Hypercarbia enhances metabolic thermotolerance of the cold temperate nototheniod Notothenia angustata

Background: Many Antarctic notothenioid fish are considered losers of global change, due to their low thermal tolerance and lack of regulative mechanisms that enhance physiological plasticity. The Austral nototheniid congener Notothenia angustata provides an alternative model to explore the effects of ocean acidification and warming, as it inhabits cold temperate to subpolar waters. It is a eurythermal species, with greater capacities for thermal acclimation relative to Antarctic congeners, and therefore presents a useful model against which Antarctic notothenioids can be contrasted. Methods: We investigated the long-term effects of hypercarbic acclimation on whole animal and cardiac mitochondrial function for the Austral nototheniid Notothenia angustata. Fish were acclimated under hypercarbic (0.2 kPa CO2, 15 days, n=6) and normocarbic conditions (control 0.04 kPa CO2, n=10). Routine metabolic rates (RMR) were determined with acute increases in temperature (3°C/d) under normocarbic and hypercarbic conditions. Mitochondrial function was then tested within permeabilised cardiac muscle fibres, and assays conducted in normocarbic (0.04 kPa CO2) and hypercarbic (3.0 kPa CO2) media at 9, 15 and 21°C. Metabolic profiles were determined in red skeletal muscle. Findings: Whole animal critical temperature thresholds occurred below 19°C for normocarbic exposed fish, while acutely hypercarbic exposed fish maintained routine metabolic rates up to 21oC. Overall mitochondria mirrored the responses of acutely exposed whole animals, with an increased mitochondrial performance in fish acclimated to chronic hypercarbia. Chronically hypercarbic exposed animals also exhibited altered metabolomes of red muscle, but not liver with apparent increases in metabolites consistent with enhanced anaerobic metabolism and elevated contents of histidine and tryptophan that may contribute to acid-base buffering. Conclusions: Overall enhanced cardiac mitochondrial capacities coincide with increasing hypercarbic and elevated temperature tolerance. This response suggests sufficient metabolic plasticity for Austral nototheniids to acclimate to a warming and acidifying ocean, which has not been observed to that extent in Antarctic notothenioids

Mitochondrial Acclimation Capacities to Ocean Warming and Acidification Are Limited in the Antarctic Nototheniid Fish, Notothenia rossii and Lepidonotothen squamifrons

Antarctic notothenioid fish are characterized by their evolutionary adaptation to the cold, thermostable Southern Ocean, which is associated with unique physiological adaptations to withstand the cold and reduce energetic requirements but also entails limited compensation capacities to environmental change. This study compares the capacities of mitochondrial acclimation to ocean warming and acidification between the Antarctic nototheniid Notothenia rossii and the sub-Antarctic Lepidonotothen squamifrons, which share a similar ecology, but different habitat temperatures. After acclimation of L. squamifrons to 9°C and N. rossii to 7°C (normocapnic/hypercapnic, 0.2 kPa CO2/2000 ppm CO2) for 4-6 weeks, we compared the capacities of their mitochondrial respiratory complexes I (CI) and II (CII), their P/O ratios (phosphorylation efficiency), proton leak capacities and mitochondrial membrane fatty acid compositions. Our results reveal reduced CII respiration rates in warm-acclimated L. squamifrons and cold hypercapnia-acclimated N. rossii. Generally, L. squamifrons displayed a greater ability to increase CI contribution during acute warming and after warm-acclimation than N. rossii. Membrane unsaturation was not altered by warm or hypercapnia-acclimation in both species, but membrane fatty acids of warm-acclimated L. squamifrons were less saturated than in warm normocapnia-/hypercapnia-acclimated N. rossii. Proton leak capacities were not affected by warm or hypercapnia-acclimation of N. rossii. We conclude that an acclimatory response of mitochondrial capacities may include higher thermal plasticity of CI supported by enhanced utilization of anaplerotic substrates (via oxidative decarboxylation reactions) feeding into the citrate cycle. L. squamifrons possesses higher relative CI plasticities than N. rossii, which may facilitate the usage of energy efficient NADH-related substrates under conditions of elevated energy demand, possibly induced by ocean warming and acidification. The observed adjustments of electron transport system complexes with a higher flux through CI under warming and acidification suggest a metabolic acclimation potential of the sub-Antarctic L. squamifrons, but only limited acclimation capacities for N. rossii