Heat-Evolved Microalgae (Symbiodiniaceae) Are Stable Symbionts and Influence Thermal Tolerance of the Sea Anemone Exaiptasia diaphana

Abstract

Symbiotic cnidarians, such as sea anemones and corals, rely on their mutualistic microalgal partners (Symbiodiniaceae) for survival. Marine heatwaves can disrupt this partnership, and it has been proposed that introducing experimentally evolved, heat-tolerant algal symbionts could enhance host thermotolerance. To test this hypothesis, the sea anemone Exaiptasia diaphana (a coral model) was inoculated with either the heterologous wild type or heat-evolved algal symbiont, Cladocopium proliferum, and homologous wild-type Breviolum minutum. The novel symbioses persisted for 1.5 years and determined holobiont thermotolerance during a simulated summer heatwave. Anemones hosting SS8, one of the six heat-evolved strains tested, exhibited the highest thermotolerance. Notably, anemones hosting the wild-type C. proliferum (WT10) were the second most thermally tolerant group, whereas anemones hosting the heat-evolved SS5 or SS9 strains were among the most thermosensitive. Elevated temperatures led to an increase in the levels of many amino acids and a decrease in tricarboxylic acid (TCA) metabolites in all anemone hosts, potentially indicating an increase in autophagy and a reduction in energy and storage production. Some consistent differences were observed in changes in metabolite levels between anemone groups in response to elevated temperature, suggesting that the algal symbiont influenced host metabolome and nutritional budget.