3K27me3-transferase in adapting the transcriptome to recurring heat exposures, beyond regulating the trainable sHSP locus.