1887

Abstract

Growth and metabolite formation were studied in oxygen-limited chemostat cultures of CBS 8066 and CBS 621 growing on glucose or maltose at a dilution rate of 0·1 h With either glucose or maltose could be grown under dual limitation of oxygen and sugar. Respiration and alcoholic fermentation occurred simultaneously and the catabolite fluxes through these processes were dependent on the magnitude of the oxygen feed. could also be grown under dual limitation of glucose and oxygen. However, at very low oxygen feed rates (i.e. below 4 mmol l h) growth was limited by oxygen only, as indicated by the high residual glucose concentration in the culture. In contrast to could not be grown anaerobically at a dilution rate of 0·1 h. With absence of oxygen resulted in wash-out, despite the presence of ergosterol and Tween-80 in the growth medium. The behaviour of with respect to maltose utilization in oxygen-limited cultures was remarkable: alcoholic fermentation did not occur and the amount of maltose metabolized was dependent on the oxygen supply. Oxygen-limited cultures of growing on maltose always contained high residual sugar concentrations. These observations throw new light on the so-called Kluyver effect. Apparently, maltose is a non-fermentable sugar for CBS 621, despite the fact that it can serve as a substrate for growth of this facultatively fermentative yeast. This is not due to the absence of key enzymes of alcoholic fermentation. Pyruvate decarboxylase and alcohol dehydrogenase were present at high levels in maltose-utilizing cells of grown under oxygen limitation. It is concluded that the Kluyver effect, in growing on maltose, results from a regulatory mechanism that prevents the sugar from being fermented. Oxygen is not a key factor in this phenomenon since under oxygen limitation alcoholic fermentation of maltose was not triggered.

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1994-04-01
2024-04-23
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References

  1. Andreasen A.A., Stier T.J.B. Anaerobic nutrition of Saccharomjces cerevisiae. I. Ergosterol requirement for growth in a defined medium. J Cell Comp Phjsiol 1953; 41:23–26
    [Google Scholar]
  2. Andreasen A.A., Stier T.J.B. Anaerobic nutrition of Saccharomjces cerevisiae. II. Unsaturated fatty acid requirement for growth in a defined medium. J Cell Comp Physiol 1954; 43:271–281
    [Google Scholar]
  3. Barnett J.A. Some controls on oligosaccharide utilization by yeasts: the physiological basis of the Kluyver effect. FEMS Microbiol Eett 1992; 100:371–378
    [Google Scholar]
  4. Barnett J.A., Payne R.W., Yarrow D. Yeast: characteristics and identification 2nd edn 1990 Cambridge: Cambridge University Press;
    [Google Scholar]
  5. Barnett J.A., Sims A.P. The requirement of oxygen for the active transport of sugars into yeasts. J Gen Microbiol 1982; 128:2303–2312
    [Google Scholar]
  6. Brown C.M., Rose A.H. Fatty -acid composition of Candida utilis as affected by growth temperature and dissolved-oxygen tension. J Bacteriol 1969; 99:371–378
    [Google Scholar]
  7. Bruinenberg P.M., de Bot P.H.M., van Dijken J.P., Scheffers W.A. NADH-linked aldose reductase: the key to anaerobic alcoholic fermentation of xylose by yeasts. Appl Microbiol Biotechnol 1984; 19:256–260
    [Google Scholar]
  8. Busturia A., Lagunas R. Catabolite inactivation of the glucose transport system in Saccharomjces cerevisiae. J Gen Microbiol 1986; 132:379–385
    [Google Scholar]
  9. Carrascosa J.M., Viguera M.D., Nunez de Castro I., Scheffers W.A. Metabolism of acetaldehyde and Custers effect in the yeast Brettanomyces abstinens. Antonie Eeeuwenhoek 1981; 47:209–215
    [Google Scholar]
  10. Clifton D., Walsh R.B., Fraenkel D.G. Functional studies of yeast glucokinase. J Bacteriol 1993; 175:3289–3294
    [Google Scholar]
  11. Custers M.T.J. Onderzoekingen over het gistgeslacht Brettanomyces 1940 The Netherlands: PhD Thesis, Delft University of Technology. ;
    [Google Scholar]
  12. Cysewski G.R., Wilke C.R. Utilization of cellulosic materials through enzymatic hydrolysis I Fermentation of hydrolysate to ethanol and single-cell protein. Biotechnol Bioeng 1976; 18:1297–1313
    [Google Scholar]
  13. van Dijken J.P., Scheffers W.A. Redox balances in the metabolism of sugars by yeasts. FEMS Microbiol Rev 1986; 32:199–224
    [Google Scholar]
  14. van Dijken J.P., van den Bosch E., Hermans J.J., Rodrigues de Miranda L., Scheffers W.A. Alcoholic fermentation by ‘non-fermentative’ yeasts. Yeast 1986; 2:123–127
    [Google Scholar]
  15. Fiechter A., Fuhrman G.F., Käppeli O. Regulation of glucose metabolism in growing yeast cells. Adv Microb Physiol 1981; 22:123–183
    [Google Scholar]
  16. Franzblau S.G., Sinclair N.A. Induction of pyruvate decarboxylase in Candida lit Hi s. Mycopathologia 1983; 83:29–33
    [Google Scholar]
  17. Furukawa K., Heinzle E., Dunn I.J. Influence of oxygen on the growth of Saccharomyces cerevisiae in continuous culture. Biotechnol Bioeng 1983; 25:2293–2317
    [Google Scholar]
  18. Gancedo C., Gancedo J.M., Sols A. Glycerol metabolism in yeasts. Pathways of utilization and production. Ear J Biochem 1968; 5:165–172
    [Google Scholar]
  19. Gaunt D.M., Degn H., Lloyd D. The influence of oxygen and organic hydrogen acceptors on glycolytic carbon dioxide production in Brettanomyces anomalus. Yeast 1988; 4:249–255
    [Google Scholar]
  20. Gommers P.J.F., van Schie B.J., van Dijken J.P., Kuenen I.G. Biochemical limits to microbial growth yields: an analysis of mixed substrate utilization. Biotechnol Bioeng 1988; 32:86–94
    [Google Scholar]
  21. Grosz R., Stephanopoulos G. Physiological, biochemical, and mathematical studies of micro-aerobic continuous ethanol fermentation by Saccharomyces cerevisiae. I. Hysteresis, oscillations, and maximum specific ethanol productivities in chemostat culture. Biotechnol Bioeng 1990; 36:1006–1019
    [Google Scholar]
  22. Höfer M., Nassar F.R. Aerobic and anaerobic uptake of sugars in Schizosaccharomycespombe. J Gen Microbiol 1987; 133:2163–2172
    [Google Scholar]
  23. Holzer H., Bernardt W., Schneider S. Zur Glycerin bildung in Backerhefe. Biochem Z 1963; 336:495–509
    [Google Scholar]
  24. Käppeli O. Regulati on of carbon metabolism in Saccharomyces cerevisiae and related yeasts. Adv Microb Physiol 1986; 28:181–209
    [Google Scholar]
  25. Käppeli O., Sonnleitner B. Regulation of sugar metabolism in Saccharomyces-Xypt yeast: experimental and conceptual considerations. Crit Rev Biotechnol 1986; 4:299–325
    [Google Scholar]
  26. Käppeli O., Gschwend-Petrik M., Fiechter A. Transient responses of Saccharomyces uvarum to a change of the growth-limiting nutrient in continuous culture. J Gen Microbiol 1985a; 131:47–52
    [Google Scholar]
  27. Käppeli O., Arreguin M., Rieger M. The respirative breakdown of glucose by Saccharomyces cerevisiae: an assessment of a physiological state. J Gen Microbiol 1985b; 131:1411–1416
    [Google Scholar]
  28. Kluyver A.J., Custers M.T.J. The suitability of disaccharides as respiration and assimilation substrates for yeasts which do not ferment these sugars. Antonie Eeeuwenhoek 1940; 6:121–162
    [Google Scholar]
  29. Kuriyama H., Kobayashi H. Effects of oxygen supply on yeast growth and metabolism in continuous fermentation. J Ferment Bioeng 1993; 75:364–367
    [Google Scholar]
  30. Lagunas R. Misconceptions about the energy metabolism of Saccharomyces cerevisiae. Yeast 1986; 2:221–228
    [Google Scholar]
  31. Lagunas R., Dominguez C., Busturia A., Sáez M.J. Mechanisms of appearance of the Pasteur effect in Saccharomyces cerevisiae: inactivation of sugar transport systems. J Bacteriol 1982; 152:19–25
    [Google Scholar]
  32. Laplace J.M., Delgenes J.P., Moletta R., Navarro J.M. Alcoholic fermentation of glucose and xylose by Pichia stipitis, Candida shehatae, Saccharomyces cerevisiae and Zymomonas mobilis: oxygen requirement as a key factor. Appl Microbiol Biotechnol 1991; 36:158–162
    [Google Scholar]
  33. Lloyd D., James C.J. The Pasteur effect in yeasts: mass spectrometric monitoring of oxygen uptake, and carbon dioxide and ethanol production. FEMS Microbiol Lett 1987; 42:27–31
    [Google Scholar]
  34. Lutstorf U., Megnet R. Multiple forms of alcohol dehydrogenase in Saccharomyces cerevisiae. I. Physiological control of ADH-2 and properties of ADH-2 and ADH-4. Arch Biochem Biophys 1968; 126:933–944
    [Google Scholar]
  35. Moss F.J., Rickard P.A.D., Beech G.A., Bush F.E. The response by microorganisms to steady state growth in controlled concentrations of oxygen and glucose. I. Candida utilis. Biotechnol Bioeng 1969; 11:561–580
    [Google Scholar]
  36. Nishizawa Y., Dunn I.J., Bourne J.R. The influence of oxygen and glucose on anaerobic ethanol production. In Proceedings of the 7th Symposium on Continuous Cultivation of Microorganisms 1980 Edited by Sikyta B., Fencl Z., Polacek V. Prague: Institute of Microbiology, Csechoslovak Academy of Sciences; pp 605–612
    [Google Scholar]
  37. Oura E. Reaction products of yeast fermentations. Process Biochem 1977; 12:19–35
    [Google Scholar]
  38. Petrik M., Käppeli O., Fiechter A. An expanded concept for the glucose effect in the yeast Saccharomyces uvarum: involvement of short-and long-term regulation. J Gen Microbiol 1983; 129:43–49
    [Google Scholar]
  39. Postma E., Scheffers W.A., van Dijken J.P. Adaptation of the kinetics of glucose transport to environmental conditions in the yeast Candida utilis CBS 621: a continuous-culture study. J Gen Microbiol 1988; 134:1109–1116
    [Google Scholar]
  40. Postma E., Scheffers W.A., van Dijken J.P. Kinetics of growth and glucose transport in glucose-limited chemostat cultures of Saccharomyces cerevisiae CBS 8066. Yeast 1989a; 5:159–165
    [Google Scholar]
  41. Postma E., Verduyn C., Scheffers W.A., van Dijken J.P. Enzymic analysis of the Crabtree effect in glucose-limited chemostat cultures of Saccharomyces cerevisiae. Appl Environ Microbiol 1989b; 55:ABB–All
    [Google Scholar]
  42. Scheffers W.A. Stimulation of fermentation in yeasts by acetoin and oxygen. Nature 1966; 210:533–534
    [Google Scholar]
  43. Schulz B., Höfer M. Utilization of lactose in nonrespiring cells of the yeast Debaryomycespolymorphus. Arch Microbiol 1986; 145:367–371
    [Google Scholar]
  44. Sims A.P., Barnett J.A. The requirement of oxygen for the utilization of maltose, cellobiose and D-galactose by certain anaerobically fermenting yeasts (Kluyver effect). J Gen Microbiol 1978; 106:277–288
    [Google Scholar]
  45. Sims A.P., Barnett J.A. Levels of activity of enzymes involved in anaerobic utilization of sugars by six yeast species: observations towards understanding the Kluyver effect. FEMS Microbiol Eett 1991; 77:295–298
    [Google Scholar]
  46. Sims A.P., Kopetzki E., Schulz B., Barnett J.A. The use of phenolic glycosides for studying the aerobic or anaerobic transport of disaccharides into yeasts. J Gen Microbiol 1984; 130:1933–1940
    [Google Scholar]
  47. Sims A.P., Stlilbrand H., Barnett J.A. The role of pyruvate decarboxylase in the Kluyver effect in the food yeast, Candida utilis. Yeast 1991; 7:479–487
    [Google Scholar]
  48. van Urk H., Mak P.R., Scheffers W.A., van Dijken J.P. Metabolic responses of Saccharomyces cerevisiae CBS 8066 and Candida utilis CBS 621 upon transition from glucose limitation to glucose excess. Yeast 1988; 4:283–291
    [Google Scholar]
  49. van Urk H., Schipper D., Breedveld G.J., Mak P.R., Scheffers W.A., van Dijken J.P. Localization and kinetics of pyruvate-metabolizing enzymes in relation to aerobic alcoholic fermentation in Saccharomyces cerevisiae CBS 8066 and Candida utilis CBS 621. Biochim Biophys Acta 1989; 992:78–86
    [Google Scholar]
  50. Verduyn C., Breedveld G.J., Scheffers W.A., van Dijken J.P. Substrate specificity of alcohol dehydrogenase from the yeasts Hansenula poljmorpha CBS 4732 and Candida utilis CBS 621. Yeast 1988; 4:143–148
    [Google Scholar]
  51. Verduyn C., Postma E., Scheffers W.A., van Dijken J.P. Physiology of Saccharomjces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol 1990; 136:395–403
    [Google Scholar]
  52. Verduyn C., Stouthamer A.H., Scheffers W.A., van Dijken J.P. A theoretical evaluation of growth yields of yeasts. Antonie Leeuwenhoek 1991; 59:49–63
    [Google Scholar]
  53. Visser W., Scheffers W.A., Batenburg-van der Vegte W.H., van Dijken J.P. Oxygen requirements of yeasts. Appl Environ Microbiol 1990; 56:3785–3792
    [Google Scholar]
  54. Weusthuis R.A., Adams H., Scheffers W.A., van Dijken J.P. Energetics and kinetics of maltose transport in Saccharomjces cerevisiae-. a continuous-culture study. Appl Environ Microbiol 1993; 59:3102–3109
    [Google Scholar]
  55. Wijsman M.R., van Dijken J.P., van Kleeff B.H.A., Scheffers W.A. Inhibition of fermentation and growth in batch cultures of the yeast Brettanomjces intermedins upon a shift from aerobic to anaerobic conditions (Custers effect). Antonie Leeuwenhoek 1984; 50:183–192
    [Google Scholar]
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