Imbalance between oxygen photoreduction and antioxidant capacities in <i>Symbiodinium</i> cells exposed to combined heat and high light stress

During the last decades, coral reefs have been affected by several large-scale bleaching events, and such phenomena are expected to increase in frequency and severity in the future, thus compromising their survival. High sea surface temperature accompanied by high levels of solar irradiance has been found to be responsible for the induction of oxidative stress ultimately ending with the disruption of the symbiosis between cnidarians and Symbiodinium. For two decades, many studies have pointed to the water–water cycle (WWC) as being one of the primary mediators of this phenomenon, but the impacts of environmental stress on the O2 reduction by PSI and the associated reactive oxygen species (ROS)-detoxifying enzymes remain to be determined. In this study, we analyzed the impacts of acute thermal and light stress on the WWC in the model Symbiodinium strain A1. We observed that the high light treatment at 26 °C resulted in the up-regulation of superoxide dismutase, ascorbate peroxidase, and glutathione reductase activities and an increased production of ROS with no significant change in O2-dependent electron transport. Under high light and at 33 °C, O2-dependent electron transport was significantly increased relative to total electron transport. This increase was concomitant with a twofold increase in ROS generation compared with the treatment at 26 °C, while enzymes involved in the WWC were largely inactivated. These data show for the first time that combined heat and light stress inactivate antioxidant capacities of the WWC and suggests that its photoprotective functions are overwhelmed under these conditions. This study also indicates that cnidarians may be more prone to bleach if they harbor Symbiodinium cells having a highly active Mehler-type electron transport, unless they are able to quickly up-regulate their antioxidant capacities