1887

Abstract

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 is inherently temperature sensitive; above 37 °C, 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 °C. Remarkably, between 30 and 37 °C, 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 . The temperature-dependent increase in efficiency required the presence of the mitochondrial glycerol-3-phosphate dehydrogenase . 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.

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2011-12-01
2020-01-22
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References

  1. Albers E., Larsson C., Lidén G., Niklasson C., Gustafsson L.. ( 1996;). Influence of the nitrogen source on Saccharomyces cerevisiae anaerobic growth and product formation. Appl Environ Microbiol62:3187–3195[PubMed]
    [Google Scholar]
  2. Alexeeva S., Hellingwerf K. J., Teixeira de Mattos M. J.. ( 2002;). Quantitative assessment of oxygen availability: perceived aerobiosis and its effect on flux distribution in the respiratory chain of Escherichia coli . J Bacteriol184:1402–1406 [CrossRef][PubMed]
    [Google Scholar]
  3. Bekker M., de Vries S., Ter Beek A., Hellingwerf K. J., de Mattos M. J.. ( 2009;). Respiration of Escherichia coli can be fully uncoupled via the nonelectrogenic terminal cytochrome bd-II oxidase. J Bacteriol191:5510–5517 [CrossRef][PubMed]
    [Google Scholar]
  4. Berthold D. A., Andersson M. E., Nordlund P.. ( 2000;). New insight into the structure and function of the alternative oxidase. Biochim Biophys Acta1460:241–254 [CrossRef][PubMed]
    [Google Scholar]
  5. Bouwman J., Kiewiet J., Lindenbergh A., van Eunen K., Siderius M., Bakker B. M.. ( 2011;). Metabolic regulation rather than de novo enzyme synthesis dominates the osmo-adaptation of yeast. Yeast28:43–53[PubMed][CrossRef]
    [Google Scholar]
  6. Boveris A., Chance B.. ( 1973;). The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J134:707–716[PubMed]
    [Google Scholar]
  7. Brookes P. S.. ( 2005;). Mitochondrial H+ leak and ROS generation: an odd couple. Free Radic Biol Med38:12–23 [CrossRef][PubMed]
    [Google Scholar]
  8. Brown G. C.. ( 1992;). The leaks and slips of bioenergetic membranes. FASEB J6:2961–2965[PubMed]
    [Google Scholar]
  9. Bunoust O., Devin A., Avéret N., Camougrand N., Rigoulet M.. ( 2005;). Competition of electrons to enter the respiratory chain: a new regulatory mechanism of oxidative metabolism in Saccharomyces cerevisiae . J Biol Chem280:3407–3413 [CrossRef][PubMed]
    [Google Scholar]
  10. De Santis A., Melandri B. A.. ( 1984;). The oxidation of external NADH by an intermembrane electron transfer in mitochondria from the ubiquinone-deficient mutant E3-24 of Saccharomyces cerevisiae . Arch Biochem Biophys232:354–365[CrossRef]
    [Google Scholar]
  11. de Vries S., Marres C. A.. ( 1987;). The mitochondrial respiratory chain of yeast. Structure and biosynthesis and the role in cellular metabolism. Biochim Biophys Acta895:205–239[PubMed][CrossRef]
    [Google Scholar]
  12. Famili I., Forster J., Nielsen J., Palsson B. O.. ( 2003;). Saccharomyces cerevisiae phenotypes can be predicted by using constraint-based analysis of a genome-scale reconstructed metabolic network. Proc Natl Acad Sci U S A100:13134–13139 [CrossRef][PubMed]
    [Google Scholar]
  13. Fitton V., Rigoulet M., Ouhabi R., Guérin B.. ( 1994;). Mechanistic stoichiometry of yeast mitochondrial oxidative phosphorylation. Biochemistry33:9692–9698 [CrossRef][PubMed]
    [Google Scholar]
  14. Gasch A. P., Werner-Washburne M.. ( 2002;). The genomics of yeast responses to environmental stress and starvation. Funct Integr Genomics2:181–192 [CrossRef][PubMed]
    [Google Scholar]
  15. Gilkerson R. W., Margineantu D. H., Capaldi R. A., Selker J. M.. ( 2000;). Mitochondrial DNA depletion causes morphological changes in the mitochondrial reticulum of cultured human cells. FEBS Lett474:1–4 [CrossRef][PubMed]
    [Google Scholar]
  16. Grandier-Vazeille X., Bathany K., Chaignepain S., Camougrand N., Manon S., Schmitter J. M.. ( 2001;). Yeast mitochondrial dehydrogenases are associated in a supramolecular complex. Biochemistry40:9758–9769 [CrossRef][PubMed]
    [Google Scholar]
  17. Guerrero-Castillo S., Vázquez-Acevedo M., González-Halphen D., Uribe-Carvajal S.. ( 2009;). In Yarrowia lipolytica mitochondria, the alternative NADH dehydrogenase interacts specifically with the cytochrome complexes of the classic respiratory pathway. Biochim Biophys Acta1787:75–85[CrossRef]
    [Google Scholar]
  18. Harris N., Bachler M., Costa V., Mollapour M., Moradas-Ferreira P., Piper P. W.. ( 2005;). Overexpressed Sod1p acts either to reduce or to increase the lifespans and stress resistance of yeast, depending on whether it is Cu2+-deficient or an active Cu,Zn-superoxide dismutase. Aging Cell4:41–52[CrossRef]
    [Google Scholar]
  19. Hou J., Lages N. F., Oldiges M., Vemuri G. N.. ( 2009;). Metabolic impact of redox cofactor perturbations in Saccharomyces cerevisiae . Metab Eng11:253–261 [CrossRef][PubMed]
    [Google Scholar]
  20. Jarmuszkiewicz W., Milani G., Fortes F., Schreiber A. Z., Sluse F. E., Vercesi A. E.. ( 2000;). First evidence and characterization of an uncoupling protein in fungi kingdom: CpUCP of Candida parapsilosis . FEBS Lett467:145–149 [CrossRef][PubMed]
    [Google Scholar]
  21. Juszczuk I. M., Rychter A. M.. ( 2003;). Alternative oxidase in higher plants. Acta Biochim Pol50:1257–1271[PubMed]
    [Google Scholar]
  22. Kerscher S., Dröse S., Zwicker K., Zickermann V., Brandt U.. ( 2002;). Yarrowia lipolytica, a yeast genetic system to study mitochondrial complex I. Biochim Biophys Acta1555:83–91 [CrossRef][PubMed]
    [Google Scholar]
  23. Larsson C., Påhlman I. L., Ansell R., Rigoulet M., Adler L., Gustafsson L.. ( 1998;). The importance of the glycerol 3-phosphate shuttle during aerobic growth of Saccharomyces cerevisiae . Yeast14:347–357 [CrossRef][PubMed]
    [Google Scholar]
  24. Lenk R., Penman S.. ( 1971;). Morphological studies of cells grown in the absence of mitochondrial-specific protein synthesis. J Cell Biol49:541–546 [CrossRef][PubMed]
    [Google Scholar]
  25. Longtine M. S., McKenzie A. III, Demarini D. J., Shah N. G., Wach A., Brachat A., Philippsen P., Pringle J. R.. ( 1998;). Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae . Yeast14:953–961 [CrossRef][PubMed]
    [Google Scholar]
  26. Luévano-Martínez L. A., Moyano E., de Lacoba M. G., Rial E., Uribe-Carvajal S.. ( 2010;). Identification of the mitochondrial carrier that provides Yarrowia lipolytica with a fatty acid-induced and nucleotide-sensitive uncoupling protein-like activity. Biochim Biophys Acta1797:81–88 [CrossRef][PubMed]
    [Google Scholar]
  27. Maxwell D. P., Wang Y., McIntosh L.. ( 1999;). The alternative oxidase lowers mitochondrial reactive oxygen production in plant cells. Proc Natl Acad Sci U S A96:8271–8276 [CrossRef][PubMed]
    [Google Scholar]
  28. McGill M., Hsu T. C., Brinkley B. R.. ( 1973;). Electron-dense structures in mitochondria induced by short-term ethidium bromide treatment. J Cell Biol59:260–265 [CrossRef][PubMed]
    [Google Scholar]
  29. Mensonides F. I. C.. ( 2007;).How Saccharomyces cerevisiae copes with heat stress: an experimental and theoretical study
  30. Molenaar D., van Berlo R., de Ridder D., Teusink B.. ( 2009;). Shifts in growth strategies reflect tradeoffs in cellular economics. Mol Syst Biol5:323 [CrossRef][PubMed]
    [Google Scholar]
  31. Moro F., Muga A.. ( 2006;). Thermal adaptation of the yeast mitochondrial Hsp70 system is regulated by the reversible unfolding of its nucleotide exchange factor. J Mol Biol358:1367–1377 [CrossRef][PubMed]
    [Google Scholar]
  32. Nicholls D. G., Locke R. M.. ( 1984;). Thermogenic mechanisms in brown fat. Physiol Rev64:1–64[PubMed]
    [Google Scholar]
  33. Onishi T.. ( 1973;). Mechanism of electron transport and energy conservation in the site I region of the respiratory chain. Biochim Biophys Acta301:105–128[PubMed][CrossRef]
    [Google Scholar]
  34. Orij R., Brul S., Smits G. J.. ( 2011;). Intracellular pH is a tightly controlled signal in yeast. Biochim Biophys Acta1810:933–944[PubMed][CrossRef]
    [Google Scholar]
  35. Ouhabi R., Rigoulet M., Guerin B.. ( 1989;). Flux-yield dependence of oxidative phosphorylation at constant ΔH+ . FEBS Lett254:199–202 [CrossRef]
    [Google Scholar]
  36. Papa S., Guerrieri F., Capitanio N.. ( 1997;). A possible role of slips in cytochrome C oxidase in the antioxygen defense system of the cell. Biosci Rep17:23–31 [CrossRef][PubMed]
    [Google Scholar]
  37. Pirt S. J.. ( 1965;). The maintenance energy of bacteria in growing cultures. Proc R Soc Lond B Biol Sci163:224–231 [CrossRef][PubMed]
    [Google Scholar]
  38. Pirt S. J.. ( 1975;). Principles of Microbe and Cell Cultivation Oxford: Blackwell Scientific Publications;
    [Google Scholar]
  39. Poot M., Zhang Y. Z., Krämer J. A., Wells K. S., Jones L. J., Hanzel D. K., Lugade A. G., Singer V. L., Haugland R. P.. ( 1996;). Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J Histochem Cytochem44:1363–1372 [CrossRef][PubMed]
    [Google Scholar]
  40. Postmus J., Canelas A. B., Bouwman J., Bakker B. M., van Gulik W., de Mattos M. J., Brul S., Smits G. J.. ( 2008;). Quantitative analysis of the high temperature-induced glycolytic flux increase in Saccharomyces cerevisiae reveals dominant metabolic regulation. J Biol Chem283:23524–23532 [CrossRef][PubMed]
    [Google Scholar]
  41. Pronk J. T., Yde Steensma H., Van Dijken J. P.. ( 1996;). Pyruvate metabolism in Saccharomyces cerevisiae . Yeast12:1607–1633 [CrossRef][PubMed]
    [Google Scholar]
  42. Rigoulet M., Leverve X., Fontaine E., Ouhabi R., Guérin B.. ( 1998;). Quantitative analysis of some mechanisms affecting the yield of oxidative phosphorylation: dependence upon both fluxes and forces. Mol Cell Biochem184:35–52 [CrossRef][PubMed]
    [Google Scholar]
  43. Rolfe D. F., Brand M. D.. ( 1997;). The physiological significance of mitochondrial proton leak in animal cells and tissues. Biosci Rep17:9–16 [CrossRef][PubMed]
    [Google Scholar]
  44. Rønnow B., Kielland-Brandt M. C.. ( 1993;). GUT2, a gene for mitochondrial glycerol 3-phosphate dehydrogenase of Saccharomyces cerevisiae . Yeast9:1121–1130 [CrossRef][PubMed]
    [Google Scholar]
  45. Rosenfeld E., Beauvoit B.. ( 2003;). Role of the non-respiratory pathways in the utilization of molecular oxygen by Saccharomyces cerevisiae . Yeast20:1115–1144 [CrossRef][PubMed]
    [Google Scholar]
  46. Siedow J. N., Umbach A. L.. ( 2000;). The mitochondrial cyanide-resistant oxidase: structural conservation amid regulatory diversity. Biochim Biophys Acta1459:432–439 [CrossRef][PubMed]
    [Google Scholar]
  47. Sluse F. E., Jarmuszkiewicz W.. ( 2002;). Uncoupling proteins outside the animal and plant kingdoms: functional and evolutionary aspects. FEBS Lett510:117–120 [CrossRef][PubMed]
    [Google Scholar]
  48. Smits G. J., Brul S.. ( 2005;). Stress tolerance in fungi – to kill a spoilage yeast. Curr Opin Biotechnol16:225–230 [CrossRef][PubMed]
    [Google Scholar]
  49. Strassburg K., Walther D., Takahashi H., Kanaya S., Kopka J.. ( 2010;). Dynamic transcriptional and metabolic responses in yeast adapting to temperature stress. OMICS14:249–259 [CrossRef][PubMed]
    [Google Scholar]
  50. Stuart R. A.. ( 2008;). Supercomplex organization of the oxidative phosphorylation enzymes in yeast mitochondria. J Bioenerg Biomembr40:411–417 [CrossRef][PubMed]
    [Google Scholar]
  51. Tempest D. W., Neijssel O. M.. ( 1984;). The status of YATP and maintenance energy as biologically interpretable phenomena. Annu Rev Microbiol38:459–486 [CrossRef][PubMed]
    [Google Scholar]
  52. Turrens J. F., Boveris A.. ( 1980;). Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J191:421–427[PubMed]
    [Google Scholar]
  53. van Dijken J. P., Scheffers W. A.. ( 1986;). Redox balances in the metabolism of sugars by yeasts. FEMS Microbiol Lett32:199–224[CrossRef]
    [Google Scholar]
  54. Verduyn C.. ( 1991;). Physiology of yeasts in relation to biomass yields. Antonie van Leeuwenhoek60:325–353 [CrossRef][PubMed]
    [Google Scholar]
  55. Verduyn C., Postma E., Scheffers W. A., van Dijken J. P.. ( 1990;). Energetics of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol136:405–412[PubMed][CrossRef]
    [Google Scholar]
  56. Verduyn C., Stouthamer A. H., Scheffers W. A., van Dijken J. P.. ( 1991;). A theoretical evaluation of growth yields of yeasts. Antonie van Leeuwenhoek59:49–63 [CrossRef][PubMed]
    [Google Scholar]
  57. Verduyn C., Postma E., Scheffers W. A., Van Dijken J. P.. ( 1992;). Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast8:501–517 [CrossRef][PubMed]
    [Google Scholar]
  58. von Jagow G., Klingenberg M.. ( 1970;). Pathways of hydrogen in mitochondria of Saccharomyces carlsbergensis . Eur J Biochem12:583–592 [CrossRef][PubMed]
    [Google Scholar]
  59. Wallace R. J., Holms W. H.. ( 1986;). Maintenance coefficients and rates of turnover of cell material in Escherichia coli ML308 at different growth temperatures. FEMS Microbiol Lett37:317–320 [CrossRef]
    [Google Scholar]
  60. Warner J. R.. ( 1999;). The economics of ribosome biosynthesis in yeast. Trends Biochem Sci24:437–440 [CrossRef][PubMed]
    [Google Scholar]
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