Abstract
Hibernating arctic ground squirrels (Urocitellus parryii), overwintering in frozen soils, maintain large gradients between ambient temperature (T(a)) and body temperature (T(b)) by substantially increasing metabolic rate during torpor while maintaining a subzero T(b). We used quantitative reverse-transcription PCR (qRT-PCR) to determine how the expression of 56 metabolic genes was affected by season (active in summer vs hibernating), metabolic load during torpor (imposed by differences in T(a): +2 vs -10°C) and hibernation state (torpid vs after arousal). Compared with active ground squirrels sampled in summer, liver from hibernators showed increased expression of genes associated with fatty acid catabolism (CPT1A, FABP1 and ACAT1), ketogenesis (HMGCS2) and gluconeogenesis (PCK1) and decreased expression of genes associated with fatty acid synthesis (ACACB, SCD and ELOVL6), amino acid metabolism, the urea cycle (PAH, BCKDHA and OTC), glycolysis (PDK1 and PFKM) and lipid metabolism (ACAT2). Stage of hibernation (torpid vs aroused) had a much smaller effect, with only one gene associated with glycogen synthesis (GSY1) in liver showing consistent differences in expression levels between temperature treatments. Despite the more than eightfold increase in energetic demand associated with defending T(b) during torpor at a T(a) of -10 vs +2°C, transcript levels in liver and brown adipose tissue differed little. Our results are inconsistent with a hypothesized switch to use of non-lipid fuels when ambient temperatures drop below freezing.
Highlights
Hibernation in mammals is characterized by a suite of interconnected morphological, physiological, molecular and behavioral changes that enable individuals to persist in environments with seasonal or unpredictable shortages in energy supply
The arctic ground squirrel (Urocitellus parryii) may exhibit the most extreme hibernation physiology known: it is capable of supercooling its core body temperature (Tb) to –2.9°C [the lowest Tb adopted by any mammal (Barnes, 1989)] and surviving winters as long as 250 days sequestered in frozen hibernacula
Body temperature The mean abdominal temperature of torpid arctic ground squirrels exposed to ambient temperatures of –10°C was –0.7±0.2°C, significantly lower than that of squirrels hibernating at +2°C (2.2±0.3°C, F1,8 316.3, P
Summary
Hibernation in mammals is characterized by a suite of interconnected morphological, physiological, molecular and behavioral changes that enable individuals to persist in environments with seasonal or unpredictable shortages in energy supply. Through metabolic inhibition and temperature or Q10 effects on enzyme kinetics, arctic ground squirrels suppress metabolic rates during torpor to 0.01 ml O2 g–1 h–1 or 2% of basal levels for up to 24 days at a time (Karpovich et al, 2009; Buck and Barnes, 2000), levels that are comparable to the minimum rates of metabolism observed during torpor in all hibernators (reviewed in Geiser and Ruf, 1995) In their high latitude habitats, arctic ground squirrels experience natural thermal conditions that are far more severe in winter than conditions experienced by temperate or alpine-dwelling hibernators. Buck and Barnes observed a concomitant increase in respiratory quotient (RQ) with decreasing Ta below 0°C, indicative of a shift from exclusive catabolism of lipids when thermoneutral
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