Distinct transcriptomic strategies underlie differential heat tolerance in Symbiodiniaceae symbionts

Dinoflagellate algae in the family Symbiodiniaceae, symbionts of many marine cnidarians are critical for the metabolic integrity of reef ecosystems, which are increasingly threatened by environmental stress. The resilience of the cnidarian-dinoflagellate symbiosis depends on thermotolerance of the partner organisms; coral hosts that harbor heat-resistant symbionts exhibit greater resistance to bleaching. Although coral responses to heat stress are well-documented, transcriptomic adaptation/acclimation of Symbiodiniaceae to elevated temperatures are limited. Here, we compare thermal responses of two species representing two genera of Symbiodiniaceae, Symbiodinium linucheae (strain SSA01; ITS2 type A4) and Breviolum minutum (strain SSB01; ITS2 type B1). SSA01 in culture maintained photosynthetic function at elevated temperatures and mounted a rapid transcriptomic response characterized by early downregulation of a JMJ21-like histone demethylase coupled with prompt upregulation of transcripts associated with DNA repair and oxidative stress, which would likely contribute to enhanced resilience to heat stress. In contrast, SSB01 experienced a decline in photosynthetic efficiency and a delayed transcriptomic response that included upregulation of transcripts encoding proteasome subunits and reduced transcripts encoding proteins involved in photosynthesis and metabolite transport. These findings indicate that a rapid and moderate transcriptomic response that results in increased expression of genes related to the synthesis and repair of biomolecules might be crucial for thermal tolerance in the Symbiodiniaceae whereas sensitivity to elevated temperatures may be reflected by increased protein turnover and a marked decline in anabolic processes. Understanding these differences is vital for predicting coral responses to warming seas and developing strategies to mitigate heat-stress impacts on reefs.