Thermal acclimation of the symbiotic alga Symbiodinium spp. alleviates photobleaching under heat stress

Abstract

A moderate increase in seawater temperature causes coral bleaching, at least partially through photobleaching of the symbiotic algae Symbiodinium spp. Photobleaching of Symbiodinium spp. is primarily associated with the loss of light-harvesting proteins of photosystem II (PSII) and follows the inactivation of PSII under heat stress. Here, we examined the effect of increased growth temperature on the change in sensitivity of Symbiodinium spp. PSII inactivation and photobleaching under heat stress. When Symbiodinium spp. cells were grown at 25°C and 30°C, the thermal tolerance of PSII, measured by the thermal stability of the maximum quantum yield of PSII in darkness, was commonly enhanced in all six Symbiodinium spp. tested. In Symbiodinium sp. CCMP827, it took 6 h to acquire the maximum PSII thermal tolerance after transfer from 25°C to 30°C. The effect of increased growth temperature on the thermal tolerance of PSII was completely abolished by chloramphenicol, indicating that the acclimation mechanism of PSII is associated with the de novo synthesis of proteins. When CCMP827 cells were exposed to light at temperature ranging from 25°C to 35°C, the sensitivity of cells to both high temperature-induced photoinhibition and photobleaching was ameliorated by increased growth temperatures. These results demonstrate that thermal acclimation of Symbiodinium spp. helps to improve the thermal tolerance of PSII, resulting in reduced inactivation of PSII and algal photobleaching. These results suggest that whole-organism coral bleaching associated with algal photobleaching can be at least partially suppressed by the thermal acclimation of Symbiodinium spp. at higher growth temperatures.

Figure 1.

Effect of growth temperature on the thermal tolerance of PSII in six different Symbiodinium spp. Cells were grown at 25°C or 30°C for 8 d. F_v/F_m was measured after incubation of cells for 1 h in darkness at temperatures ranging from 25°C to 38°C. Values are means ± sd from three independent experiments.

Figure 2.

Thermal acclimation of PSII stability in Symbiodinium sp. CCMP827. A, Symbiodinium sp. CCMP827 cells were grown at different temperatures ranging from 25°C to 32°C for 8 d. B, Symbiodinium sp. CCMP827 cells grown at 25°C were transferred to 30°C and incubated for different periods (3 h, 6 h, 1 d, or 8 d). C, Symbiodinium sp. CCMP827 cells grown at 30°C for 3 d were transferred to 25°C and incubated for different periods (2, 4, or 6 d). Control (Cont.) results are from experiments with cells continuously grown at 25°C. F_v/F_m was measured after incubation for 1 h in darkness at temperatures ranging from 25°C to 35°C. Values are means ± sd from three independent experiments.

Figure 3.

Effect of moderately increased growth temperature on the thermal tolerance of PSII in the presence and absence of chloramphenicol (Cm) in Symbiodinium sp. CCMP827. F_v/F_m was measured in CCMP827 cells incubated at 25°C or 30°C for 12 h in darkness in the absence (A) or presence of 1 mm chloramphenicol (B). Values are means ± sd from three independent experiments.

Figure 4.

Effect of moderately increased growth temperature on the thermal sensitivity of PSII to photoinhibition and subsequent repair in Symbiodinium sp. CCMP827. CCMP827 cells grown at 25°C or 30°C for more than 3 d were used for experiments. A, Cells were incubated at temperatures ranging from 25°C to 34°C in darkness for 1 h and then exposed to light at 200 µmol m⁻² s⁻¹ for 12 h. B, Cells were incubated at 30°C or 33°C in darkness for 1 h and then exposed to light at 200 µmol m⁻² s⁻¹ for 3 h in the presence of 1 mm chloramphenicol. C, Cells were preexposed to light at 2,000 µmol m⁻² s⁻¹ at their respective growth temperatures for 1 h. Cells were then incubated at 30°C or 33°C in darkness for 1 h before monitoring the recovery of F_v/F_m for 3 h at 20 µmol m⁻² s⁻¹. In all experiments, F_v/F_m was measured after 10 min of incubation in darkness. Values are means ± sd from three independent experiments. g.t., Growth temperature; t.t., treated temperature.

Figure 5.

Effect of moderately increased growth temperature on the thermal sensitivity of Symbiodinium spp. to photobleaching. Symbiodinium sp. CCMP827 cells grown at 25°C or 30°C were incubated at different temperatures ranging from 25°C to 35°C for 1 h in darkness. Subsequently, cells (5 µg chlorophyll mL⁻¹) were exposed to light at 200 µmol m⁻² s⁻¹ for 12 h at the same temperature. Total chlorophyll content (chlorophylls a and c₂) was measured before and after light exposure, and the loss of chlorophyll content (percentage of initial) was calculated. Values are means ± sd from three independent experiments.

Figure 6.

Effect of DCMU on the sensitivity of Symbiodinium spp. to photobleaching. Symbiodinium sp. CCMP827 cells grown at 25°C were incubated for 1 h in darkness with (+) or without (−) 5 µm DCMU and used for experiments. All experiments were carried out at 25°C. A, Effect of DCMU on photosynthesis. Photosynthetic oxygen production rate was measured under the light at 1,000 µmol photons m⁻² s⁻¹. The photosynthetic oxygen production rate was 115 ± 7.6 µmol oxygen mg⁻¹ chlorophyll h⁻¹ in the absence of DCMU (control). B, Effect of DCMU on photobleaching. Cells (5 µg chlorophyll mL⁻¹) were exposed to light at 200 µmol m⁻² s⁻¹ for 12 h. Total chlorophyll content (chlorophylls a and c₂) was measured before and after light exposure, and the loss of chlorophyll content (percentage of initial) was calculated. Values are means ± sd from three independent experiments.