Effects of metal toxicity on photosynthetic processes in coral symbionts, Symbiodinium spp.

Abstract

Metal toxicity affects a myriad of physiological and metabolic processes, including photosynthesis, in plant cells; however, the primary sites of metal poisoning and the sequence of physiological alterations remain a topic of controversy. Using a fluorescence induction and relaxation technique and quantitative immunoblots, we examined toxic effects of metal ions (Cu, Zn, Cd and Pb) on photosynthetic light-harvesting processes, photochemistry in photosystem II (PSII), and photosynthetic electron transport in symbiotic dinoflagellates, Symbiodinium spp. (zooxanthellae). The analysis of metal-induced alterations in fluorescence parameters revealed an early inhibition of the electron transport between PSII and PSI and of the maximum rates of photosynthetic electron transport (Pmax), suggesting that the primary targets of metal toxicity are the processes downstream PSII, rather than photochemistry in PSII. The Cu-, Zn-, and Cd-induced inhibition of electron transport between PSII and PSI was followed by a decrease in the energy transfer in light-harvesting complexes, implying that these metals may impact the functional integrity of lipid membranes. A striking decrease in Pmax was observed much earlier than any alterations in photochemistry or time constants for electron transport within PSII and occurred prior to a decrease in cellular Rubisco content. This is common for both essential (Cu and Zn) and non-essential (Cd and Pb) metals. However, Cu and Zn have a greater impact on photosynthetic processes, while Cd and Pb affect cell growth rates to a greater extent. Immunoblot protein analysis revealed that PSII core proteins, PsbA and PsbD, start to degrade prior to Rubisco and ATP synthase under exposure to Zn, Cd, or Pb. In contrast, Cu poisoning leads to stronger degradation of Rubisco and ATP synthase than of PsbA and PsbD. High growth irradiance accelerated the damage to the electron transport between PSII and PSI and photochemistry in PSII. Our results are important for understanding the physiological processes involved in metal poisoning in aquatic organisms and provide a background for the development of express diagnostics and identification of stressors in aquatic environments.