Selective upregulation of lipid metabolism in skeletal muscle of foraging juvenile king penguins: an integrative study

Abstract

The passage from shore to marine life of juvenile penguins represents a major energetic challenge to fuel intense and prolonged demands for thermoregulation and locomotion. Some functional changes developed at this crucial step were investigated by comparing pre-fledging king penguins with sea-acclimatized (SA) juveniles (Aptenodytes patagonicus). Transcriptomic analysis of pectoralis muscle biopsies revealed that most genes encoding proteins involved in lipid transport or catabolism were upregulated, while genes involved in carbohydrate metabolism were mostly downregulated in SA birds. Determination of muscle enzymatic activities showed no changes in enzymes involved in the glycolytic pathway, but increased 3-hydroxyacyl-CoA dehydrogenase, an enzyme of the β-oxidation pathway. The respiratory rates of isolated muscle mitochondria were much higher with a substrate arising from lipid metabolism (palmitoyl-L-carnitine) in SA juveniles than in terrestrial controls, while no difference emerged with a substrate arising from carbohydrate metabolism (pyruvate). In vivo, perfusion of a lipid emulsion induced a fourfold larger thermogenic effect in SA than in control juveniles. The present integrative study shows that fuel selection towards lipid oxidation characterizes penguin acclimatization to marine life. Such acclimatization may involve thyroid hormones through their nuclear beta receptor and nuclear coactivators.

Figure 1.

Respiration rates of mitochondria isolated from pectoralis muscle of never-immersed (NI, open bars) or sea-acclimatized (SA, filled bars) king penguin juveniles. Oxygen uptake was determined with a Clark oxygen electrode (Rank Brother LTD) placed into a glass chamber thermostated at 38°C. State 4 was initiated with either: (a) 5 mM pyruvate and 2.5 mM malate, (b) 50 µM palmitoyl-l-carnitine and 2.5 mM malate, (c) 5 mM succinate in the presence of 5 µM rotenone. Phosphorylating respiration (state 3) was initiated with 500 µM ADP. Non-phosphorylating respiration (state 4) was obtained by addition of 1 µg ml⁻¹ oligomycin and fully uncoupled respiration was obtained with 2 µM FCCP. Means ± s.e.m. *p < 0.05 versus NI birds.

Figure 2.

Metabolic response to triglyceride (TG) infusion in NI (open symbols) or SA (filled symbols) king penguin immatures. (a) Changes in metabolic rate (MR) at 10°C (thermoneutrality) in NI (n = 5) or SA (n = 6) birds. Horizontal black lines represent infusions of either saline or TG emulsion for 30 min. Mean body mass was 9.5 ± 0.2 kg in NI and 8.9 ± 0.3 kg in SA birds. Means ± s.e.m. *p < 0.05 indicates that all of the MR values after the end of TG infusion were significantly different from basal level in SA birds. Shaded areas represent the points incorporated into the AUC and dashed horizontal lines mark the level of resting MR determined after saline infusion. (b) Bars represent the integrated total effect of TG infusion on MR (area under the curve) in NI (open bar) or SA (filled bar) juveniles. Means ± s.e.m. *p < 0.05 significantly different from NI birds. Open diamonds with solid line, NI; filled diamonds with solid line, SA.

Figure 3.

Changes in plasma lipid levels in NI (open symbols, n = 5) or SA (filled symbols, n = 6) king penguin juveniles. (a) Plasma TG levels. (b) Plasma non-esterified fatty acid (NEFA) levels. Black lines represent infusions of either saline solution or TG emulsion for 30 min. Blood aliquots were taken at different time point (0, 10, 45, 110, 120, 130, 140, 150, 160, 170, 185, 215, 245, 305 min). Values are means ± s.e.m.