Optics and Ecophysiology of Coral Reef Organisms

In order to understand the contribution of pigmented coral tissues to the extraordinary optical properties of the coral-symbiont-skeleton unit, we analyzed the associations between structural and optical traits for four coral species, which broadly differ in skeleton morphology, tissue thickness and in the variation of coral pigmentation, symbiont content, Symbiodinium dominant type and Symbiodinium cell pigmentation (Ci). Significant differences among species were found for the maximum capacity of light absorption (A_max) and for the minimum pigmentation required to reach that maximum. The meandroid morphotype represented by Pseudodiploria strigosa showed a slightly lower A_max than the other three chalice-type species, while the thickest species, Montastraea cavernosa, required 2–3.5 times higher pigmentation to reach A_max. In contrast, Orbicella faveolata and Orbicella annularis, which were able to harbor high number of symbionts and achieve the highest photosynthetic rates per area, showed the largest abilities for light collection at decreasing symbiont densities, leading to a more fragile photophysiological condition under light and heat-stress. Holobiont photosynthesis was more dependent on Symbiodinium performance in the less populated organisms. At reduced pigmentation, we observed a similar non-linear increase in holobiont light absorption efficiency (a*_Chla), which was differentially modulated by reductions in the number of symbionts and Symbiodinium Ci. For similar pigmentation, larger symbiont losses relative to Ci declines resulted in smaller increases in a*_Chla. Two additional optical traits were used to characterize light absorption efficiency of Symbiodinium (a*_sym) and coral host (a*_M). Optimization of a*_sym was well represented by P. strigosa, whereas a*_M was better optimized by O. annularis. The species with the largest symbiont content, O. faveolata, and with the thickest tissues, M. cavernosa, represented, respectively, less efficient solutions for both coral traits. Our comparison demonstrates the utility of optical traits to characterize inter-specific differences in coral acclimatization and performance. Furthermore, holobiont light absorption efficiency (a*_Chla) appeared as a better proxy for the “bleached phenotype” than simple reductions in coral color. The analysis of a putative coordinated variation in the number of symbionts and in Symbiodinium cell pigmentation deserves special attention to understand holobiont optimization of energy collection (a*_Chla) and photosynthetic performance.

Photosynthetic coral reef structures extend from the shallow sundrenched waters to the dimly lit, “twilight” mesophotic depths. For their resident endosymbiotic dinoflagellates, primarily from the genus Symbiodinium spp., this represents a photic environment that varies ~15-fold in intensity and also differs in spectral composition. We examined photosynthesis in the scleractinian coral Stylophora pistillata in shallow (3 m) and mesophotic settings (65 m) in the northern Red Sea. Symbiodinium spp. in corals originating from the mesophotic environment consistently performed below their photosynthetic compensation point and also exhibited distinct light harvesting antenna organization. In addition, the non-photochemical quenching activity of Symbiodinium spp. from mesophotic corals was shown to be considerably lower than those found in shallow corals, showing they have fewer defenses to high-light settings. Over a period of almost 4 years, we extensively utilized closed circuit Trimix rebreather diving to perform the study. Phylogenetic analysis showed that shallow corals (3 m) transplanted to a deep reef environment (65 m) maintained their initial Symbiodinium spp. community (clade A), rather than taking on deep low-light clades (clade C), demonstrating that shallow S. pistillata acclimate to low-light mesophotic environments while maintaining their shallow photosynthetic traits. Mesophotic corals exhibited static depth-related chlorophyll content per cell, a decrease in PSI activity and enhanced sigmoidal fluorescence rise kinetics. The sigmoidal fluorescence rise kinetics we observed in mesophotic corals is an indication of energy transfer between photosynthetic units. We postulate that at mesophotic depths, a community of adapted Symbiodinium spp. utilize a unique adaptation to lower light conditions by shifting their light harvesting to a PSII based system, where PSII is structured near PSI, with additional PCP soluble antenna also trapping light that is funneled to the PSI reaction center. In this study, we provide evidence that mesophotic Symbiodinium spp. have developed novel adaptive low-light characteristics consisting of a cooperative system for excitation energy transfer between photosynthetic units that maximizes light utilization.