Dual protective role of manganese in the coral Stylophora pistillata under thermal stress: Scavenging of ambient superoxide and Symbiodiniaceae-associated Mn oxide production

The world is currently experiencing the fourth global coral bleaching event, which intensifies the urgency to create interventions that enhance coral thermal tolerance. Manganese (Mn) had been previously shown to offer benefits to corals under heat stress; however, the protective pathway remains unclear, and this uncertainty hampers moving forward in designing effective conservation and restoration strategies to protect coral reefs. For this reason, the scleractinian coral Stylophora pistillata, associated with dinoflagellate symbionts (Symbiodiniaceae) clade A, was exposed to thermal stress with and without Mn enrichment to determine the role of this metal in protecting the coral holobiont under a heatwave scenario. Our results showed a significant decline in superoxide in the ambient seawater with Mn addition, suggesting a protective action against ambient oxidative stress. Additionally, Symbiodiniaceae showed a higher photosynthetic efficiency, and the activity of the enzyme glutathione peroxidase (GPx) in corals decreased significantly with Mn supplementation, suggesting a reduced activity in neutralising reactive oxygen species (ROS) and a decrease in the ambient concentration of ROS. In contrast, superoxide dismutase (SOD) remained unaltered despite the expectation of a higher activity by its manganese-dependent component, MnSOD, to neutralise superoxide radicals produced by the stressed symbionts. Consistently, MnSOD gene expression was significantly downregulated with Mn supplementation, suggesting that MnSOD does not participate in the endogenous antioxidant defence of corals under thermal stress. Mn oxides (MnOx) were detected in Symbiodiniaceae with increasing Mn supplementation, with clade D showing the highest production compared with clades A and C. Together with previous findings, our results indicate that Mn concentrations of 6.4 to 75 nM support corals under heat stress via two possible pathways (i) by Mn uptake that leads to the production of MnOx by Symbiodiniaceae that function as antioxidants, mimicking the coral endogenous antioxidant defence, and (ii) by scavenging of superoxide radicals in seawater.