Exposure to anoxia leads to rapid ATP depletion, alters metabolic pathways and exacerbates succinate accumulation. Upon re-oxygenation, the preferential oxidation of accumulated succinate most often impairs mitochondrial function. Few species can survive prolonged periods of hypoxia and anoxia at tropical temperatures and those that do may rely on mitochondria plasticity in response to disruptions to oxygen availability. Two carpet sharks, the epaulette shark (Hemiscyllium ocellatum; ES) and the grey carpet shark (Chiloscyllium punctatum; GCS) display different adaptive responses to prolonged anoxia: while the ES enters energy conserving metabolic depression, the GCS temporarily elevates its haematocrit prolonging oxygen delivery. High-resolution respirometry was used to investigate mitochondrial function in the cerebellum, a highly metabolically active organ that is oxygen sensitive and vulnerable to injury after anoxia/re-oxygenation (AR).
Succinate was titrated into cerebellar preparations in vitro, with or without pre-exposure to AR, then the activity of mitochondrial complexes was examined. Like most vertebrates, GCS mitochondria significantly increased succinate oxidation rates, with impaired complex I function post-AR. In contrast, ES mitochondria inhibited succinate oxidation rates and both complex I and II capacities were conserved, resulting in preservation of oxidative phosphorylation capacity post-AR.
Divergent mitochondrial plasticity elicited by elevated succinate post A/R parallels the inherently divergent physiological adaptations of these animals to prolonged anoxia, namely the absence (GCS) and presence of metabolic depression (ES). Since anoxia tolerance in these species also occurs at temperatures close to that of humans, examining their mitochondrial responses to AR could provide insights for novel interventions in clinical settings.
