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. 1990 Jul;172(7):3631–3636. doi: 10.1128/jb.172.7.3631-3636.1990

Involvement of gamma-glutamyl peptides in osmoadaptation of Escherichia coli.

D McLaggan 1, T M Logan 1, D G Lynn 1, W Epstein 1
PMCID: PMC213336  PMID: 1972940

Abstract

Accumulation of K+ ions and glutamate plays a primary role in maintaining osmotic balance in Escherichia coli, as illustrated by the high concentrations of these ions present in cells growing in medium of high osmolality. We found that two gamma-glutamyl peptides and glutamine also accumulated during growth at high osmolarity. In a mutant unable to make trehalose growing in 1.3 osM medium, glutathione, gamma-glutamylglutamine, and glutamine accumulated to levels of 73, 33, and 140 mumol/g of protein, respectively. In such cells, K+ was present at 1,450 mumol/g of protein, indicating that glutathione and gamma-glutamylglutamine accounted for less than 10% of the low-molecular-weight anions accumulated with K+. However, glutathione is needed for wild-type osmotolerance in this species. A mutant deficient in glutathione because of an insertion in the gshA gene was unable to grow above 1.4 osM, grew more slowly at intermediate osmolarities, and took longer to adapt to growth following osmotic upshock. The involvement of glutathione in osmoregulation was independent of the effect of glutathione on K+ retention.

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Selected References

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  1. Anderson C. B., Witter L. D. Glutamine and proline accumulation by Staphylococcus aureus with reduction in water activity. Appl Environ Microbiol. 1982 Jun;43(6):1501–1503. doi: 10.1128/aem.43.6.1501-1503.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson M. E. Determination of glutathione and glutathione disulfide in biological samples. Methods Enzymol. 1985;113:548–555. doi: 10.1016/s0076-6879(85)13073-9. [DOI] [PubMed] [Google Scholar]
  3. Apontoweil P., Berends W. Glutathione biosynthesis in Escherichia coli K 12. Properties of the enzymes and regulation. Biochim Biophys Acta. 1975 Jul 14;399(1):1–9. doi: 10.1016/0304-4165(75)90205-6. [DOI] [PubMed] [Google Scholar]
  4. Bakker E. P., Booth I. R., Dinnbier U., Epstein W., Gajewska A. Evidence for multiple K+ export systems in Escherichia coli. J Bacteriol. 1987 Aug;169(8):3743–3749. doi: 10.1128/jb.169.8.3743-3749.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Booth I. R., Epstein W., Giffard P. M., Rowland G. C. Roles of the trkB and trkC gene products of Escherichia coli in K+ transport. Biochimie. 1985 Jan;67(1):83–89. doi: 10.1016/s0300-9084(85)80233-9. [DOI] [PubMed] [Google Scholar]
  6. Booth I. R. Regulation of cytoplasmic pH in bacteria. Microbiol Rev. 1985 Dec;49(4):359–378. doi: 10.1128/mr.49.4.359-378.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burchill B. R., Oliver J. M., Pearson C. B., Leinbach E. D., Berlin R. D. Microtubule dynamics and glutathione metabolism in phagocytizing human polymorphonuclear leukocytes. J Cell Biol. 1978 Feb;76(2):439–447. doi: 10.1083/jcb.76.2.439. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Castle A. M., Macnab R. M., Shulman R. G. Coupling between the sodium and proton gradients in respiring Escherichia coli cells measured by 23Na and 31P nuclear magnetic resonance. J Biol Chem. 1986 Jun 15;261(17):7797–7806. [PubMed] [Google Scholar]
  9. Csonka L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. doi: 10.1128/mr.53.1.121-147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Csonka L. N. Proline over-production results in enhanced osmotolerance in Salmonella typhimurium. Mol Gen Genet. 1981;182(1):82–86. doi: 10.1007/BF00422771. [DOI] [PubMed] [Google Scholar]
  11. Epstein W., Kim B. S. Potassium transport loci in Escherichia coli K-12. J Bacteriol. 1971 Nov;108(2):639–644. doi: 10.1128/jb.108.2.639-644.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Giaever H. M., Styrvold O. B., Kaasen I., Strøm A. R. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J Bacteriol. 1988 Jun;170(6):2841–2849. doi: 10.1128/jb.170.6.2841-2849.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Greenberg J. T., Demple B. Glutathione in Escherichia coli is dispensable for resistance to H2O2 and gamma radiation. J Bacteriol. 1986 Nov;168(2):1026–1029. doi: 10.1128/jb.168.2.1026-1029.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heinrikson R. L., Meredith S. C. Amino acid analysis by reverse-phase high-performance liquid chromatography: precolumn derivatization with phenylisothiocyanate. Anal Biochem. 1984 Jan;136(1):65–74. doi: 10.1016/0003-2697(84)90307-5. [DOI] [PubMed] [Google Scholar]
  15. Killham K., Firestone M. K. Salt stress control of intracellular solutes in streptomycetes indigenous to saline soils. Appl Environ Microbiol. 1984 Feb;47(2):301–306. doi: 10.1128/aem.47.2.301-306.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Larsen P. I., Sydnes L. K., Landfald B., Strøm A. R. Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose. Arch Microbiol. 1987 Feb;147(1):1–7. doi: 10.1007/BF00492896. [DOI] [PubMed] [Google Scholar]
  17. Liang C. M., Lee N., Cattell D., Liang S. M. Glutathione regulates interleukin-2 activity on cytotoxic T-cells. J Biol Chem. 1989 Aug 15;264(23):13519–13523. [PubMed] [Google Scholar]
  18. Measures J. C. Role of amino acids in osmoregulation of non-halophilic bacteria. Nature. 1975 Oct 2;257(5525):398–400. doi: 10.1038/257398a0. [DOI] [PubMed] [Google Scholar]
  19. Meister A., Anderson M. E. Glutathione. Annu Rev Biochem. 1983;52:711–760. doi: 10.1146/annurev.bi.52.070183.003431. [DOI] [PubMed] [Google Scholar]
  20. Meister A. Glutathione metabolism and its selective modification. J Biol Chem. 1988 Nov 25;263(33):17205–17208. [PubMed] [Google Scholar]
  21. Meury J., Kepes A. Glutathione and the gated potassium channels of Escherichia coli. EMBO J. 1982;1(3):339–343. doi: 10.1002/j.1460-2075.1982.tb01171.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Moon D. C., Kelley J. A. A simple desalting procedure for fast atom bombardment mass spectrometry. Biomed Environ Mass Spectrom. 1988 Sep;17(3):229–237. doi: 10.1002/bms.1200170312. [DOI] [PubMed] [Google Scholar]
  23. Munro G. F., Hercules K., Morgan J., Sauerbier W. Dependence of the putrescine content of Escherichia coli on the osmotic strength of the medium. J Biol Chem. 1972 Feb 25;247(4):1272–1280. [PubMed] [Google Scholar]
  24. Richey B., Cayley D. S., Mossing M. C., Kolka C., Anderson C. F., Farrar T. C., Record M. T., Jr Variability of the intracellular ionic environment of Escherichia coli. Differences between in vitro and in vivo effects of ion concentrations on protein-DNA interactions and gene expression. J Biol Chem. 1987 May 25;262(15):7157–7164. [PubMed] [Google Scholar]
  25. Smith L. T., Smith G. M. An osmoregulated dipeptide in stressed Rhizobium meliloti. J Bacteriol. 1989 Sep;171(9):4714–4717. doi: 10.1128/jb.171.9.4714-4717.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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