Symbiont dynamics during thermal acclimation using cnidarian-dinoflagellate model holobionts

Warming oceans menace reef ecosystems by disrupting symbiosis between cnidarians and Symbiodinium zooxanthellae, thus triggering bleach episodes. Temperature fluctuations promote adjustments in physiological variables and symbiont composition, which can cause stress responses, but can also yield adaptation if fitter host-symbiont homeostasis are achieved. To understand such processes manipulative studies are required, but many reef-building cnidarians pose limitations to experimental prospects. We exposed Exaiptasia anemones to Gradual Thermal Stress (GTS) and Heat Shock (HS) exposures and monitored chlorophyll and symbiont dynamics to test the phenotypic plasticity of these photosynthetic holobionts. GTS enhanced chlorophyll concentrations and decreased Symbiodinium proliferation. A recovery period after GTS returned chlorophyll to lower concentrations and symbiont divisions to higher rates. HS triggered a stress response characterized by intense symbiont declines through degradation and expulsion, algal compensatory proliferation, and chlorophyll accumulation. Anemones pre-exposed to GTS displayed more acute signs of symbiont paucity after HS, demonstrating that recurrent stress does not always induce bleaching-resistance. Our study is the first documenting Symbiodinium C and D, along with the predominant Clade B1 in Exaiptasia anemones. C subclades found in outdoor specimens faded under laboratory exposures. Clade D emerged after HS treatments, and especially after GTS pre-exposure. This highlights the thermotolerance of D subclades found in E. pallida and shows that bleaching-recovery can involve shifts of background symbiont phylotypes. This study enlightens the capability of Exaiptasia anemones to acclimate to gradually increased temperatures, and explores into how thermal history influences in subsequent stress tolerance in symbiotic cnidarians.