Critical role of oxygen photoreduction downstream of PSI in Symbiodinium: photoprotection, energetic adjustement and ROS production

The ecological success of symbiotic cnidarians (reef building-corals and sea anemones) relies on the symbiosis between cnidarians and photosynthetic dinoflagellates of the genus Symbiodinium. Photosynthetic organisms have evolved various photoprotective and regulatory mechanisms to cope with changing and high light intensities, but the nature and relative amplitude of these mechanisms is still a matter of debate in Symbiodinium. Few studies showed that molecular oxygen (O2) can be an efficient electron sink during photosynthesis in Symbiodinium, with an O2 uptake capacity that could represent up to half the maximum O2 evolution. In addition, members of clade A Symbiodinium were proposed to possess enhanced capabilities for alternative photosynthetic electron flows. In this work, the amplitude of photosynthetic alternative electron flows to oxygen (chlororespiration, Mehler reaction, mitochondrial respiration) and PSI cyclic electron flow were investigated in Symbiodinium strains belonging to different Clades (A, B and F). Joint measurements of oxygen evolution, PSI and PSII activities allowed us to demonstrate that photoreduction of oxygen downstream PSI by the so-called Mehler reaction is the main alternative electron sink at the onset and steady state of photosynthesis in all strains1. This mechanism in Symbiodinium sustains significant photosynthetic electron flux under high light, thus acting as a photoprotective mechanism and modifying the ratio of ATP/NADPH to match the requirements of carbon reduction. At higher temperature (26 to 33°C), the amplitude of Mehler reaction was still significantly increased but the capacity of enzymes responsible for superoxide detoxification largely decreased. This imbalance generated twice more ROS than during the treatment at 26°C, suggesting that under conditions known to induce coral bleaching, the photoprotective role of Mehler reaction can no longer be maintained, at least at short term.