title: High fatty acid oxidation capacity and phosphorylation control despite elevated leak and reduced respiratory capacity in northern elephant seal muscle mitochondria.
abstract: Northern elephant seals (Mirounga angustirostris) are extreme, hypoxia-adapted endotherms that rely largely on aerobic metabolism during extended breath-hold dives in near-freezing water temperatures. While many aspects of their physiology have been characterized to account for these remarkable feats, the contribution of adaptations in the aerobic powerhouses of muscle cells, the mitochondria, are unknown. In the present study, the ontogeny and comparative physiology of elephant seal muscle mitochondrial respiratory function was investigated under a variety of substrate conditions and respiratory states. Intact mitochondrial networks were studied by high-resolution respirometry in saponin-permeabilized fiber bundles obtained from primary swimming muscles of pup, juvenile and adult seals, and compared with fibers from adult human vastus lateralis. Results indicate that seal muscle maintains a high capacity for fatty acid oxidation despite a progressive decrease in total respiratory capacity as animals mature from pups to adults. This is explained by a progressive increase in phosphorylation control and fatty acid utilization over pyruvate in adult seals compared with humans and seal pups. Interestingly, despite higher indices of oxidative phosphorylation efficiency, juvenile and adult seals also exhibit a ~50% greater capacity for respiratory 'leak' compared with humans and seal pups. The ontogeny of this phenotype suggests it is an adaptation of muscle to the prolonged breath-hold exercise and highly variable ambient temperatures experienced by mature elephant seals. These studies highlight the remarkable plasticity of mammalian mitochondria to meet the demands for both efficient ATP production and endothermy in a cold, oxygen-limited environment.
authors.affiliation: Mitochondrial Physiology Laboratory, Colorado State University, Fort Collins, CO 80523-1582, USA Health and Exercise Science, Colorado State University, Fort Collins, CO 80523-1582, USA Cell and Molecular Biology Program, Colorado State University, Fort Collins, CO 80523-1582, USA Adam.Chicco@colostate.edu.
authors.forename: Adam J
authors.initials: AJ
authors.lastname: Chicco
authors.affiliation: Mitochondrial Physiology Laboratory, Colorado State University, Fort Collins, CO 80523-1582, USA Cell and Molecular Biology Program, Colorado State University, Fort Collins, CO 80523-1582, USA.
authors.forename: Catherine H
authors.initials: CH
authors.lastname: Le
authors.affiliation: Extreme Physiology Laboratory, Colorado State University, Fort Collins, CO 80523-1582, USA Department of Biology, Colorado State University, Fort Collins, CO 80523-1582, USA.
authors.forename: Amber
authors.initials: A
authors.lastname: Schlater
authors.affiliation: Mitochondrial Physiology Laboratory, Colorado State University, Fort Collins, CO 80523-1582, USA Health and Exercise Science, Colorado State University, Fort Collins, CO 80523-1582, USA.
authors.forename: Alex
authors.initials: A
authors.lastname: Nguyen
authors.affiliation: Mitochondrial Physiology Laboratory, Colorado State University, Fort Collins, CO 80523-1582, USA Health and Exercise Science, Colorado State University, Fort Collins, CO 80523-1582, USA.
authors.forename: Spencer
authors.initials: S
authors.lastname: Kaye
authors.affiliation: Health and Exercise Science, Colorado State University, Fort Collins, CO 80523-1582, USA.
authors.forename: Joseph W
authors.initials: JW
authors.lastname: Beals
authors.affiliation: Health and Exercise Science, Colorado State University, Fort Collins, CO 80523-1582, USA.
authors.forename: Rebecca L
authors.initials: RL
authors.lastname: Scalzo
authors.affiliation: Health and Exercise Science, Colorado State University, Fort Collins, CO 80523-1582, USA.
authors.forename: Christopher
authors.initials: C
authors.lastname: Bell
authors.affiliation: Department of Visceral, Transplant and Thoracic Surgery, Medical University of Innsbruck, 6020 Innsbruck, Austria.
authors.forename: Erich
authors.initials: E
authors.lastname: Gnaiger
authors.affiliation: Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, Santa Cruz, CA 95064, USA.
authors.forename: Daniel P
authors.initials: DP
authors.lastname: Costa
authors.affiliation: Department of Biology, Sonoma State University, Rohnert Park, CA 94928, USA.
authors.forename: Daniel E
authors.initials: DE
authors.lastname: Crocker
authors.affiliation: Extreme Physiology Laboratory, Colorado State University, Fort Collins, CO 80523-1582, USA Department of Biology, Colorado State University, Fort Collins, CO 80523-1582, USA.
authors.forename: Shane B
authors.initials: SB
authors.lastname: Kanatous
mesh_terms: D000222:Adaptation, Physiological; D000328:Adult; D000818:Animals; D019069:Cell Respiration; D004242:Diving; D005227:Fatty Acids / Q000378:metabolism; D006801:Humans; D008297:Male; D008931:Mitochondria, Muscle / Q000502:physiology*; D018482:Muscle, Skeletal / Q000502:physiology*; D010084:Oxidation-Reduction; D010766:Phosphorylation; D046048:Seals, Earless / Q000502:physiology*; D055815:Young Adult
chemical_list: D005227:Fatty Acids
keywords: Adaptive thermogenesis; Diving mammals; Hypoxia adaptations; Mitochondria