Long-term fasting decreases mitochondrial avian UCP-mediated oxygen consumption in hypometabolic king penguins

1 Université de Lyon, Lyon, F-69003 France; CNRS UMR 5123, Physiologie Intégrative Cellulaire et Moléculaire, Villeurbanne, France; 2 Centre for Ornithology, School of Biosciences, University of Birmingham, Birmingham, United Kingdom; and 3 Institut Pluridisciplinaire Hubert Curien, Département Ecologie, Physiologie et Ethologie, Strasbourg, France Submitted 20 April 2007 ; accepted in final form 7 May 2008 In endotherms, regulation of the degree of mitochondrial coupling affects cell metabolic efficiency. Thus it may be a key contributor to minimizing metabolic rate during long periods of fasting. The aim of the present study was to investigate whether variation in mitochondrial avian uncoupling proteins (avUCP), as putative regulators of mitochondrial oxidative phosphorylation, may contribute to the ability of king penguins ( Aptenodytes patagonicus ) to withstand fasting for several weeks. After 20 days of fasting, king penguins showed a reduced rate of whole animal oxygen consumption ( O 2 ; –33%) at rest, together with a reduced abundance of avUCP and peroxisome proliferator-activated receptor- coactivator-1 (PGC1- ) mRNA in pectoralis muscle (–54%, –36%, respectively). These parameters were restored after the birds had been refed for 3 days. Furthermore, in recently fed, but not in fasted penguins, isolated muscle mitochondria showed a guanosine diphosphate-inhibited, fatty acid plus superoxide-activated respiration, indicating the presence of a functional UCP. It was calculated that variation in mitochondrial UCP-dependent respiration in vitro may contribute to nearly 20% of the difference in resting O 2 between fed or refed penguins and fasted penguins measured in vivo. These results suggest that the lowering of avUCP activity during periods of long-term energetic restriction may contribute to the reduction in metabolic rate and hence the ability of king penguins to face prolonged periods of fasting. metabolic rate; mitochondria; oxidative capacity Address for reprint requests and other correspondence: C. Duchamp, Laboratoire de Physiologie Intégrative, Cellulaire et Moléculaire, UMR 5123 CNRS, Université Claude Bernard Lyon1, 43 bd du 11 novembre 1918, F-69622 Villeurbanne Cedex, France (e-mail address: claude.duchamp{at}univ-lyon1.fr )