Gene regulation underpinning increased thermal tolerance in a laboratory-evolved coral photosymbiont.

Small increases in ocean temperature can disrupt the obligate symbiosis between corals and dinoflagellate microalgae, resulting in coral bleaching. Little is known about the genes that drive the physiological and bleaching response of algal symbionts to elevated temperature. Moreover, many studies to-date have compared highly divergent strains, making it challenging to accredit specific genes to contrasting traits. Here, we compare transcriptional responses at ambient (27°C) and bleaching-relevant (31°C) temperatures in a monoclonal, wild-type (WT) strain of Symbiodiniaceae to those of a selected-strain (SS), derived from the same monoclonal culture and experimentally evolved to elevated temperature over 80 generations (2.5 years). Thousands of genes were differentially expressed at a log fold-change of >8 between the WT and SS over a 35 days temperature treatment period. At 31°C, WT cells exhibited a temporally unstable transcriptomic response upregulating genes involved in the universal stress response such as molecular chaperoning, protein repair, protein degradation and DNA repair. Comparatively, SS cells exhibited a temporally stable transcriptomic response and downregulated many stress response genes that were upregulated by the WT. Among the most highly upregulated genes in the SS at 31°C were algal transcription factors and a gene probably of bacterial origin that encodes a type II secretion system protein, suggesting interactions with bacteria may contribute to the increased thermal tolerance of the SS. Genes and functional pathways conferring thermal tolerance in the SS could be targeted in future genetic engineering experiments designed to develop thermally resilient algal symbionts for use in coral restoration and conservation.