Over the past three decades, massive bleaching events of zooxanthellate corals have been documented across the range of global distribution. Although the phenomenon is correlated with relatively small increases in sea-surface temperature and enhanced light intensity, the underlying physiological mechanism remains unknown. In this article we demonstrate that thylakoid membrane lipid composition is a key determinate of thermal-stress sensitivity in symbiotic algae of cnidarians. Analyses of thylakoid membranes reveal that the critical threshold temperature separating thermally tolerant from sensitive species of zooxanthellae is determined by the saturation of the lipids. The lipid composition is potentially diagnostic of the differential nature of thermally induced bleaching found in scleractinian corals. Measurements of variable chlorophyll fluorescence kinetic transients indicate that thermally damaged membranes are energetically uncoupled but remain capable of splitting water. Consequently, a fraction of the photosynthetically produced oxygen is reduced by photosystem I through the Mehler reaction to form reactive oxygen species, which rapidly accumulate at high irradiance levels and trigger death and expulsion of the endosymbiotic algae. Differential sensitivity to thermal stress among the various species of Symbiodinium seems to be distributed across all clades. A clocked molecular phylogenetic analysis suggests that the evolutionary history of symbiotic algae in cnidarians selected for a reduced tolerance to elevated temperatures in the latter portion of the Cenozoic.C oral bleaching on a global scale is a growing concern because of both the reduction in essential ecological services provided by zooxanthellate corals within reef communities (1, 2) and the potentially devastating economic impacts accompanying the phenomenon (3). Small, positive deviations in temperature of Ͻ2°C can trigger massive losses of symbiotic algae, Symbiodinium spp., from their cnidarian host cells (4). However, not all corals within a reef are equally susceptible to elevated temperature stress (5, 6). Although elevated temperatures often lead to a reduction in the quantum yield of photochemistry, a concomitant increase in the rate of protein turnover in oxygen-generating reaction center, photosystem (PS)II (7-9), and an increase in the production of reactive oxygen species (ROS) (10-12), no mechanism has been elucidated. Here we show that thermal sensitivity in isolated clones of zooxanthellae and in symbiotic animal hosts is correlated with the degree of saturation of the lipids in the thylakoid membranes in the algal plastids. Our results provide a mechanistic basis for understanding and diagnosing coral bleaching patterns in nature.
Materials and MethodsCultures and Corals. Cultures of Symbiodinium spp., obtained from culture collections or isolated from hosts, were grown in F͞2 medium under a 10͞14-h light͞dark cycle and illuminated with 100 mol quanta m Ϫ2 ⅐s Ϫ1 . Corals were grown at 26°C in 800 liters of aquaria with running ...