Does the membrane pacemaker theory of metabolism explain the size dependence of metabolic rate in marine mussels?

• Published in: Journal of experimental biology Vol. 220; no. Pt 8; pp. 1423 - 1434
• Main Authors: Sukhotin, Alexey, Fokina, Natalia, Ruokolainen, Tatiana, Bock, Christian, Pörtner, Hans-Otto, Lannig, Gisela
• Format: Journal Article
• Language: English
• Published: England The Company of Biologists Ltd 15-04-2017
• Subjects: Allometry; Animal metabolism; Animals; Basal Metabolism; Birds; Body mass; Body Size; Cell size; Cells, Cultured; Energy conservation; Fatty acids; Fatty Acids - metabolism; Gills - anatomy & histology; Gills - cytology; Gills - enzymology; Gills - metabolism; Heart Rate; Interspecific; Lipid composition; Mammals; Membrane permeability; Membranes; Metabolic rate; Metabolism; Mitochondria; Mollusks; Mussels; Mytilus edulis; Mytilus edulis - anatomy & histology; Mytilus edulis - cytology; Mytilus edulis - enzymology; Mytilus edulis - metabolism; Oxygen Consumption; Permeability; Phospholipids; Phospholipids - metabolism; Respiration; Scaling; Heart rate; Enzyme activity; Allometric scaling; Fatty acids; Cardiac magnetic resonance imaging; Cells
• ISSN: 0022-0949; 1477-9145
• DOI: 10.1242/jeb.147108

According to the membrane pacemaker theory of metabolism (MPT), allometric scaling of metabolic rate in animals is determined by the composition of cellular and mitochondrial membranes, which changes with body size in a predictable manner. MPT has been elaborated from interspecific comparisons in mammals. It projects that the degree of unsaturation of membrane phospholipids decreases in larger organisms, thereby lowering ion permeability of the membranes and making cellular, and thus whole-animal metabolism more efficient. Here, we tested the applicability of the MPT to a marine ectotherm, the mussel
at the intraspecific level. We determined effects of body mass on whole-organism, tissue and cellular oxygen consumption rates, on heart rate, metabolic enzyme activities and on the lipid composition of membranes. In line with allometric patterns, the organismal functions and processes such as heart rate, whole-animal respiration rate and phospholipid contents showed a mass-dependent decline. However, the allometry of tissue and cellular respiration and activity of metabolic enzymes was poor; fatty acid unsaturation of membrane phospholipids of gill tissue was independent of animal size. It is thus conceivable that most of the metabolic allometry observed at the organismal level is determined by systemic functions. These whole-organism patterns may be supported by energy savings associated with growing cell size but not by structural changes in membranes. Overall, the set of processes contributing to metabolic allometry in ectotherms may differ from that operative in mammals and birds, with a reduced involvement of the mechanisms proposed by the MPT.