Abstract
Polyunsaturated fatty acids (PUFA) have a multitude of health effects. Their incorporation into membrane phospholipids (PL) is generally believed to depend directly on dietary influx. PL influence transmembrane protein activity and thus can compensate temperature effects; e.g. PL n-6 PUFA are thought to stabilize heart function at low body temperature (Tb), whereas long chain (>C18) n-3 PUFA may boost oxidative capacity. We found substantial remodeling of membranes in free-living alpine marmots which was largely independent of direct dietary supply. Organ PL n-6 PUFA and n-6 to n-3 ratios were highest at onset and end of hibernation after rapid increases during a brief transitional period prior to hibernation. In contrast, longer chain PL n-3 PUFA content was low at end of summer but maximal at end of hibernation. After termination of hibernation in spring, these changes in PL composition were rapidly reversed. Our results demonstrate selective trafficking of PUFA within the body, probably governed by a circannual endogenous rhythm, as hibernating marmots were in winter burrows isolated for seven months from food and external cues signaling the approaching spring. High concentrations of PL n-6 PUFA throughout hibernation are in line with their hypothesized function of boosting SERCA 2a activity at low Tb. Furthermore, we found increasing rate of rewarming from torpor during winter indicating increasing oxidative capacity that could be explained by the accumulation of long-chain PL n-3 PUFA. It may serve to minimize the time necessary for rewarming despite the increasing temperature range to be covered, because rewarming is a period of highest metabolic rate and hence production of reactive oxygen species. Considering the importance of PUFA for health our results may have important biomedical implications, as seasonal changes of Tb and associated remodeling of membranes are not restricted to hibernators but presumably common among endothermic organisms.
Highlights
Cellular membranes contain variable amounts of essential polyunsaturated fatty acids (PUFA), generally believed to depend directly on dietary influx and tissue specific differences [1,2,3,4,5,6,7,8]
Function of seasonal transitions If a membrane rich in n-6 PUFA is necessary for maintaining heart function in hibernating mammals [21], it should be available when an animal undergoes the first bout of torpor
Other unexpected findings are the selective transfer of LA from white adipose tissue (WAT) into organ PL in preparation for winter and removal of PUFA from PL when returning to a life at high Tb
Summary
Cellular membranes contain variable amounts of essential polyunsaturated fatty acids (PUFA), generally believed to depend directly on dietary influx and tissue specific differences [1,2,3,4,5,6,7,8]. Rapid and diet-independent adjustments of membrane composition in response to changing cell temperature are well known for ectotherms [9,10]. This so-called ‘‘homeoviscous adaptation’’ is thought to maintain membrane integrity at lower temperatures. Endothermic organisms show fluctuations in body temperature (Tb) on a daily and seasonal basis, carried to the extreme by hibernators and daily heterotherms [11,12,13]. Integration of PUFA into phospholipids (PL) in order to cope with lower cell temperature may be conserved in endotherms. Studies in the laboratory found such changes in hibernating mammals [14,15,16], and in deer mice exhibiting a higher propensity for daily torpor induced by short photoperiod [17]
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