1887

Abstract

Outer membranes were isolated from iron-limited and iron-sufficient ATCC 12334 by sucrose density centrifugation or treatment with Sarkosyl. Analysis of the outer membranes by sodium dodecyl sulphate polyacrylamide gel electrophoresis revealed that iron-limited cells produced greater amounts of two proteins of apparent molecular mass 74 kDa and 70 kDa than iron-sufficient cells. The enhanced production of these two proteins was evident when media contained less than 9·7 μ added iron with maximum production occurring when media contained less than 1·1 μ added iron. Iron-limited growth conditions also caused ATCC 12334 to excrete a visible yellow, blue-white fluorescent compound into culture supernatant fluids with maximum levels being produced in media that contained less than 1·1 μ added iron. This fluorescent compound had a distinctive pH-dependent absorption maximum characteristic of pyoverdin-type siderophores and appeared to bind iron. Furthermore, culture supernatant fluids containing the fluorescent compound promoted the uptake of Fe in ATCC 12334 cells. Three other strains, NCIB 10958, NCIB 8700 and NCIB 9129, produced iron-repressible outer-membrane proteins but only the former two strains produced the iron-repressible fluorescent compound. It is proposed that the iron-regulated proteins and fluorescent compound produced by may function in high-affinity iron uptake.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-135-5-1229
1989-05-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/135/5/mic-135-5-1229.html?itemId=/content/journal/micro/10.1099/00221287-135-5-1229&mimeType=html&fmt=ahah

References

  1. Armstrong J.McD. 1964; The molar extinction coefficient of 2,6-dichlorophenol indophenol. Biochimica et biophysica acta 86:194–197
    [Google Scholar]
  2. Bachhawat A.K., Ghosh S. 1987; Isolation and characterization of the outer membrane proteins of Azospirillum brasilense . Journal of General Microbiology 133:1751–1758
    [Google Scholar]
  3. Bingle W.H., Doran J.L., Page W.J. 1984; Regular surface layer of Azotobacter vinelandii . Journal of Bacteriology 159:251–259
    [Google Scholar]
  4. Brown M.R.W., Anwar H., Lambert P.A. 1984; Evidence that mucoid Pseudomonas aeruginosa in the cystic fibrosis lung grows under iron- restricted conditions. FEMS Microbiology Letters 21:113–117
    [Google Scholar]
  5. Chopra I., Shales S.W. 1980; Comparison of the polypeptide composition of Escherichia coli outer membranes prepared by two methods. Journal of Bacteriology 144:425–427
    [Google Scholar]
  6. Cody Y.S., Gross D.C. 1987; Outer membrane protein mediating iron uptake via pyoverdinpss, the fluorescent siderophore produced by Pseudomonas syringae pv. syringae . Journal of Bacteriology 169:2207–2214
    [Google Scholar]
  7. Collinson S.K., Doran J.L., Page W.J. 1987; Production of 3,4-dihydroxybenzoic acid by Azo- monas macrocytogenes and Azotobacter paspali . Canadian Journal of Microbiology 33:169–175
    [Google Scholar]
  8. Cox C.D., Adams P. 1985; Siderophore activity of pyoverdin for Pseudomonas aeruginosa . Infection and Immunity 48:130–138
    [Google Scholar]
  9. Demange P., Wendenbaum S., Bateman A., Dell A., Meyer J.M., Abdallah M.A. 1986; Bacterial siderophores: structure of pyoverdins and related compounds. In Iron, Siderophores, and Plant Diseases pp 131–147 Swinburne T. R. Edited by New York: Plenum Press;
    [Google Scholar]
  10. Demange P., Wendenbaum S., Bateman A., Dell A., Abdallah M.A. 1987; Bacterial siderophores : structure and physicochemical properties of pyoverdins and related compounds. In Iron Transport in Microbes, Plants and Animals pp 167–187 Winkelmann G., Van der Helm D., Neilands J. B. Edited by Weinheim, FRG: VCH Verlagsgesellschaft;
    [Google Scholar]
  11. Demange P., Bateman A., Dell A., Abdallah M.A. 1988; Structure of azotobactin D, a siderophore of Azotobacter vinelandii strain D (CCM 289). Biochemistry 27:2745–2752
    [Google Scholar]
  12. De Smedt J., Bauwens M., Tytgat R., De Ley J. 1980; Intra- and intergeneric similarities of riboso- mal ribonucleic acid cistrons of free-living, nitrogenfixing bacteria. International Journal of Systematic Bacteriology 30:106–122
    [Google Scholar]
  13. De Weger L.A., Van Boxtel R., Van Der Burg B., Gruters R.A., Geels F.P., Schippers B., Lugtenberg B. 1986; Siderophores and outer membrane proteins of antagonistic, plant-growth- stimulating, root-colonizing Pseudomonas spp. Journal of Bacteriology 165:585–594
    [Google Scholar]
  14. Ells H.A. 1959; A colorimetric method for the assay of soluble succinic dehydrogenase and pyridine- nucleotide-linked dehydrogenases. Archives of Biochemistry and Biophysics 85:561–562
    [Google Scholar]
  15. Fairbanks G., Steck T.L., Wallach D.F.H. 1971; Electrophoretic analysis of the major polypeptides of the human erythrocyte membrane. Biochemistry 10:2606–2617
    [Google Scholar]
  16. Filip C., Fletcher G., Wulff J.L., Earhart C.F. 1973; Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. Journal of Bacteriology 115:717–722
    [Google Scholar]
  17. Gerhardt B., Beevers H. 1968; Influence of sucrose on protein determination by the Lowry procedure. Analytical Biochemistry 24:337–352
    [Google Scholar]
  18. Greenwood N.N., Earnshaw A. 1984; Iron, ruthenium, and osmium. In Chemistry of the Elements pp 1242–1289 Oxford: Pergamon Press;
    [Google Scholar]
  19. Griffiths E. 1983; Availability of iron and survival of bacteria in infection. In Medical Microbiology 3 pp 153–177 Easmon C. S. F., Jeljaszewicz J., Brown M. R. W., Lambert P. A. Edited by London: Academic Press;
    [Google Scholar]
  20. Healy W.B., Cheng S.-C., Mcelroy W.D. 1955; Metal toxicity and iron deficiency effects on enzymes in Neurospora . Archives of Biochemistry and Biophysics 54:206–214
    [Google Scholar]
  21. Hinton , Burge M.L.E., Hartman G.C. 1969; Sucrose interference in the assay of enzymes and protein. Analytical Biochemistry 29:248–256
    [Google Scholar]
  22. Hoe M., Wilkinson B.J., Hindahl M.S. 1985; Outer membrane proteins induced upon iron deprivation of Paracoccus denitrificans . Biochimica et biophysica acta 813:338–342
    [Google Scholar]
  23. Johnstone D.B. 1957; The use of a fluorimeter in the characterization of fluorescing substances elaborated by Azotobacter . Applied Microbiology 5:103–106
    [Google Scholar]
  24. Johnstone D.B., Pfeffer M., Blanchard G.C. 1958; Fluorescence of Azotobacter, its chemical nature and bacteriological significance. In. VII International Congress for Microbiology 4-9 Aug.1958, Stockholm (abstracts) pp 386–387 Tunevall G. Edited by Uppsala, Sweden: Almquist & Wiksells;
    [Google Scholar]
  25. Kasahara M., Anraku Y. 1974; Succinate dehydrogenase of Escherichia coli membrane vesicles. Journal of Biochemistry 76:959–966
    [Google Scholar]
  26. Knosp O., Von Tigerstrom M., Page W.J. 1984; Siderophore-mediated uptake of iron in Azotobacter vinelandii . Journal of Bacteriology 159:341–347
    [Google Scholar]
  27. Laemmli U.K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227:680–685
    [Google Scholar]
  28. Lugtenberg B., Van Alphen L. 1983; Molecular architecture and functioning of the outer membrane of Escherichia coli and other gram-negative bacteria. Biochimica et biophysica acta 737:51–115
    [Google Scholar]
  29. Magazin M.D., Moores J.C., Leong J. 1986; Cloning of the gene coding for the outer membrane receptor protein for ferric pseudobactin, a siderophore from a plant growth-promoting Pseudomonas strain. Journal of Biological Chemistry 261:795–799
    [Google Scholar]
  30. Menichi B., Buu A. 1986; Peptidoglycan association of bacteriophage T5 receptor in Escherichia coli K-12. Journal of Bacteriology 166:1137–1140
    [Google Scholar]
  31. Meyer J.M., Abdallah M.A. 1978; The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. Journal of General Microbiology 107:319–328
    [Google Scholar]
  32. Meyer J.M., Mock M., Abdallah M.A. 1979; Effect of iron on the protein composition of the outer membrane of fluorescent pseudomonads. FEMS Microbiology Letters 5:395–398
    [Google Scholar]
  33. Mizuno T., Kageyama M. 1978; Separation and characterization of the outer membrane of Pseudomonas aeruginosa . Journal of Biochemistry 84:179–191
    [Google Scholar]
  34. Neilands J.B. 1981; Microbial iron compounds. Annual Review of Biochemistry 50:715–731
    [Google Scholar]
  35. Neilands J.B. 1982; Microbial envelope proteins related to iron. Annual Review of Microbiology 36:285–309
    [Google Scholar]
  36. Neilands J.B. 1984; Siderophores of bacteria and fungi. Microbiological Sciences 1:9–14
    [Google Scholar]
  37. Osborn M.J., Gander J.E., Parisi E., Carson J. 1972; Mechanism of assembly of the outer membrane of Salmonella typhimurium, isolation and characterization of cytoplasmic and outer membrane. Journal of Biological Chemistry 247:3962–3972
    [Google Scholar]
  38. Page W.J. 1987; Iron-dependent production of hydroxamate by sodium-dependent Azotobacter chroococcum . Applied and Environmental Microbiology 53:1418–1424
    [Google Scholar]
  39. Page W.J., Collinson S.K. 1987; Characterization of Azomonas macrocytogenes strains isolated from Alberta soils. Canadian Journal of Microbiology 33:830–833
    [Google Scholar]
  40. Page W.J., Huyer M. 1984; Derepression of the Azotobacter vinelandii siderophore system, using iron-containing minerals to limit iron repletion. Journal of Bacteriology 158:496–502
    [Google Scholar]
  41. Page W.J., Sadoff H.L. 1976; Physiological factors affecting transformation of Azotobacter vinelandii . Journal of Bacteriology 125:1080–1087
    [Google Scholar]
  42. Page W.J., Von Tigerstrom M. 1982; Iron- and molybdenum-repressible outer membrane proteins in competent Azotobacter vinelandii . Journal of Bacteriology 151:237–242
    [Google Scholar]
  43. Page W.J., Von Tigerstrom M. 1988; Aminoche- lin, a catecholamine siderophore produced by Azotobacter vinelandii . Journal of General Microbiology 134:453–460
    [Google Scholar]
  44. Philson S.B., Llinäs M. 1982; Siderochromes from Pseudomonas fluorescens . Journal of Biological Chemistry 257:8081–8085
    [Google Scholar]
  45. Schnaitman C.A. 1970; Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli . Journal of Bacteriology 104:890–901
    [Google Scholar]
  46. Spiro TH.G., Saltman P. 1969; Polynuclear complexes of iron and their biological implications. Structure and Bonding 6:116–156
    [Google Scholar]
  47. Thompson J.P., Skerman V.B.D. 1979; Azotobacteraceae: The Taxonomy and Ecology of the Aerobic Nitrogen-Fixing Bacteria, pp. 196- 197304 London: Academic Press;
    [Google Scholar]
  48. Torres L., Pérez-Ortin J.E., Tordera V., Beltrán J.P. 1986; Isolation and characterization of an Fe(III)-chelating compound produced by Pseudomonas syringae . Applied and Environmental Microbiology 52:157–160
    [Google Scholar]
  49. Westervelt P., Bloom M.L., Mabbott G.A., Fekete F.A. 1985; The isolation and identification of 3,4-dihydroxybenzoic acid formed by nitrogen-fixing Azomonas macrocytogenes . FEMS Microbiology tetters 30:331–335
    [Google Scholar]
  50. Williams P., Brown M.R.W., Lambert P.A. 1984; Effect of iron deprivation on the production of siderophores and outer membrane proteins in Klebsiella aerogenes . Journal of General Microbiology 130:2357–2365
    [Google Scholar]
  51. Winder F.G., O’HARA C. 1964; Effects of iron deficiency and of zinc deficiency on the activities of some enzymes in Mycobacterium smegmatis . Biochemical Journal 90:122–126
    [Google Scholar]
  52. Wright A.C., Simpson L.ML, Maneval D.R. Jr Oliver J.D., Morris J.G. Jr 1986; Siderophore production and outer membrane proteins of selected Vibrio vulnificus strains under conditions of iron limitation. FEMS Microbiology tetters 35:255–260
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-135-5-1229
Loading
/content/journal/micro/10.1099/00221287-135-5-1229
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