Spectral measurements of mitochondrial thermal tolerance in failing hearts of temperate and tropical perciformes

As marine ectotherms approach critical thermal limits, hearts are the first organs to fail. Previously, we reported that at sub-threshold temperatures for heart failure: heart mitochondria increased O ₂ demand and were not fully coupled to oxidative phosphorylation, failing to supply sufficient ATP to drive the beating heart. While mitochondrial uncoupling in response to thermal stress predicts heart failure, such responses have been only been assessed within isolated fibres in the presence of saturating substrates and oxygen in vitro . Here, we assess mitochondrial response to thermal stress ex vivo , within beating hearts exposed to ramped thermal stress by controlling perfusate temperature. Mitochondrial reduction-oxidation states were measured spectrophotometrically in two perciforms (i) the temperate Notolabrus fucicola (acclimated at 18ºC); and (ii) the tropical, Scarus ghobban (acclimated at 25ºC).In N. fucicola , synchronised beats and electro-activities of hearts increased gradually following temperature elevation, then showed an inflection with a decrease occurring at 24.7ºC, mediating rapid heart failure at 28.1ºC. In contrast, the heartbeat of S. ghobban suddenly weakened at 31.8ºC, became arrhythmic and failed at 38.2 ºC. In both species, myoglobin saturation and the spectra of mitochondrial cytochromes fluctuated in synchrony with their weakening heartbeat. Cytochrome b absorbance analysis revealed loss of mitochondrial membrane potential and flavine mononucleotide release suggests loss of mitochondrial complex I capacity. This study showcases heart mitochondrial responses to thermal stress ex vivo , reinforcing the hypothesis that mitochondrial dysfunction contributes to heart failure near the upper thermal limits of habitat in both tropical and temperate adult perciform species.