Abstract
BackgroundThe performance of elite breath hold divers (BHD) includes static breath hold for more than 11 minutes, swimming as far as 300 m, or going below 250 m in depth, all on a single breath of air. Diving mammals are adapted to sustain oxidative metabolism in hypoxic conditions through several metabolic adaptations, including improved capacity for oxygen transport and mitochondrial oxidative phosphorylation in skeletal muscle. It was hypothesized that similar adaptations characterized human BHD. Hence, the purpose of this study was to examine the capacity for oxidative metabolism in skeletal muscle of BHD compared to matched controls.MethodsBiopsies were obtained from the lateral vastus of the femoral muscle from 8 Danish BHD and 8 non-diving controls (Judo athletes) matched for morphometry and whole body VO2max. High resolution respirometry was used to determine mitochondrial respiratory capacity and leak respiration with simultaneous measurement of mitochondrial H2O2 emission. Maximal citrate synthase (CS) and 3-hydroxyacyl CoA dehydrogenase (HAD) activity were measured in muscle tissue homogenates. Western Blotting was used to determine protein contents of respiratory complex I-V subunits and myoglobin in muscle tissue lysates.ResultsMuscle biopsies of BHD revealed lower mitochondrial leak respiration and electron transfer system (ETS) capacity and higher H2O2 emission during leak respiration than controls, with no differences in enzyme activities (CS and HAD) or protein content of mitochondrial complex subunits myoglobin, myosin heavy chain isoforms, markers of glucose metabolism and antioxidant enzymes.ConclusionWe demonstrated for the first time in humans, that the skeletal muscles of BHD are characterized by lower mitochondrial oxygen consumption both during low leak and high (ETS) respiration than matched controls. This supports previous observations of diving mammals demonstrating a lower aerobic mitochondrial capacity of the skeletal muscles as an oxygen conserving adaptation during prolonged dives.
Highlights
Diving mammals are adapted to sustained aerobic metabolism under hypoxic conditions, and relative to comparable terrestrial mammals, skeletal muscles of pinnipeds have higher volume density of mitochondria [Vv(mt)] and correspondingly higher citrate synthase (CS) activity, higher beta-hydroxyacyl CoA dehydrogenase (HAD) activity and a higher capacity for fatty acid catabolism for aerobic ATP production [1]
The purpose of this study was to examine the capacity for oxidative metabolism in skeletal muscle of breath hold divers (BHD) compared to matched controls
We demonstrated for the first time in humans, that the skeletal muscles of BHD are characterized by lower mitochondrial oxygen consumption both during low leak and high (ETS) respiration than matched controls
Summary
Diving mammals are adapted to sustained aerobic metabolism under hypoxic conditions, and relative to comparable terrestrial mammals, skeletal muscles of pinnipeds (seals and sea lions) have higher volume density of mitochondria [Vv(mt)] and correspondingly higher citrate synthase (CS) activity, higher beta-hydroxyacyl CoA dehydrogenase (HAD) activity and a higher capacity for fatty acid catabolism for aerobic ATP production [1]. The oxidative phosphorylation (OXPHOS) capacity of the northern elephant seal (NES) muscle is generally lower than in humans [2], but the difference is leak respiration in NES is less with lipid-based substrates (palmitoylcarnitine + malate) than with pyruvate. This supports that a relatively low mitochondrial capacity with a preference for lipid oxidation contributes to an improved diving performance. Together, these metabolic features expand the animals dive capacity, while relying primarily on oxygen stored in blood and muscle. The purpose of this study was to examine the capacity for oxidative metabolism in skeletal muscle of BHD compared to matched controls
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