Mitochondrial phenotypic flexibility enhances energy savings during winter fast in king penguin chicks

Abstract

Energy conservation is a key priority for organisms that live in environments with seasonal shortages in resource supplies or that spontaneously fast during their annual cycle. The aim of this study was to determine whether the high fasting endurance of winteracclimatized king penguin chicks (Aptenodytes patagonicus) is associated with an adjustment of mitochondrial bioenergetics in pectoralis muscle, the largest skeletal muscle in penguins. The rates of mitochondrial oxygen consumption, and ATP synthesis and mitochondrial efficiency (ATP/O ratio) were measured in winteracclimatized chicks. We used pyruvate/malate and palmitoyl-Lcarnitine/malate as respiratory substrates and results from naturally fasted chicks were compared to experimentally re-fed chicks. Bioenergetics analysis of pectoralis muscle revealed that mitochondria are on average 15% more energy efficient in naturally fasted than in experimentally fed chicks, indicating that fasted birds consume less nutrients to sustain their energy-demanding processes. We also found that moderate reductions in temperature from 38°C to 30°C further increase by 23% the energy coupling efficiency at the level of mitochondria, suggesting that king penguin chicks realize additional energy savings while becoming hypothermic during winter. It has been calculated that this adjustment of mitochondrial efficiency in skeletal muscle may contribute to nearly 25% of fasting-induced reduction in mass-specific metabolic rate measured in vivo. The present study shows that the regulation of mitochondrial efficiency triggers the development of an economical management of resources, which would maximize the conservation of endogenous fuel stores by decreasing the cost of living in fasted winteracclimatized king penguin chicks. KEY WORDS: Bird, Skeletal muscle, Mitochondria, Energy efficiency, Starvation INTRODUCTIONSpontaneous fast is a major characteristic of the annual cycle of sea birds when breeding or moulting on land, whereas they feed exclusively at sea. In situations where food is lacking or not used, the allocation of limited endogenous resources causes trade-offs between competing traits, such as reproduction, somatic growth and maintenance. During food deprivation, animals cannot maximize all of their life-history traits and must exhibit adaptive behavioural, physiological and biochemical responses to reduce metabolism and/or the cost of current activities in order to maintain biological value (Wang et al., 2006). Among sea birds, penguins, especially the Aptenodytes genus, which inhabits cold environments, have evolved to tolerate some of the greatest relative body mass losses and to survive several months of starvation, which can be up to 5 months in winter-acclimatized king penguin chicks (Cherel and Le Maho, 1985;Groscolas, 1990;McCue, 2010). RESEARCH ARTICLEKing penguin chicks (Aptenodytes patagonicus, Miller J. F. 1778) experience a severe nutritional shortage when left alone for a long period of time, and they may be fed infrequently or not at all by their p...

Variation in Metabolic Rate among Individuals Is Related to Tissue-Specific Differences in Mitochondrial Leak Respiration

“…Leak respiration in the liver was significantly greater in high-SMR individuals, while MMR was positively related to leak respiration in the muscle. These results are consistent with other studies comparing experimental groups or taxa that have shown animals with higher metabolism to have higher leak respiration (Rolfe and Brand 1997;Brookes et al 1998;Jacobs et al 2012;Salin et al 2012;Monternier et al 2014; but see Larsen et al 2011). Though there is a need for some mitochondrial ATP to support diverse cellular activities in vivo, the low respiration rate under basal conditions (i.e., SMR or BMR) results from both basal ATP demand and the effects of mitochondrial proton leak (Kadenbach 2003;Brand and Nicholls 2011).…”

“…This is because MMR was measured during peak excess postexercise oxygen consumption (EPOC), when the major requirement for oxygen is in the removal of lactate and the restoration of cellular homeostasis, which is supported by white muscle (Wood 1991). However, given that white muscle contributes approximately 35% to the total body mass of a trout (calculated according to Houlihan et al 1986), it is perhaps surprising that white muscle mitochondria did not explain any of the substantial variation in SMR, in contrast to that relationship reported in other species (Rolfe and Brand 1996;Monternier et al 2014). Instead, only the bioenergetics of the liver contributed to the variability in SMR.…”

“…Intraspecific variability in LEAK and OXPHOS can be considerable and is positively related to SMR and BMR (Brown et al 2012;Salin et al 2012;Monternier et al 2014) and MMR (Coen et al 2012;Jacobs et al 2012;Schlagowski et al 2013). These investigations into the effects of these mitochondrial properties on minimum or maximum metabolic rate have generally focused on comparisons of mean values between treatment groups or life stages (Brown et al 2012;Coen et al 2012;Jacobs et al 2012;Khan et al 2014;Monternier et al 2014). However, accounting for individual heterogeneity within a population is critical for understanding properties affecting fitness, since individual variation is what natural selection acts on (Careau and Garland 2012;Vindenes and Langangen 2015).…”

The oxidative debt of fasting: evidence for short to medium-term costs of advanced fasting in adult king penguins

“…Although such metabolic changes provide immediate lifesaving responses, medium-to long-term costs associated with metabolic changes during fasting remain little investigated in wild species that typically cope with repeated and sometimes prolonged periods of food shortage (Vázquez-Medina et al, 2010). Because mitochondria are cornerstone organelles implicated in metabolic responses to fasting (Monternier et al, 2014), but also the first site of production of damaging reactive oxygen species (ROS) (Andreyev et al, 2005), direct oxidative costs to prolonged fasting may be expected (e.g. Chausse et al, 2015;Geiger et al, 2012;Sorensen et al, 2006;Wasselin et al, 2014).…”

Skeletal muscle heterogeneity in fasting-induced mitochondrial oxidative phosphorylation flexibility in cold-acclimated ducklings

“…Although winter-acclimatized king penguin chicks retain a high capacity for thermogenesis (Duchamp et al, 1989), such starvation resistance reflects their ability to store energy as fat (34% adiposity in the pre-winter period) and control its allocation to minimize energy expenditure (growth arrest, lower basal metabolic rate, shallow hypothermia, reduced thermogenic effect of lipids) in order to maximize energy conservation (Duchamp et al, 1989;Cherel et al, 1993Cherel et al, , 2004Eichhorn et al, 2011;Teulier et al, 2013). In a recently published paper, it was shown that skeletal muscle mitochondria from fasted winteracclimatized chicks minimized the cost of ATP synthesis by increasing the efficiency of oxidative phosphorylation processes, which would ultimately alleviate the need for energy substrates (Monternier et al, 2014). This finding is of particular interest for at least two reasons.…”