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Volume 138, Issue 10

Transport of glycine betaine in the extremely haloalkaliphilic sulphur bacterium Free

Abstract

The effect of osmotic stress on the transport of the compatible solute glycine betaine was examined in , an extremely haloalkaliphilic, phototrophic sulphur bacterium. Kinetic data indicated that possesses an active transport system for glycine betaine which is saturable and exhibits Michaelis-Menten kinetics. Experiments with chloramphenicol-treated cells (50 μg per ml of cell suspension) indicated that the transport system is constitutive and might be activated by a change in osmotic pressure. The uncouplers carbonyl cyanide -chlorophenylhydrazone (CCCP) and carbonyl cyanide -(trifluoromethoxy)-phenylhydrazone (CCFP) totally blocked uptake at concentrations of 25 μM and 100 μM, respectively. The system was insensitive to the cytochrome oxidase inhibitor sodium azide (1 mM), the respiratory chain inhibitor potassium cyanide (1 mM) and the glycolysis inhibitor iodoacetate (1 mM). The ionophore nigericin (50 μM) had the greatest inhibitory effect, completely abolishing uptake, while monensin (100 μM) caused 80% inhibition. Glycine betaine transport possessed considerable structural specifity: proline betaine was the most effective competitor and trigonelline and dimethylglycine exerted inhibition to a lesser extent. Transport in the dark was at a greatly reduced rate. These results collectively implied that the specific transport of glycine betaine might be driven by the electrochemical proton gradient generated by anaerobic photosynthesis.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
© Society for General Microbiology, 1992
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1992-10-01
2024-04-25
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References

  1. Abee T., , Palmen R., , Hellingwerf K. J., & Konings N. W. 1990; Osmoregulation in Rhodobacter sphaeroides . Journal of Bacteriology 173:229–233
     [Google Scholar]
  2. Barron A., , Jung J. U., & Villarejo M. 1987; Purification and characterization of a glycine betaine binding protein from Escherichia coli . Journal of Biological Chemistry 262:11841–11846
     [Google Scholar]
  3. Borowitzka L. J. 1980 Solute accumulation and regulation of cell water activity. In The Physiology and Biochemistry of Drought Resistance in Plants, pp. 97–130 Edited by Paleg L. B., & person-group-type="editor"> Aspinall D. Sydney, Australia: Academic Press;
     [Google Scholar]
  4. Brown A. D. 1976; Microbial water stress. Bacteriological Reviews 40:803–846
     [Google Scholar]
  5. Cairney J., , Booth I. R., & Higgins C. F. 1985a; Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system. Journal of Bacteriology 164:1224–1232
     [Google Scholar]
  6. Cairney J., , Booth I. R., & Higgins C. F. 1985b; Salmonella typhimurium encodes a transport system for the osmoprotectant betaine. Journal of Bacteriology 164:1218–1223
     [Google Scholar]
  7. Cromwell B. T., & Rennie S. O. 1953; The biosynthesis and metabolism of betaines in plants. Biochemical Journal 55:189–192
     [Google Scholar]
  8. Fougere F., & Rudulier Le. 1990; Uptake of glycine betaine and its analogues by bacteroids of Rhizobium meliloti . Journal of General Microbiology 136:157–163
     [Google Scholar]
  9. Gabbay-Azaria R., , Tel-OR E., & Schönfeld M. 1988; Glycine-betaine as an osmoregulant and compatible solute in the marine cyanobacterium Spirulina subsalsa . Archives of Biochemistry and Biophysics 264:333–339
     [Google Scholar]
  10. Galinski E. A. 1986 Salzadaptation durch kompatible Solute bei halophilen phototrophen Bakterien. Doctoral thesis University of Bonn, Germany:
     [Google Scholar]
  11. Galinski E. A. 1987 Halo-fermentation, a novel low water process for the production of organic chemicals and enzyme protective agents. In Bioreactors and Biotransformation, pp. 201–212 Edited by Moody G. W., & person-group-type="editor"> Baker P. B. Amsterdam: Elsevier;
     [Google Scholar]
  12. Galinski E. A., & Herzog R. M. 1990; The role of trehalose as a substitute for nitrogen-containing compatible solutes (Ectothiorhodospira halochloris) . Archives of Microbiology 153:607–613
     [Google Scholar]
  13. Galinski E. A., & Truper H. G. 1982; Betaine, a compatible solute in the extremely halophilic phototrophic bacterium Ectothiorhodospira halochloris . FEMS Microbiology Letters 13:357–360
     [Google Scholar]
  14. Grant W. O., , MILLS A. A., & SCHOFIELD A. K. 1979; An alkalophilic species of Ectothiorhodospira from a Kenyan soda lake. Journal of General Microbiology 110:137–142
     [Google Scholar]
  15. Hanes C. S. 1932; Studies on plant amylases. Biochemical Journal 26:1406–1421
     [Google Scholar]
  16. Higgins C. F., , Cairney J., , Stirling D. A., , Sutherland L., & Booth I. R. 1987; Osmotic regulation of gene expression: ionic strength as an intracellular signal. Trends in Biochemical Sciences 12:339–344
     [Google Scholar]
  17. Hutkins R. W., , Ellefson W. L., & Kashet E. R. 1987; Betaine transport imparts osmotolerance on a strain of Lactobacillus acidophilus . Applied and Environmental Microbiology 53:2275–2281
     [Google Scholar]
  18. Ikuta S., , Matuura K., , Imamura S., & Horituti Y. 1977; Oxidative pathway of choline to betaine in the soluble fraction prepared from Arthrobacter globiformis . Journal of Biochemistry 82:157–163
     [Google Scholar]
  19. Imhoff J. F., & Rodriguez-Valera F. 1984; Betaine is the main compatible solute of halophilic eubacteria. Journal of Bacteriology 160:478–479
     [Google Scholar]
  20. Imhoff J. F., & Truper H. G. 1977; Ectothiorhodospira halochloris sp. nov., a new extremely halophilic phototrophic bacterium containing bacteriochlorophyll b. Archives of Microbiology 114:115–121
     [Google Scholar]
  21. Imhoff J. F., , Hashwa F. F., & Trüper H. G. 1978; Isolation of extremely halophilic phototrophic bacteria from the alkaline Wadi Natrun, Egypt. Archives of Hydrobiology 84:381–388
     [Google Scholar]
  22. Ken-Oror S., , Preger R., & Av1-D0R Y. 1986; Role of betaine in the control of respiration and osmoregulation of a halotolerant bacterium. FEMS Microbiology Reviews 39:115–120
     [Google Scholar]
  23. Koo S.-P., , Higgins F., & Booth I. R. 1991; Regulation of compatible solute accumulation for a glycine betaine efflux system. Journal of General Microbiology 137:2617–2625
     [Google Scholar]
  24. Le Rudulier D., & Bouillard L. 1983; Glycine betaine, an osmotic effector of Klebsiella pneumoniae and other members of the Enterobacteriaceae . Applied and Environmental Microbiology 46:152–159
     [Google Scholar]
  25. Le Rudulier D., , Yang S. S., & Csonka L. N. 1982; Nitrogen fixation in Klebsiella pneumoniae during osmotic stress. Effect of exogenous praline or a praline overproducing plasmid. Biochimica et Biophysica Acta 719:273–283
     [Google Scholar]
  26. Le Rudulier D., , Gloux K., & Riou N. 1991; Identification of an osmotically induced periplasmic glycine betaine-binding protein from Rhizobium meliloti . Biochimica et Biophysica Acta 1061:197–205
     [Google Scholar]
  27. Matheron R., & Baulaigue R. 1972; Bacteries photosynthetiques sulfureuses marines. Assimilation des substances organiques et minerales et influence de la tenuer en chlorure de sodium du milieu de culture sur leur developpement. Archives of Microbiology 86:291–304
     [Google Scholar]
  28. May G., , Faatz E., , Villarejo M., & Bremer E. 1986; Binding protein dependent transport of glycine betaine and its osmotic regulation in Escherichia coli K12. Molecular and General Genetics 205:225–233
     [Google Scholar]
  29. Meyer B. 1987 ATPase und ATP-Synthese in Ectothiorhodospira halochloris. Doctoral thesis University of Bonn, Germany:
     [Google Scholar]
  30. Mohammad F. A. A., , Reed R.H., & Stewart W. D. P. 1983; The halophilic cyanobacterium Synechocystis DUN 52 and its osmotic responses. FEMS Microbiology Letters 16:287–290
     [Google Scholar]
  31. Moore D. J., , Reed R.H., & Stewart W. D. P. 1987; A glycine betaine transport system in Aphanothece halophytica and other glycine betaine-synthesizing cyanobacteria. Archives of Microbiology 147:399–405
     [Google Scholar]
  32. Oren A. 1990; Formation and breakdown of glycine betaine and trimethylamine in hypersaline environments. Antonie van Leeuwenhoek 58:291–298
     [Google Scholar]
  33. Peters P., , Galinski E. A., & Truper H. G. 1990; The biosynthesis of ectoine. FEMS Microbiology Letters 71:157–162
     [Google Scholar]
  34. Pierce. 1989 Review of assay protocol. In BCA Protein Assay Reagent, pp. 1–13 Pierce: USA;
     [Google Scholar]
  35. Rmu N., , Poggi M. C., & Le Rudulier D. 1991; Characterization of an osmoregulated periplasmic glycine betaine-binding protein in Azospirillum brasilense sp7. Biochimie 73:1187–1193
     [Google Scholar]
  36. Robertson D. E., , Roberts M. F., , Belay N., , Stetter K., & Boone D. R. 1990; Occurrence of p-glutamate, a novel osmolyte, in marine methanogenic bacteria. Applied and Environmental Microbiolgy 56:1504–1508
     [Google Scholar]
  37. Rowland I., & Tristram H. 1975; Specificity of the Escherichia coli proline transport system. Journal of Bacteriology 123:871–877
     [Google Scholar]
  38. Severin J., , Wohlfarth A., & Galinski E. A. 1992; The predominant role of recently discovered tetrahydropyrimidines for the osmoadaptation of halophilic eubacteria. Journal of General Microbiology 138:1629–1638
     [Google Scholar]
  39. Sutherland L., , Cairney J., , Elmore M. J., , Booth I. R., & Higgins C. F. 1986; Osmotic regulation of transcription: induction of the proU betaine transport gene is dependent on accumulation of intracellular potassium. Journal of Bacteriology 168:805–814
     [Google Scholar]
  40. Tschichholz I., & Truper H. G. 1990; Fate of compatible solutes during dilution stress in Ectothiorhodospira halochloris . FEMS Microbiology Ecology 73:181–186
     [Google Scholar]
  41. Warburg O., & Christian W. 1941; Isolierung und Kristallisation des Giirungsfermentes Enolase. Biochemische Zeitschrift 310:384–421
     [Google Scholar]
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Transport of glycine betaine in the extremely haloalkaliphilic sulphur bacterium Ectothiorhodospira halochloris
Microbiology 138, 1993 (1992); https://doi.org/10.1099/00221287-138-10-1993
/content/journal/micro/10.1099/00221287-138-10-1993
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