Photoecophysiology of symbiotic zooxanthellae of hermatypic corals

Abstract

Coral bleaching involves the breakdown of the symbiosis between corals and dinoflagellates of the diverse genus Symbiodinium (also referred to as zooxanthellae), where the zooxanthellae and/or algal pigments are lost from the coral-algae symbiosis. Elevated temperatures and high solar irradiances are considered to be the primary factors causing mass coral bleaching. Yet, in spite of extensive research in this area, the physiological processes underlying the bleaching response, specifically the large inter- and intraspecific variability of bleaching susceptibility, are not unequivocally resolved. The major objective of this study was to provide further insights into the mechanistic understanding of the inter- and intraspecific variability of bleaching susceptibility by addressing potential causes for this variability. The study focussed on photophysiological responses of Symbiodinium to elevated temperatures and high light (HL), with a particular emphasis on the engagement of photoprotection, and on the role of the coral host in modifying the response of the algal symbionts to HL. The capacity of corals to change their mode of nutrition towards heterotrophy under light deprivation in order to maintain the integrity of the symbiosis was also evaluated. In a bi-factorial experiment, the combined effects of enhanced temperatures and increased irradiances on photosynthetic performance and photoprotective mechanisms of two Symbiodinium clade A phylotypes in culture were investigated over a period of three weeks. Both phylotypes clearly differed in their thermal sensitivity, and HL exposure generally amplified the temperature effect. Symbiodinium Ax was highly sensitive to elevated temperatures greater than 30°C, showing strongly impaired growth and a sharp decline in photochemical efficiency of photosystem II (PSII) indicative of severe chronic photoinhibition. By contrast, Symbiodinium A1 was thermally tolerant and maintained high photochemical efficiency even at 32°C and HL. This could be attributed to an enhanced photoprotective capacity associated with higher cellular concentrations of xanthophyll cycle pigments and the low-molecular antioxidant as well as the dynamic regulation of these photoprotective pathways in response to experimental conditions. Glutathione plays a central role in the cellular antioxidative system due to its involvement in many antioxidative reactions. This study presents the first results on the role of glutathione as a proxy for oxidative stress in cultured Symbiodinium under thermal and HL stress. The findings of the differential temperature sensitivity prove that the generalization of physiological attributes to specific Symbiodinium clades is not justified. To evaluate the contribution of the coral host in modifying the bleaching response, the photophysiological response of in hospite Symbiodinium to short-term HL exposure was studied in two coexisting corals, both associated with the same Symbiodinium phylotype. The photophysiological responses towards high levels of solar radiation clearly differed between both coral species: The rapid synthesis of photoprotective pigments, including xanthophyll cycle pigments as well as a high xanthophyll cycling activity, was solely observed in symbionts of the thin-tissued Pocillopora damicornis. Nonetheless, this up-regulation of photoprotection was insufficient to prevent photoinhibition and bleaching in P. damicornis. By contrast, the thick-tissued Pavona decussata was able to withstand HL exposure without experiencing a sustained decline in photochemical efficiency or symbiont density and, most notably, without a pronounced engagement of photoprotective pigments. Our results suggest species-specific differences in the light levels reaching Symbiodinium within the coral tissue, presumably due to disparate inherent optical properties of the coral tissue in both species. The importance of phototrophic vs. heterotrophic mode of nutrition for the functionality of the photosynthetic apparatus of algal symbionts and the integrity of the entire coral-algae symbiosis was investigated in P. damicornis by exposing corals to artificial light deprivation in situ at two sites in a (natural) reef. Both sites are located around Heron Island (Great Barrier Reef, Australia), but differ in their hydrodynamic characteristics. Site-specific differences in the response of P. damicornis to light deprivation were detected: light-deprived corals at North Wistari Reef (low flow-site) showed a partial decline in photochemical efficiency of PSII and a dramatic loss of symbionts after two weeks, while corals at Coral Gardens (high flow-site) maintained a functional symbiosis. Hence, the higher water flow may have enabled corals at Coral Gardens to shift from photo- to heterotrophic nutrition more efficiently in order to meet the energy needs of the symbiosis compared to those at North Wistari reef due to a higher availability of food.