Heat stress causes inhibition of the de novo synthesis of antenna proteins and photobleaching in cultured Symbiodinium

Coral bleaching, caused by heat stress, is accompanied by the light-induced loss of photosynthetic pigments in in situ symbiotic dinoflagellate algae (Symbiodinium spp.). However, the molecular mechanisms responsible for pigment loss are poorly understood. Here, we show that moderate heat stress causes photobleaching through inhibition of the de novo synthesis of intrinsic light-harvesting antennae [chlorophyll a-chlorophyll c₂-peridinin- protein complexes (acpPC)] in cultured Symbiodinium algae and that two Clade A Symbiodinium species showing different thermal sensitivities of photobleaching also show differential sensitivity of this key protein synthesis process. Photoinhibition of photosystem II (PSII) and subsequent photobleaching were observed at temperatures of >31°C in cultured Symbiodinium CS-73 cells grown at 25-34°C, but not in cultures of the more thermally tolerant control Symbiodinium species OTcH-1. We found that bleaching in CS-73 is associated with loss of acpPC, which is a major antennae protein in Symbiodinium. In addition, the thermally induced loss of this protein is light-dependent, but does not coincide directly with PSII photoinhibition and is not caused by stimulated degradation of acpPC. In cells treated at 34°C over 24 h, the steady-state acpPC mRNA pool was modestly reduced, by ≈30%, whereas the corresponding synthesis rate of acpPC was diminished by >80%. Our results suggest that photobleaching in Symbiodinium is consequentially linked to the relative susceptibility of PSII to photoinhibition during thermal stress and occurs, at least partially, because of the loss of acpPC via undefined mechanism(s) that hamper the de novo synthesis of acpPC primarily at the translational processing step.