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Seasonal acclimatization: From the organism to cellular membranes
Mammals and birds living in seasonal environments face during winter a two-fold challenge: The energetic cost of maintaining a high body temperature (Tb) is higher at lower ambient temperatures while food availability and quality is poor. Hibernators and daily heterotherms cope with these challenges by switching to fat reserves as the major metabolic fuel, reducing foraging activity, size of organs, and, most importantly, by abandoning maintenance of a high body temperature (Tb). We found similar reactions in several “non-hibernating” large mammals, except that Tb changes were substantial only in peripheral body parts. Reduction of Tb is preceded by incorporation of essential polyunsaturated fatty acids (PUFA) into phospholipids, apparently to compensate for temperature (Arrhenius) effects on membrane-bound enzymes, with specific roles for different PUFA. For instance, membranes of hibernators rich in omega-6 linoleic acid (LA) boost Ca++ handling in myocytes, whereas omega-3 docosahexaenoic acid seem to improve ATP production but deteriorate Ca++ handling, as does LA-derived arachidonic acid. I conclude that seasonal acclimatization, in particular hypometabolism and voluntary hypothermia seem to be ubiquitous among endotherms, as is associated membrane remodeling. Specific effects of PUFA suggest trade-offs determining the state-dependent optimization of the fatty acid composition of membranes.
Giroud S, Frare C, Strijkstra A, Boerema A, Arnold W, Ruf T (2013) Membrane phospholipid fatty acid composition regulates cardiac SERCA activity in a hibernator, the Syrian hamster (Mesocricetus auratus). PLoS One 8: e63111.
Arnold W, Ruf T, Frey-Roos F, Bruns U (2011) Diet-independent remodeling of cellular membranes precedes seasonally changing body temperature in a hibernator. PLoS One 6: e18641.
Turbill C, Ruf T, Mang T, Arnold W (2011) Regulation of heart rate and rumen temperature in red deer: effects of season and food intake. J Exp Biol 214, 963-970.
Signer C, Ruf T, Arnold W (2011) Hypometabolism and basking: The strategies of Alpine ibex to endure harsh over-wintering conditions. Funct Ecol 25, 537-547.
Ruf T, Arnold W (2008). Effects of polyunsaturated fatty acids on hibernation and torpor: a review and hypothesis. Am J Physiol Regul Integr Comp Physiol. 294, R1044-R1052.
Arnold W, Ruf T, Kuntz R (2006) Seasonal adjustment of energy budget in a large wild mammal, the Przewalski horse (Equus ferus przewalskii) II. Energy expenditure. J Exp Biol 209, 4566-4573.