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

Author:

Sukhotin Alexey12ORCID,Fokina Natalia3,Ruokolainen Tatiana3,Bock Christian4,Pörtner Hans-Otto45,Lannig Gisela4

Affiliation:

1. White Sea Biological Station, Zoological Institute of Russian Academy of Sciences, Saint-Petersburg, 199034, Russia

2. Saint-Petersburg State University, Saint-Petersburg, Russia

3. Institute of Biology, Karelian Research Centre of Russian Academy of Sciences, Petrozavodsk, Russia

4. Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Bremerhaven, Germany

5. University of Bremen, Bremen, Germany

Abstract

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 that 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 Mytilus edulis 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.

Funder

Russian Foundation for Basic Research

Hanse-Wissenschaftskolleg

Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research

Publisher

The Company of Biologists

Subject

Insect Science,Molecular Biology,Animal Science and Zoology,Aquatic Science,Physiology,Ecology, Evolution, Behavior and Systematics

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