From Africa to Antarctica: Exploring the Metabolism of Fish Heart Mitochondria Across a Wide Thermal Range.

Florence Hunter-Manseau,H William Detrich,Nathalie R Le François,Pierre U Blier,Christian Nozais,France Dufresne,Véronique Desrosiers

doi:10.3389/fphys.2019.01220

Abstract

The thermal sensitivity of ectotherms is largely dictated by the impact of temperature on cellular bioenergetics, particularly on mitochondrial functions. As the thermal sensitivity of bioenergetic pathways depends on the structural and kinetic properties of its component enzymes, optimization of their collective function to different thermal niches is expected to have occurred through selection. In the present study, we sought to characterize mitochondrial phenotypic adjustments to thermal niches in eight ray-finned fish species occupying a wide range of thermal habitats by comparing the activities of key mitochondrial enzymes in their hearts. We measured the activity of four enzymes that control substrate entrance into the tricarboxylic acid (TCA) cycle: pyruvate kinase (PK), pyruvate dehydrogenase complex (PDHc), carnitine palmitoyltransferase (CPT), and hydroxyacyl-CoA dehydrogenase (HOAD). We also assayed enzymes of the electron transport system (ETS): complexes I, II, I + III, and IV. Enzymes were assayed at five temperatures (5, 10, 15, 20, and 25°C). Our results showed that the activity of CPT, a gatekeeper of the fatty acid pathway, was higher in the cold-water fish than in the warmer-adapted fish relative to the ETS (complexes I and III) when measured close to the species optimal temperatures. The activity of HOAD showed a similar pattern relative to CI + III and thermal environment. By contrast, PDHc and PK did not show the similar patterns with respect to CI + III and temperature. Cold-adapted species had high CIV activities compared to those of upstream complexes (I, II, I + III) whereas the converse was true for warm-adapted species. Our findings reveal a significant variability of heart mitochondrial organization among species that can be linked to temperature adaptation. Cold-adapted fish do not appear to compensate for PDHc activity but likely adjust fatty acids oxidation through higher activities of CPT and HOAD relative to complexes I + III.

Highlights

Mitochondrial ATP production depends on the interactions of various metabolic pathways
The capacity to feed tricarboxylic acid (TCA) by fatty acid oxidation, appears higher in cold-adapted fish since the activities of carnitine palmitoyltransferase (CPT), relative to CI + CIII are greater for the three species with lowest optimal temperatures when compared to four of the five species adapted to higher temperatures (Figure 2A)
Prior work on the thermal sensitivity of mitochondrial metabolism in fish have often focused on enzymes of OXPHOS, the pyruvate dehydrogenase complex (PDHc) and some enzymes of TCA cycle such as CS, but have largely neglected fatty acid oxidation pathways (Takeuchi et al, 2009; Lemieux et al, 2010a,b; Blier et al, 2014; but see Ekström et al, 2017)

Summary

Introduction

Mitochondrial ATP production depends on the interactions of various metabolic pathways. The thermal sensitivity of state 3 mitochondrial respiration in the heart of the Atlantic wolffish (Anarhichas lupus) has been shown to be similar to that of the pyruvate dehydrogenase complex (PDHc) but to differ from the sensitivity of other mitochondrial enzymes (Lemieux et al, 2010a,b) This has led authors to suggest that state 3 may be limited at low temperature in part by the activity of PDHc when mitochondria are fed with pyruvate. Further work on Drosophila simulans revealed an excess of complex IV (CIV) capacity at low temperature, indicating upstream limitation in the electron transport system (ETS) with PDHc as the likely cause of this limitation (Pichaud et al, 2010, 2011) These authors further noted that Drosophila CIV controlled mitochondrial metabolism at high temperature but not at low temperature. These results support the hypothesis that an excess of CIV activity at low temperature occurs due to a rate-limiting step upstream in ectotherms (Blier et al, 2014)

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