Mucilage-induced necrosis reveals cellular oxidative stress in the Mediterranean gorgonian Paramuricea clavata

The red gorgonian Paramuricea clavata is a fundamental ecosystem engineer of coralligenous biocenosis in the Mediterranean Sea, where it plays crucial ecological functions and enhances the habitat biodiversity. However, this species is strongly endangered due to climate change-related stressors such as mucilage events, which have increased in recent decades causing extensive damage and mortality, but whose impacts at the molecular and cellular levels are still unexplored. In this study, different cellular stress biomarkers were analyzed in mucilage-colonized P. clavata specimens living in the Portofino Marine Protected Area (Ligurian Sea, Italy), in order to elucidate the cellular pathways affected by mucilage and the cellular defense mechanisms adopted. Within these colonies, portions of healthy tissue located at different distances from mucilage-induced necrosis were considered. Our results showed that mucilage affected the cellular oxidative status and impaired lipid cell membranes of the whole P. clavata colony. Indeed, an increase in the superoxide dismutase (SOD) and glutathione reductase (GR) enzymatic activity and in the level of lipid peroxidation (LPO) was detected in colonies showing mucilage-induced necrotic tissues compared to healthy ones. In particular, fragments sampled just next to the necrotic tissue displayed the highest levels of SOD and LPO, indicating that harmful oxidative damage was in progress, especially in portions neighboring the mucilage colonization. In this context, the up-regulation of the antioxidant mechanisms might represent a defense and a barrier from hypoxic or anoxic conditions created by mucilage overgrowth or by the invasion of toxic organisms embedded in the mucilaginous aggregates. On the contrary, the cellular protein homeostasis, analyzed by the expression of the 60-kDa Heat shock protein (Hsp60), was not altered by the mucilage. This analysis contributes to provide new insights into the cellular and molecular response of gorgonians to a stress source whose effects are likely to worsen in a climate change scenario.