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First published online April 26, 2005
Journal of Experimental Biology 208, 1593-1599 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01482

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Review article: Basal metabolic rate and cellular energetics

Membranes and the setting of energy demand

A. J. Hulbert^1,2,* and P. L. Else^1,3

¹ Metabolic Research Centre, University of Wollongong, Wollongong, NSW 2522, Australia
² School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia
³ Department of Biomedical Sciences, University of Wollongong, Wollongong, NSW 2522, Australia

^* Author for correspondence (e-mail: hulbert{at}uow.edu.au)

Accepted 30 December 2004

Summary

In his classic 1961 book, The Fire of Life, Max Kleiber presented a critique of the theories advanced to explain the BMR-body size relationship. One of the theories he dismissed was that the chemical composition of animals varies with body size. Since this time, however, much has been learned about the make-up of BMR in different animals as well as the chemical composition of different-sized animals. Specifically, in recent years it has become obvious that mammal species and bird species do vary in chemical composition in a systematic manner associated with the body size of the species. Small mammal and bird species have cellular membranes that are predominantly polyunsaturated, and as mammal and bird species increase in size, their cellular membranes become progressively less polyunsaturated. Since Kleiber's time, it has also become obvious that a substantial amount of the energy turnover of BMR is associated with the activity of membrane processes, specifically the maintenance of trans-membrane gradients, such as the Na⁺ gradient across the plasmalemmal membrane and the H⁺ gradient across the mitochondrial inner membrane. The variation in both membrane composition and membrane processes associated with body size variation in metabolic rate has been combined in the `membrane pacemaker' theory of metabolism. This theory proposes that: (1) membrane-associated activities are significant and dominant components of BMR; (2) when BMR varies among species, all the activities that constitute BMR vary in unison; (3) species with high mass-specific BMR have highly polyunsaturated membranes while those with low BMR have less polyunsaturation of their membranes; (4) highly polyunsaturated membranes have distinctive physical properties that cause the proteins in the membranes to have a high molecular activity, and this results in higher rates of metabolism of cells, tissues and, consequently, the whole animal. Evidence supporting this theory is both correlative and experimental. Manipulation of membrane composition changes the molecular activity of membrane proteins. These differences in membrane composition may also represent a link between metabolism and aging. They probably explain the lifespan-body size relationship in mammals and birds and also the mammal-bird difference in lifespan.

Key words: basal metabolic rate, lifespan, membrane lipid, sodium pump, docosahexaenoic acid

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