Oxygen conserving mitochondrial adaptations in the skeletal muscles of breath hold divers

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.

Skeletal muscle, haematological and splenic volume characteristics of elite breath-hold divers

“…The lack of mitochondrial content fibre-type difference in the ND is supported by Hoppeller (1986) findings who likewise reported a similar mitochondrial content across the muscle fibres of trained individuals (Saltin et al 1977). Additionally, our findings are in agreement with Kjeld et al (2018) who showed a similar citrate synthase maximal enzyme activity in EBHD with ND controls. Qualitative assessment of the relative myoglobin and mitochondrial protein distribution in muscle fibres revealed, a stronger fluorescence intensity and a homogenous distribution of myoglobin and mitochondria at the sub-sarcolemmal regions of type I muscle fibres in the EBHD compared with ND.…”

“…No between group differences in fibre type distribution (type I vs type II) were observed in the present study. This is consistent with earlier observations made in EBHD and swimmers (Gollnick et al 1972; Kjeld et al 2018). However, contrary to Bae et al (2003), we failed to report any between group FA differences.…”

“…Evidence suggest that skeletal muscle myoglobin expression and protein content increase in response to combined exercise and hypoxia (Terrados et al 1990; Kanatous et al 2009). However, Kjeld et al (2018) found no between-group differences in myoglobin content after Western Blot analyses of skeletal muscle homogenates in the m. vastus lateralis of male EBHD compared with matched controls. Although Western Blot methodology is useful, it does not provide information on the localisation and spatial distribution of proteins nor the relative distribution of proteins between muscle fibre types.…”

“…This blunted training response in muscle oxidative potential during hypoxia may be advantageous in a breath-hold diving context. Interestingly, a lower mitochondrial oxygen consumption during non-phosphorylating and uncoupled respiration was identified in the m. vastus lateralis of male EBHD compared with matched controls (Kjeld et al 2018). Therefore, the lower mitochondrial respiratory capacity may be important for oxygen conservation during prolonged dynamic breath-hold attempts.…”

“…haematocrit and haemoglobin) of elite breath-hold divers (EBHD) have been examined extensively in the literature (Richardson et al 2005; Ferretti et al 2012; Schagatay et al 2012; Fernadez et al 2017). In comparison, relatively few studies have investigated the skeletal muscle characteristics of EBHD (Bae et al 2003; Kjeld et al 2018).…”