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Volume 134, Issue 11

Osmotic Adjustment and the Accumulation of Organic Solutes in Whole Cells and Protoplasts of Free

Abstract

In the presence of a suitable carbon source, whole cells and protoplasts of synthesized glycerol as a compatible organic solute in response to increased external osmotic pressure. Boyle-van’t Hoff plots showed that protoplasts, and non-turgid cells, exhibited a linear relationship between volume and the external osmotic pressure (i.e. they behaved as near-ideal osmometers), and that both protoplasts and cells have a component which is not osmotically responsive - the non-osmotic volume (NOV). Glycerol levels in whole cells and protoplasts were elevated by increased external osmotic pressure over a similar time-scale to the period of exponential cell growth, reaching a maximum value at 6–12 h and declining thereafter. This suggests that the restoration of turgor pressure in whole cells was not the sole regulator of glycerol accumulation. Stationary phase whole cells had negligible levels of intracellular glycerol after growth in a medium of raised osmotic pressure. However, intracellular trehalose synthesis in these cells began earlier and reached a higher maximum level than in basal medium. Once exponential growth had stopped, cell turgor and internal osmotic pressure decreased somewhat. These new, lower values may be determined by the extent of trehalose accumulation in stationary phase cells.

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© Society for General Microbiology 1988
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1988-11-01
2024-04-19
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References

  1. Adler L., Blomberg A., Nilsson A. 1985; Glycerol metabolism and osmoregulation in the salttolerant yeast Debaryomyces hansenii.. Journal of Bacteriology 162:300–306
     [Google Scholar]
  2. André L., Nilsson A., Adler L. 1988; The role of glycerol in osmotolerance of the yeast Debaryomyces hansenii.. Journal of General Microbiology 134:669–677
     [Google Scholar]
  3. Arakawa T., Timasheff S.N. 1985; The stabilization of proteins by osmolytes.. Biophysical Journal 47:411–414
     [Google Scholar]
  4. Arnold W.N., Lacy J.S. 1977; Permeability of the cell envelope and osmotic behaviour of Saccharomyces cerevisiae.. Journal of Bacteriology 131:564–571
     [Google Scholar]
  5. Ben-Amotz A., Avron M. 1983; Accumulation of metabolites by halotolerant algae and its industrial potential.. Annual Review of Microbiology 37:95–119
     [Google Scholar]
  6. Borowitzka L.J. 1985; Glycerol and other carbohydrate osmotic effectors.. In Transport Processes - Iono- and Osmoregulation pp. 437–453 Gilles R., Gilles-Baillien M. Edited by Berlin: Springer- Verlag;
     [Google Scholar]
  7. Borowitzka L.J., Brown A.D. 1974; The salt relations of marine and halophilic species of the unicellular green alga, Dunaliella: the role of glycerol as a compatible solute.. Archives of Microbiology 96:37–52
     [Google Scholar]
  8. Brown A.D. 1976; Microbial water stress.. Bacteriological Reviews 40:803–846
     [Google Scholar]
  9. Brown A.D. 1978; Compatible solutes and extreme water stress in eukaryotic microorganisms.. Advances in Microbial Physiology 7:181–242
     [Google Scholar]
  10. Brown A.D., Simpson J.R. 1972; Water relations of sugar-tolerant yeasts: the role of intracellular polyols.. Journal of General Microbiology 72:589–591
     [Google Scholar]
  11. Brown A.D., Mackenzie K.F., Singh K.K. 1986; Selected aspects of microbial osmoregulation.. FEMS Microbiology Reviews 39:31–36
     [Google Scholar]
  12. Clint G.M. 1985; The investigation of stomatal ionic relations using guard cell protoplasts. II. Osmotic relations of guard cell protoplasts in short and long-term incubations.. Journal of Experimental Botany 36:1739–1748
     [Google Scholar]
  13. Conway E.J., Armstrong W.MCD. 1961; The total intracellular concentration of solutes in yeast and other plant cells and the distensibility of the plant-cell wall.. Biochemical Journal 81:631–639
     [Google Scholar]
  14. Cram W.J. 1976; Negative feedback regulation of transport in cells.. The maintenance of turgor volume and nutrient supply. In Encyclopaedia of Plant Physiology, New Series 2A: pp. 284–316 Lüttge U., Pitman M. G. Edited by Berlin: Springer-Verlag;
     [Google Scholar]
  15. Crowe L.M., Mouradian R., Crowe J.H., Jackson S., Womersley C. 1984a; Effects of carbohydrates on membrane stability at low water activity.. Biochimica et biophysica acta 769:141–150
     [Google Scholar]
  16. Crowe L.M., Mouradian R., Crowe J.H., Jackson S., Womersley C. 1984b; Interactions of phospholipid monolayers with carbohydrates.. Biochimica et biophysica acta 769:151–159
     [Google Scholar]
  17. Dainty J. 1972; Plant cell-water relations: the elasticity of the cell wall.. Proceedings of the Royal Society of Edinburgh A70:89–93
     [Google Scholar]
  18. Dainty J. 1976; Water relations of plant cells.. In Encyclopaedia of Plant Physiology, New Series 2A pp. 12–35 Liittge U., Pitman M. G. Edited by Berlin: Springer-Verlag;
     [Google Scholar]
  19. Edgley M., Brown A.D. 1983; Yeast water relations: physiological changes induced by solute stress in Saccharomyces cerevisiae and Saccharomyces rouxii.. Journal of General Microbiology 129:3453–3463
     [Google Scholar]
  20. Gadd G.M. 1988; Carbon nutrition and metabolism.. In Physiology of Industrial Fungi Berry D. R. Edited by Oxford: Blackwell Scientific Publications (in the Press);
     [Google Scholar]
  21. Gadd G.M., Chudek J.A., Foster R., Reed R.H. 1984; The osmotic responses of Penicilliumochro-chloron: changes in internal solute levels in response to copper and salt stress.. Journal of General Microbiology 130:1969–1975
     [Google Scholar]
  22. Gadd G.M., Chalmers K., Reed R.H. 1987; The role of trehalose in dehydration resistance of Saccharomyces cerevisiae.. FEMS Microbiology Letters 48:249–254
     [Google Scholar]
  23. Gustaffson L. 1979; The ATP pool in relation to the production of glycerol and heat during growth of the halotolerant yeast Debaryomyces hansenii.. Archives of Microbiology 120:15–23
     [Google Scholar]
  24. Hellebust J.A. 1976; Osmoregulation.. Annual Review of Plant Physiology 27:485–505
     [Google Scholar]
  25. Hocking A.D. 1986; Effects of water activity and culture age on the glycerol accumulation patterns of five fungi.. Journal of General Microbiology 132:269–275
     [Google Scholar]
  26. Indge K.J. 1968; Metabolic lysis of yeast protoplasts.. Journal of General Microbiology 51:433–440
     [Google Scholar]
  27. Jennings D.H. 1983; Some aspects of the physiology and biochemistry of marine fungi.. Biological Reviews 58:423–459
     [Google Scholar]
  28. Jennings D.H. 1984; Polyol metabolism in fungi.. Advances in Microbial Physiology 25:149–193
     [Google Scholar]
  29. Kotyk A., Michaljaničová D., Struzinsky R., Baryshnikova L.M., Sychrová H. 1985; Absence of glucose-stimulated transport in yeast protoplasts.. Folia microbiologica 30:110–116
     [Google Scholar]
  30. Larsen P.I., Sydnes L.K., Landfald B., Strom A.R. 1987; Osmoregulation in E. coli by accumulation of organic osmolytes: betaines, glutamic acid and trehalose.. Archives of Microbiology 147:1–7
     [Google Scholar]
  31. Le Rudulier D., Strøm A.R., Dandekar A.M., Smith L.T., Valentine R.C. 1984; Molecular biology of osmoregulation.. Science 224:1064–1068
     [Google Scholar]
  32. Levin R.L. 1979; Water permeability of yeast cells at sub-zero temperatures.. Journal of Membrane Biology 46:91–124
     [Google Scholar]
  33. Low P.S. 1985; Molecular basis of the biological compatibility of nature’s solutes.. In Transport Processes - Iono- and Osmoregulation pp. 469–477 Gilles R., Gilles-Baillien M. Edited by Berlin: Springer-Verlag;
     [Google Scholar]
  34. Mackay M.A., Norton R.S., Borowitzka L.J. 1984; . Organic osmoregulatory solutes in cyanobacteria.. Journal of General Microbiology 130:2177–2191
     [Google Scholar]
  35. Measures J.C. 1975; The role of amino acids in osmoregulation of non-halophilic bacteria.. Nature; London: 257:398–400
     [Google Scholar]
  36. Morris G.J., Winters L., Coulson G.E., Clarke K.J. 1986; Effect of osmotic stress on the ultrastructure and viability of the yeast Saccharomyces cerevisiae.. Journal of General Microbiology 132:2023–2034
     [Google Scholar]
  37. Munns R., Greenway H., Kirst G.O. 1983; Halotolerant eukaryotes.. In Encyclopaedia of Plant Physiology, New Series 12C: pp. 60–131 Lange O. L., Nobel P. S., Osmond C. B., Ziegler H. Edited by New York: Springer-Verlag;
     [Google Scholar]
  38. Neဝas O. 1979; Regeneration of protoplasts.. In Advances in Protoplast Research, Proceedings of the 5th International Protoplast Symposium pp. 151–161 Ferenczy L., Farkas G. L. Edited by Oxford: Pergamon Press;
     [Google Scholar]
  39. Nobel P.S. 1983 Biophysical Plant Physiology and Ecology. San Francisco: W. H. Freeman;
     [Google Scholar]
  40. Onishi H. 1963; Osmophilic yeasts.. Advances in Food Research 12:53–94
     [Google Scholar]
  41. Panek A.D. 1985; Trehalose metabolism and its role in Saccharomyces cerevisiae.. Journal of Biotechnology 3:121–130
     [Google Scholar]
  42. Quain D.E., Boulton C.A. 1987; Growth and metabolism of mannitol by strains of Saccharomyces cerevisiae.. Journal of General Microbiology 133:1675–1684
     [Google Scholar]
  43. Reed R.H. 1984; Use and abuse of osmo- terminology.. Plant, Cell and Environment165–170
     [Google Scholar]
  44. Reed R.H., Chudek J.A., Foster R., Stewart W.D.P. 1984a; Osmotic adjustment in cyanobacteria from hypersaline environments.. Archives of Microbiology 138:333–337
     [Google Scholar]
  45. Reed R.H., Richardson D.L., Warr S.R.C., Stewart W.D.P. 1984b; Carbohydrate accumulation and osmotic stress in cyanobacteria.. Journal of General Microbiology 130:1–4
     [Google Scholar]
  46. Reed R.H., Richardson D.L., Stewart W.D.P. 1985; Na+ uptake and extrusion in the cyanobacteriumSynechocystis PCC 6714 in response to hypersaline treatment: evidence for transient changes in plasmalemma Na+ permeability.. Biochimica et biophysica acta 814:347–355
     [Google Scholar]
  47. Reed R.H., Chudek J.A., Foster R., Gadd G.M. 1987; Osmotic significance of glycerol accumulation in exponentially growing yeasts.. Applied and Environmental Microbiology 53:2119–2123
     [Google Scholar]
  48. Vreeland R.H. 1987; Mechanisms of halotolerance in microorganisms.. CRC Critical Reviews in Microbiology 14:311–356
     [Google Scholar]
  49. Wethered J.M., Metcalfe E.C., Jennings D.H. 1985; Carbohydrate metabolism in the fungus Dendryphiellasalina. VIII. The contribution of polyols and ions to the mycelial solute potential in relation to the external osmoticum.. New Phytologist 101:631–649
     [Google Scholar]
  50. White C., Gadd G.M. 1987; The uptake and cellular distribution of zinc in Saccharomyces cerevisiae.. Journal of General Microbiology 133:727–737
     [Google Scholar]
  51. Wolf A.V., Brown M.G., Prentiss P.G. 1979; Concentrative properties of aqueous solutions: conversion tables, p. D227-276.. In CRC Handbook of Chemistry & Physics, 60th edn. Weast R. C. Edited by Palm Beach, Florida: CRC Press;
     [Google Scholar]
  52. Yagi T. 1988; Intracellular levels of glycerol necessary for initiation of growth under salt-stressed conditions in a salt tolerant yeast, Zygosaccharomyces rouxii.. FEMS Microbiology Letters 49:25–31
     [Google Scholar]
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Osmotic Adjustment and the Accumulation of Organic Solutes in Whole Cells and Protoplasts of Saccharomyces cerevisiae
Microbiology 134, 3049 (1988); https://doi.org/10.1099/00221287-134-11-3049
/content/journal/micro/10.1099/00221287-134-11-3049
/content/journal/micro/10.1099/00221287-134-11-3049
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