To adapt to changes in the environment, cells have to dynamically alter their phenotype in response to, for instance, temperature and oxygen availability. Interestingly, mitochondrial function in Saccharomyces cerevisiae is inherently temperature sensitive; above 37 6C, yeast cells cannot grow on respiratory carbon sources. To investigate this phenomenon, we studied the effect of cultivation temperature on the efficiency (production of ATP per atom of oxygen consumed, or P/O) of the yeast respiratory chain in glucose-limited chemostats. We determined that even though the specific oxygen consumption rate did not change with temperature, oxygen consumption no longer contributed to mitochondrial ATP generation at temperatures higher than 37 6C. Remarkably, between 30 and 37 6C, we observed a linear increase in respiratory efficiency with growth temperature, up to a P/O of 1.4, close to the theoretical maximum that can be reached in vivo. The temperature-dependent increase in efficiency required the presence of the mitochondrial glycerol-3-phosphate dehydrogenase GUT2. Respiratory chain efficiency was also altered in response to changes in oxygen availibility. Our data show that, even in the absence of alternative oxidases or uncoupling proteins, yeast has retained the ability to dynamically regulate the efficiency of coupling of oxygen consumption to proton translocation in the respiratory chain in response to changes in the environment.
INTRODUCTIONUnicellular organisms have to cope with environmental changes in order to maintain homeostasis and to survive. The changes may perturb cellular functions, such as metabolic fluxes, cellular structures, chemical gradients etc., and can thus result in reduced growth or even cell death. Microbes such as yeasts can rapidly adapt to challenging conditions by altering their genetic expression profile or tuning the activity of key enzymes to function in the variety of environments these organisms encounter (Bouwman et al., 2011;Gasch & Werner-Washburne, 2002;Postmus et al., 2008;Smits & Brul, 2005;Strassburg et al., 2010). Adaptive responses put a significant additional energetic burden on the cells, since the gene expression cascade requires a substantial expenditure of energy (Tempest & Neijssel, 1984;Verduyn, 1991;Warner, 1999). The fraction of the energy generated in catabolism that is used in processes other than biomass production is the so-called maintenance energy (Pirt, 1965). Increases in maintenance energy may be caused by, for instance, increases in maintenance of membrane gradients, turnover of (damaged) cell components or energetically suboptimal biosynthetic pathways (Molenaar et al., 2009;Tempest & Neijssel, 1984).Baker's yeast has multiple strategies for energy generation. Carbohydrates are dissimilated into pyruvate, a key branching point in carbohydrate metabolism (Pronk et al., 1996). During fermentative metabolism, pyruvate is converted into acetaldehyde and subsequently reduced to ethanol or oxidized to acetate. In respiratory metabolism, pyruvate is conv...