1887

Abstract

A continuous culture of IFO 0233, growing with glucose as the major carbon and energy source, shows oscillations of respiration with a period of 48 min. Samples taken at maxima and minima indicate that (i) periodic changes do not occur as a result of carbon depletion, (ii) intrinsic differences in respiratory activity occur in washed organisms and (iii) a respiratory inhibitor accumulates during respiratory oscillations. Plasma membrane and inner mitochondrial membranes generate transmembrane electrochemical potentials; changes in these can be respectively assessed using anionic or cationic fluorophores. Thus flow cytometric analyses indicated that an oxonol dye [DiBAC(3); bis(1,3-dibutylbarbituric acid)trimethine oxonol] was excluded from yeasts to a similar extent (in >98% of the population) at all stages, showing that the plasma membrane potential was maintained at a steady value. However, uptake of Rhodamine 123 was greatest at that phase characterized by a low respiratory rate. Addition of uncouplers of energy conservation [CCCP (-chlorocarbonylcyanide phenylhydrazone) or S-13(5-chloro-3--butyl-2-chloro-4-nitrosalicylanilide)] to the continuous cultures increased the respiration, but had only a transient effect on the period of the oscillation. Electron microscopy showed changes in mitochondrial ultrastructure during the respiratory oscillation. At low respiration the cristae were more clearly defined due to swelling of the matrix; this corresponds to the ‘orthodox’ conformation. When respiration was high the mitochondrial configuration was ‘condensed’. It has been shown previously that a temperature-compensated ultradian clock operates in . It is proposed that mitochondria undergo cycles of energization in response to energetic demands driven by this ultradian clock output.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-11-3715
2002-11-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/11/1483715a.html?itemId=/content/journal/micro/10.1099/00221287-148-11-3715&mimeType=html&fmt=ahah

References

  1. Chance B., Williams R. G. 1956; The respiratory chain and oxidative phosphorylation. Adv Enzymol Relat Areas Mol Biol 17:65–134
    [Google Scholar]
  2. Chance B, Legallais V, Sorge J., Graham N. 1975; A versatile time-sharing, multichannel spectrophotometer, reflectometer and fluorometer. Anal Biochem 66:498–514
    [Google Scholar]
  3. Chen L. B. 1988; Mitochondrial membrane potential in living cells. Annu Rev Cell Biol 4:155–181
    [Google Scholar]
  4. Dinsdale M. G, Lloyd D., Jarvis B. 1995; Yeast vitality during cider fermentation: two approaches to the measurement of membrane potential. J Inst Brew 101:453–458
    [Google Scholar]
  5. Edwards S. W., Lloyd D. 1978; Oscillations of respiration and adenine nucleotides in synchronous cultures of Acanthamoeba castellanii . J Gen Microbiol 108:197–204
    [Google Scholar]
  6. Edwards S. W., Lloyd D. 1980; Oscillations in protein and RNA content during synchronous growth of Acanthamoeba castellanii . FEBS Lett 109:21–26
    [Google Scholar]
  7. Hackenbrock C. R. 1968a; Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states. Proc Natl Acad Sci USA 61:598–605
    [Google Scholar]
  8. Hackenbrock C. R. 1968b; Ultrastructural bases for metabolically-linked mechanical activities in mitochondria. II. Electron transport-linked ultrastructural transformation in mitochondria. J Cell Biol 37:345–369
    [Google Scholar]
  9. Hanstein W. G. 1976; Uncoupling of oxidative phosphorylation. Biochim Biophys Acta 456:129–148
    [Google Scholar]
  10. Harrison D. E. F., Chance B. 1970; Fluorimetric technique for monitoring changes in the level of reduced nicotinamide nucleotides in continuous cultures of microorganisms. Appl Microbiol 19:446–450
    [Google Scholar]
  11. Keulers M., Kuriyama H. 1998; Extracellular signalling in oscillatory yeast culture. In Information Processing Cells and Tissues pp 85–94 Edited by Holcombe W. M. L., Paton R., Holcombe M. New York: Plenum;
    [Google Scholar]
  12. Keulers M, Suzuki T, Satroutdinov A. D., Kuriyama H. 1996a; Autonomous metabolic oscillation in continuous culture of Saccharomyces cerevisiae growth on ethanol. FEMS Microbiol Lett 142:253–258
    [Google Scholar]
  13. Keulers M, Satroutdinov A. D, Suzuki T., Kuriyama H. 1996b; Synchronisation affector of autonomous short-period-sustained oscillation of Saccharomyces cerevisiae . Yeast 12:673–682
    [Google Scholar]
  14. Klevecz R. R., Murray D. B. 2001; Genome wide oscillations in expression. Mol Biol Rep 28:73–82
    [Google Scholar]
  15. Lloyd D. 1974 The Mitochondria of Microorganisms London: Academic Press;
    [Google Scholar]
  16. Lloyd D. 1988; Circadian and ultradian clock-controlled rhythms in unicellular microorganisms. Adv Microb Physiol Biochem 39:291–298
    [Google Scholar]
  17. Lloyd D. 1992; Intracellular timekeeping: epigenetic oscillations reveal the functions of an ultradian clock. In Ultradian Rhythms in Life Processes pp 5–22 Edited by Lloyd D., Rossi E. R. London: Springer;
    [Google Scholar]
  18. Lloyd D., Edwards S. W. 1978; Electron transport pathways alternative to the main phosphorylating chain. In Functions of Alternative Oxidases pp 1–10 Edited by Degn H., Lloyd D., Hill G. C. Oxford: Pergamon;
    [Google Scholar]
  19. Lloyd D., Edwards S. W. 1984; Epigenetic oscillations during the cell cycles of lower eukaryotes are coupled to a clock: life’s slow dance to the music of time. In Cell Cycle Clocks pp 27–46 Edited by Edmunds L. N. New York: Marcel Dekker;
    [Google Scholar]
  20. Lloyd D., Edwards S. W. 1987; Temperature-compensated ultradian rhythms in lower eukaryotes: timers for cell cycle and circadian events?. In Advances in Chronobiology, Part A pp 131–151 Edited by Pauly J. E., Scheving L. E. New York: Alan R. Liss;
    [Google Scholar]
  21. Lloyd D., Murray D. S. 2000; Redox cycling of intracellular thiols: state variables for ultradian, cell division cycle and circadian cycles. In Redox Behaviour of Circadian Systems pp 85–94 Edited by Driessche T. Vanden., Guisset J.-L., Vries G. P. De. Amsterdam: Kluwer;
    [Google Scholar]
  22. Lloyd D, Edwards S. W., Williams J. L. 1981; Oscillatory accumulation of total cellular protein in synchronous cultures of Candida utilis . FEMS Microbiol Lett 12:295–298
    [Google Scholar]
  23. Lloyd D, Edwards S. W., Fry J. C. 1982a; Temperature-compensated oscillations in respiration and cellular protein content in synchronous cultures of Acanthamoeba castellanii . Proc Natl Acad Sci USA 79:3785–3788
    [Google Scholar]
  24. Lloyd D, Poole R. K., Edwards S. W. 1982b The Cell Division Cycle: Temporal Control of Cellular Growth and Reproduction New York: Academic Press;
    [Google Scholar]
  25. Luzikov V. N. 1984; Mechanisms of mitochondrial stabilization. In Mitochondrial Biogenesis and Breakdown, pp 109–114 New York: Plenum;
    [Google Scholar]
  26. Mitchell P., Moyle J. 1969; Estimation of membrane potential and pH difference across the cristal membrane of rat-liver mitochondria. Eur J Biochem 7:471–478
    [Google Scholar]
  27. Murray D. B, Engelen F. A, Keulers M, Kuriyama H., Lloyd D. 1998a; NO+ but not NO· inhibits respiratory oscillations in ethanol-grown chemostat cultures of Saccharomyces cerevisiae . FEBS Lett 431:297–299
    [Google Scholar]
  28. Murray D. B, Engelen F. A, Keulers M, Kuriyama H., Lloyd D. 1998b; NO+ but not NO· inhibits respiratory oscillations in ethanol-grown chemostat cultures of Saccharomyces cerevisiae . Trans Biochem Soc 26:S339
    [Google Scholar]
  29. Murray D. B, Engelen F, Lloyd D., Kuriyama H. 1999; Involvement of glutathione in the regulation of respiratory oscillation during a continuous culture of Saccharomyces cerevisiae . Microbiology 145:2739–2745
    [Google Scholar]
  30. Murray D. B, Roller S, Kuriyama H., Lloyd D. 2001; Clock control of ultradian respiratory oscillation found during yeast continuous culture. J Bacteriol 183:7253–7259
    [Google Scholar]
  31. Ohnishi T, Kawaguchi K., Hagihara B. 1966; Isolation of intact mitochondria from yeast. J Biol Chem 241:1797–1806
    [Google Scholar]
  32. Poole R. K, Lloyd D., Kemp R. B. 1973; Respiratory oscillations and heat evolution in synchronously dividing cultures of the fission yeast Schizosaccharomyces pombe 972h . J Gen Microbiol 77:209–220
    [Google Scholar]
  33. Salgado L. E. J, Murray D. B., Lloyd D. 2002; Some antidepressant agents (Li+, monoamine oxidase type A inhibitors) perturb the ultradian clock in Saccharomyces cerevisiae . Biol Rhythm Res 33:351–361
    [Google Scholar]
  34. Satroutdinov A. D, Kuriyama H., Kobayashi H. 1992; Oscillatory metabolism of Saccharomyces cerevisiae in continuous culture. FEMS Microbiol Lett 98:261–268
    [Google Scholar]
  35. Sohn H.-Y., Kuriyama H. 2001; Ultradian metabolic oscillation of Saccharomyces cerevisiae during aerobic continuous culture: H2S, a population synchroniser is produced by sulphite reductase. Yeast 18:125–135
    [Google Scholar]
  36. Sohn H.-Y, Murray D. B., Kuriyama H. 2000; Ultradian oscillation of Saccharomyces cerevisiae during aerobic continuous culture: hydrogen sulphide mediates population synchrony. Yeast 16:1185–1190
    [Google Scholar]
  37. Vogel A. I. 1954; Reactions of sulphides. In Macro and Semimicro Qualitative Inorganic Analysis, 4th edn. p 336 London: Longmans, Green & Co;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-11-3715
Loading
/content/journal/micro/10.1099/00221287-148-11-3715
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error