Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species

Abstract

Coral bleaching caused by heat stress is accompanied by photoinhibition, which occurs under conditions where the rate of photodamage to photosystem II (PSII) exceeds the rate of its repair, in the symbiotic algae (Symbiodinium spp.) within corals. However, the mechanism of heat stress-induced photoinhibition in Symbiodinium still remains poorly understood. In the present work, we have investigated the effect of elevated temperature on the processes associated with the repair of photodamaged PSII in cultured Symbiodinium (OTcH-1 and CS-73). Severe photoinhibition was observed at temperature exceeding 32°C in Symbiodinium CS-73 cells grown at 25-34°C but not in cultures of the more thermally tolerant Symbiodinium OTcH-1. After photoinhibition treatment by strong light, photodamaged PSII was repaired close to initial levels under low light at 25°C in both OTcH-1 and CS-73. However, the repair was strongly inhibited by increased temperature exceeding 31°C in CS-73 but only weakly in OTcH-1. We found that inhibition of the repair process in CS-73 is attributed to impairment of both protein synthesis-dependent and -independent repair processes and is at least partially caused by suppression of the de novo synthesis of thylakoid membrane proteins and impairment of the generation of ⌬pH across the thylakoid membrane, respectively. Our results suggest that acceleration of photoinhibition by moderate heat stress is attributed primarily to inhibition of the repair of photodamaged PSII and that the photoinhibition sensitivity of Symbiodinium to heat stress is determined by the thermal sensitivity of the PSII repair processes.coral bleaching ͉ heat stress ͉ photoinhibition ͉ photosystem II ͉ zooxanthellae

Lipid biomarkers in Symbiodinium dinoflagellates: new indicators of thermal stress

“…A culture study of Synechocystis cells genetically unable to produce PUFAs showed that this strain was more sensitive to thermal stress than the PUFA-producing wild type; the difference was attributed to PSII repair efficiency (Gombos et al 1994). The capacity to efficiently repair thermally damaged PSII structures may also determine thermal stress tolerance in Symbiodinium (Takahashi et al 2009). Recent experiments with Arabidopsis thaliana mutants demonstrated that triunsaturated fatty acids are abundant in wild-type thylakoid membranes and are required for thermal tolerance (Routaboul et al 2012).…”

Temperature Effects on the Growth Rates and Photosynthetic Activities of Symbiodinium Cells

“…Several hypotheses have been proposed to explain how elevated temperatures affect the photochemical pathway: excessive photon absorption by light harvesting antennae damages the PSII reaction center, particularly the D1 protein [17][18][19]; elevated temperatures may limit photosynthesis by destabilizing the thylakoid membranes [7]; the activity of Rubisco may be a primary site of damage by elevated temperature [20], though a recent study suggests that inhibition of the Calvin-Benson cycle alone does not induce coral bleaching [21]; damaged PSII reaction centers may be replaced by re-synthesized D1 protein, but this mechanism is inhibited when temperature is elevated [10]; elevated temperatures may also suppress the synthesis of light harvesting antennae protein at the translational step, thereby promoting losses of major light harvesting proteins [9]. Several of these postulates have been supported by recent studies indicating that the thermal stress susceptibility of Symbiodinium is determined by the repair capacity of the photosynthetic mechanism [10,22,23].…”

“…Thermal stress has different impacts on the photobiology and growth of diverse phylotypes of cultured Symbiodinium cells [7][8][9][10][11]. The production of reactive oxygen species (ROS) in response to elevated temperature differs among Symbiodinium types [12,13].…”

The dynamics of microbial partnerships in the coral Isopora palifera

“…Symbiodinium are geographically specific; the clades C and D are dominant in the corals dwelling in western Pacific Ocean, whereas other types are detected in other oceans, for example, the Caribbean Sea (Baker, 2003). Symbiodinium are functionally diverse and, typically, display variations in tolerance against high temperature and irradiance (Baker, 2003;Stat et al, 2008;Mieog et al, 2009;Takahashi et al, 2009). For instance, Symbiodinium clade D is more heat tolerant and is thus found more often in corals subject to conditions of higher temperature or irradiance (Baker, 2001;Rowen, 2004).…”