1887

Abstract

Exogenously supplied L-pipecolic acid was accumulated by cells and protected them while growing at inhibitory osmolarity. Using specific uptake mutants and competitive assays, we established that the imino acid enters the cells through the ProP and ProU systems with values of 225 and 53 μM, respectively. Surprisingly, in spite of the requirement for the wild-type gene for osmoprotective ability, no binding activity of labelled pipecolate with the periplasmic protein encoded by could be detected. In an attempt to demonstrate whether the two porters (ProP and ProU) are the only carriers involved in osmoregulation, a variety of molecules known for their intracellular osmolarity-dependent accumulation in various organisms were investigated. -Dimethylproline (proline betaine), -dimethylglycine, homobetaine (β-alanine betaine), γ-butyrobetaine and dimethylsulfonio-propionate were found to be capable of promoting the growth of osmotically stressed . All of these molecules enter bacterial cells via ProP and ProU porters. None of the osmoprotectants except -dimethylproline was able to bind the periplasmic protein encoded by , while this protein was necessary for their uptake. Apparently, ProP and ProU are the sole osmoporters involved in osmolyte influx into cells.

Loading

Article metrics loading...

/content/journal/micro/10.1099/13500872-140-9-2415
1994-09-01
2024-12-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/140/9/mic-140-9-2415.html?itemId=/content/journal/micro/10.1099/13500872-140-9-2415&mimeType=html&fmt=ahah

References

  1. Anthoni U., Christophersen C., Hougaard L., Nielsen P. H. 1991; Quaternary ammonium compounds in the biosphere -an example of a versatile adaptative strategy. Comp Biochem Physiol 99B:1–18
    [Google Scholar]
  2. Argast M., Boos W. 1979; Purification and properties of the sn- glycerol 3-phosphate-binding protein of Escherichia coli. J Biol Chem 254:10931–10935
    [Google Scholar]
  3. Barron A., Jung J. U., Villarejo M. 1987; Purification and characterization of a glycine betaine binding protein from Escherichia coli. J Biol Chem 262:11841–11846
    [Google Scholar]
  4. Bernard T., Pocard J.-A., Perroud B., Le Rudulier D. 1986; Variations in the response of salt-stressed Khizobium strains to betaines.. Arch Microbiol 143:359–364
    [Google Scholar]
  5. Blunden G., Gordon S. 1986; Betaines and their sulphonio analogues in marine algae. Prop Physiol 4:39–80
    [Google Scholar]
  6. Cairney J., Booth I. R., Higgins C. F. 1985; Salmonella typhimurium pro P gene encodes a transport system for the osmoprotectant betaine. J Bacteriol 164:1218–1223
    [Google Scholar]
  7. Casadaban M.J. 1976; Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol 104:541–555
    [Google Scholar]
  8. Chambers S.T., Kunin C. M. 1987; Osmoprotective activity for E.rcherichia coli in mammalian renal inner medulla and urine. Correlation of glycine and proline betaines and sorbitol with response to osmotic loads.. J Clin Invest 80:1255–1260
    [Google Scholar]
  9. Chang Y.-F., Ghosh P., Rao V. V. 1990; L-pipecolic acid metabolism in human liver L-OC aminoadipate d-semialdehvde reductase.. Biochim Biophys Acta 1038:300–305
    [Google Scholar]
  10. Csonka L.N. 1989; Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev 53:121–147
    [Google Scholar]
  11. Csonka L.N., Hanson A. D. 1991; Prokaryotic osmoregulation: genetics and physiology. Annu Rev Microbiol 45:569–606
    [Google Scholar]
  12. Dattananda C.S., Gowrishankar J. 1989; Osmoregulation in Escherichia coli: complementation analysis and gene-protein relationship in the pro U locus. J Bacterial 171:1915–1922
    [Google Scholar]
  13. Dinnbier U., Limpinsel E., Schmid R., Bakker E. P. 1988; Transient accumulation of potassium glutamate and its replacement bv trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations.. Arch Microbiol 150:348–357
    [Google Scholar]
  14. Gouesbet G., Blanco C., Hamelin J., Bernard T. 1992; Osmotic adjustment in Brevibacterium ammoniagenes: pipecolic acid accumulation at elevated osmolalities.. J Gen Microbiol 138:959–965
    [Google Scholar]
  15. Gowrishankar J. 1985; Identification of osmoresponsive genes in Escherichia coli: evidence for participation of potassium and proline transport systems in osmoregulation. J Bacteriol 164:434–445
    [Google Scholar]
  16. Gowrishankar J. 1986; pro P-mediated proline transport also plays a role in Escherichia coli osmoregulation. J Bacteriol 166:331–333
    [Google Scholar]
  17. Grothe S., Krogsrud R. L., McClellan D. J., Milner J. L., Wood J. M. 1986; Proline transport and osmotic stress response in E. coli K-12. J Bacteriol 166:253–259
    [Google Scholar]
  18. Ikuta S., Matuura K., Imamura S., Misaki H., Horiuti Y. 1977; Oxidative pathway of choline to betaine in the soluble fraction prepared from Artbrobacter globijormis.. J Biochem 82:157–163
    [Google Scholar]
  19. Imhoff J.F. 1986; Osmoregulation and compatible solutes in eubacteria. FEMS Microbiol Rev 39:57–66
    [Google Scholar]
  20. Jebbar M., Talibart R., Gloux K., Bernard T., Blanco C. 1992; Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics. J Bacteriol 174:5027–5035
    [Google Scholar]
  21. Lai M.-C., Sowers K. R., Robertson D. E., Roberts M. F., Gunsalus R. P. 1991; Distribution of compatible solutes in the halophilic methanogenic archaebacteria. J Bacteriol 173:5352–5358
    [Google Scholar]
  22. Larsen P. I., Sydnes L. K., Landfald B., Strom A. R. 1987; Osmoregulation in Escherichia coli by accumulation of organic osmolytes: betaines, glutamic acid, and trehalose.. Arch Microbiol 147:1–7
    [Google Scholar]
  23. Le Rudulier D., Bernard T. 1986; Salt tolerance in Rhiryobium: a possible role for betaines.. FEMS Microbiol Rev 39:67–72
    [Google Scholar]
  24. Le Rudulier D., Bernard T., Goas G., Hamelin J. 1984; Osmoregulation in Klebsiella pneumoniae: enhancement of anaerobic growth and nitrogen fixation under stress by proline betaine, γ-butyrobetaine, and other related compounds.. Can J Microbiol 30:299–305
    [Google Scholar]
  25. Le Rudulier D., Gloux K., Riou N. 1991; Identification of an osmotically induced periplasmic glycine betaine-binding protein from Rhiryobium meliloti. Biochim Biophys Acta 1061:197–205
    [Google Scholar]
  26. Lucht J.M., Bremer E. 1991; Characterization of mutations affecting the osmoregulated pro U promoter of Escherichia coli and identification of 5' sequences required for high-level expression. J Bacteriol 173:801–809
    [Google Scholar]
  27. Mason T.G., Blunden G. 1989; Quaternary ammonium and tertiary sulphonium compounds of algal origin as alleviators ot osmotic stress. Bot Alar 32:313–316
    [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.. Mol Gen Genet 205:225–233
    [Google Scholar]
  29. McLaggan D., Epstein W. 1991; Escherichia coli accumulates the eukaryotic osmolyte taurine at high osmolarity.. FEMS Microbiol Lett 81:209–214
    [Google Scholar]
  30. Miller J.H. 1972 Experiments in Slolecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [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-synthesising cyanobacteria.. Arch Microbiol 147:399–405
    [Google Scholar]
  32. Neu H., Heppel L. A. 1965; The release of enzymes from Escherichia coli by osmotic shock and during the formation of spheroplasts. J Biol Chem 240:3685–3692
    [Google Scholar]
  33. Perroud B., Le Rudulier D. 1985; Glycine betaine transport in Escherichia coli: osmotic modulation. J Bacteriol 161:393–401
    [Google Scholar]
  34. Rhodes D., Hanson A. D. 1993; Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384
    [Google Scholar]
  35. Richarme G., Kepes A. 1983; Study of binding protein-ligand interaction by ammonium sulfate-assisted adsorption on cellulose ester filters. Biochim Biophys Acta 742:16 –24
    [Google Scholar]
  36. Romeo J.T., Prass W. A. 1977; Proline-pipecolic acid accumulation in xeric Ptelea species.. Plant Physiol 5992
    [Google Scholar]
  37. Stewart G.R., Larher F. 1980; Accumulation of amino acids and related compounds in relation to environmental stress. Biochem Plants 5:609–635
    [Google Scholar]
  38. Strom A. R., Falkenberg P., Landfald B. 1986; Genetics of osmoregulation in Escherichia coli: uptake and biosynthesis of organic osmolytes.. FEMS Alicrobiol Rev 39:79–86
    [Google Scholar]
  39. Triiper H.G., Galinski E. A. 1990; Biosynthesis and fate of compatible solutes in extremely halophilic phototrophic eubacteria. FEMS Alicrobiol Rev 75:247–254
    [Google Scholar]
  40. Yancey P. H., Clark M. E., Hand S. C., Bowlus R. D., Somero G. N. 1982; Living with water stress: evolution of osmolyte systems. Science 217:1214–1222
    [Google Scholar]
  41. Zaar K., Angermuller S., Volkl A., Fahimi H. D. 1986; Pipecolic acid is oxidized by renal and hepatic peroxisomes.. J Exp Cell Res 164:267–271
    [Google Scholar]
/content/journal/micro/10.1099/13500872-140-9-2415
Loading
/content/journal/micro/10.1099/13500872-140-9-2415
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