O2: Dr Jekyll and Mr Hyde in symbiotic dinoflagellates (Symbiodinium) from reef-building corals

Coral reefs are among the most beautiful and complex of all ecosystems on Earth. Although they cover less than 1% of the world’s oceans area, this marine ecosystem harbors a huge biodiversity and is vital to human society and industries. The foundation of coral reefs relies on the fragile mutualistic relationship between reef-building corals and their photosynthetic dinoflagellates of the genus Symbiodinium. However, this symbiosis is highly sensitive to environmental or anthropogenic disturbances and may be disrupted, thus leading to the coral bleaching phenomenon. It has been reported that the initial steps of this process are linked to photosynthesis and the antioxidant network in Symbiodinium. However the nature of the cellular mechanisms leading to the generation of reactive oxygen species and to the disruption of the symbiosis is not completely unraveled. Therefore, this study aimed to highlight the existence of photosynthetic alternative electron flows reducing molecular oxygen and the way by which they can induces an oxidative stress, in four Symbiodinium strains belonging to three different clades. Joint measurements of oxygen evolution, PSI and PSII activities by chlorophyll a fluorescence and spectrophotometric measurements allowed us to demonstrate that photoreduction of oxygen by the so-called Mehler reaction is the main electron sink at the onset of photosynthesis and during steady state photosynthesis. When Symbiodinium cells were exposed to high light conditions, the Mehler reaction and the ascorbate-glutathione cycle (water-water cycle) acted as a safety valve and drained up to 50% of the electrons from PSII, protecting it from photoinhibition and dissipating rapidly the excess photon energy by downregulation of PSII. As long as the WWC efficiency was maintained in the chloroplasts of Symbiodinium, ROS generated as a by-product of the Mehler reaction did not significantly damage target molecules and induced an acclimatory response through up-regulation of enzymes involved in the antioxidant response (superoxide dismutase, ascorbate peroxidase, glutathione reductase). Nevertheless, when cells were exposed to light stress and elevated temperature (33°C), the WWC supported 75% of the electrons coming from PSII. This increase generated twice more H2O2 than during the treatment at 26°C and resulted in the inactivation of target enzymes of the WWC. Therefore, this means that under these conditions the photoprotective functions of the WWC can no longer be maintained, thus opening the way to ROS accumulation and to the induction of coral bleaching.We found that the response to oxidative stress differed between and within Symbiodinium clades. Symbiodinium clade A was less sensitive to the chemical induced oxidative stress than the others investigated strains. These variations are most likely related to their geographic origin, their thermal history, as well as to their physiological adaptations to the local environment. They may contribute to the explanation of why coral colonies and coral species have been found to differ in their susceptibilities to bleach. However, although the antioxidant response differs to some extent, some common traits were conserved. Among them, Diatoxanthin, a xanthophyll pigment involved in the non-photochemical quenching process could also have an antioxidant function. In addition, it seems that the ubiquitin-proteasome pathway is involved in the antioxidant response by eliminating carbonylated protein