1887

Abstract

In iron-limited medium, Azotobacter vinelandii strain UW produces three catecholate siderophores: the tricatecholate protochelin, the dicatecholate azotochelin and the monocatecholate aminochelin. Each siderophore was found to bind Fe preferentially to Fe, in a ligand:Fe ratio of 1:1, 3:2 and 3:1, respectively. Protochelin had the highest affinity for Fe, with a calculated proton-independent solubility coefficient of 10, comparable to ferrioxamine B. Iron-limited wild-type strain UW grown under N-fixing or nitrogen-sufficient conditions hyper-produced catecholate siderophores in response to oxidative stress caused by high aeration. In addition, superoxide dismutase activity was greatly diminished in iron-limited cells, whereas catalase activity was maintained. The ferredoxin I (Fdl)-negative A. vinelandii strain LM100 also hyper-produced catecholates, especially protochelin, under oxidative stress conditions, but had decreased activities of both superoxide dismutase and catalase, and was about 10 times more sensitive to paraquat than strain UW. Protochelin and azotochelin held Fe firmly enough to prevent its reduction by.O and did not promote the generation of hydroxyl radical by the Fenton reaction. Ferric-aminochelin was unable to resist reduction by O and was a Fenton catalyst. These data suggest that under iron-limited conditions, A. vinelandii suffers oxidative stress caused by.O . The catecholate siderophores azotochelin, and especially protochelin, are hyper-produced to offer chemical protection from oxidative damage catalysed by.O and Fe. The results are also consistent with Fdl being required for oxidative stress management in A. vinelandii.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-144-7-1747
1998-07-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/micro/144/7/mic-144-7-1747.html?itemId=/content/journal/micro/10.1099/00221287-144-7-1747&mimeType=html&fmt=ahah

References

  1. Allgood G.S., Perry J.J. 1985; Oxygen defense systems in obligately thermophilic bacteria.. Can J Microbiol 31:1006–1010
    [Google Scholar]
  2. Barnum D.W. 1977; Spectrophotometric determination of catechol, epinephrine, DOPA, dopamine and other aromatic vic- diols.. Anal Chim Acta 89:157–166
    [Google Scholar]
  3. Beauchamp C., Fridovich I. 1971; Superoxide dismutase: improved assays and an assay applicable to acrylamide gels.. Anal Biochem 44:276–287
    [Google Scholar]
  4. Beyer W.F., Fridovich I. 1991; In vivo competition between iron and manganese for occupancy of the active site region of the manganese-superoxide dismutase of Escherichia coli. . J Biol Chem 266:303–308
    [Google Scholar]
  5. Bishop P. 1993; Three genetically distinct nitrogenase systems in Azotobacter vinelandii. . In Iron Chelation in Plants and Soil Microorgansims pp. 301–324 Edited by Barton L., Hemming B. C. San Diego: Academic Press;
    [Google Scholar]
  6. Carrano C.J., Raymond K.N. 1978; Coordination chemistry of microbial iron transport compounds. 10. Characterization of the complexes of rhodotorulic acid, a dihydroxamate siderophore.. J Am Chem Soc 100:5371–5374
    [Google Scholar]
  7. Chaberek S., Martell A.E. 1959 Organic Sequestering Agents New York: Wiley;
    [Google Scholar]
  8. Clare D.A., Duong M.N., Darr D., Archibald F., Fridovich I. 1984; Effects of molecular oxygen on detection of superoxide radical with nitroblue tetrazolium and on activity stains for catalase.. Anal Biochem 140:532–537
    [Google Scholar]
  9. Coffman T.J., Cox C.D., Edeker B.L., Britigan B.E. 1990; Possible role of bacterial siderophores in inflammation. Iron bound to the Pseudomonas siderophore pyochelin can function as a hydroxyl radical catalyst.. J Clin Invest 86:1030–1037
    [Google Scholar]
  10. Cohen G. 1994; Enzymatic/nonenzymatic sources of oxyradicals and regulation of antioxidant defenses.. Ann N Y Acad Sci 738:8–14
    [Google Scholar]
  11. Corbin J.L., Bulen W.A. 1969; The isolation and identification of 2,3-dihydroxybenzoic acid and 2-N,6-N-di(2,3-dihydroxy- benzoyl)-L-lysine formed by iron-deficient Azotobacter vinelandii. . Biochemistry 8:757–762
    [Google Scholar]
  12. Cornish A.S., Page W.J. 1995; Production of the tricatecholate siderophore protochelin by Azotobacter vinelandii. . BioMetals 8:332–338
    [Google Scholar]
  13. Demple B. 1996; Redox signaling and gene control in Escherichia coli soxRS oxidative stress regulon - a review.. Gene 179:53–57
    [Google Scholar]
  14. DiGuiseppi J., Fridovich I. 1984; The toxicity of molecular oxygen.. Crit Rev Toxicol 12:315–343
    [Google Scholar]
  15. Fridovich I. 1986; Biological effects of the superoxide radical.. Arch Biochem Biophys 247:1–11
    [Google Scholar]
  16. Guerinot M.L. 1994; Microbial iron transport.. Annu Rev Microbiol 48:743–772
    [Google Scholar]
  17. Harris W.R., Carrani C.J., Cooper S.R., Sofen S.R., Avdeef A.E., McArdle J.V., Raymond K.N. 1979; Coordination chemistry of microbial iron transport compounds. 19. Stability constants and electrochemical behavior of ferric enterobactin and model complexes.. J Am Chem Soc 101:6097–6104
    [Google Scholar]
  18. Hassett D.J., Sokol P.A., Howell M.L., Ma J.-F., Schweitzer H.T., Ochsner U., Vasil M.L. 1996; Ferric uptake regulator (Fur) mutants of Pseudomonas aeruginosa demonstrate defective siderophore-mediated iron uptake, altered aerobic growth, and decreased superoxide dismutase and catalase activities.. J Bacterial 178:3996–4003
    [Google Scholar]
  19. Hider R.C. 1984; Siderophore mediated absorption of iron.. In Structure and Bonding: Siderophores from Microorganisms and Plants 58 pp. 26–87 Edited by Clarke M. J., Ibers J. A., Mingos D. M. P., Palmer G. A., Sadler P. J., Williams R. J. P. Berlin: Springer;
    [Google Scholar]
  20. Isas J.M., Yannone S.M., Burgess B.K. 1995; Azotobacter vinelandii NADPH: ferredoxin reductase cloning, sequencing, and overexpression.. J Biol Chern 36:21258–21263
    [Google Scholar]
  21. Jurtshuk P., Yang T. 1980; Oxygen reactive hemoprotein components in bacterial respiratory systems.. In Diversity of Bacterial Respiratory Systems pp. 138–59 Editied by Knowles C. J. Boca Raton, FL: CRC Press;
    [Google Scholar]
  22. Jurtshuk P., Jong-Kang L., Moore E.R.B. 1984; Comparative cytochrome oxidase and superoxide dismutase analyses on strains of Azotobacter vinelandii and other related free-living nitrogenfixing bacteria.. Appl Environ Microbiol 47:1185–1187
    [Google Scholar]
  23. Kolonay J.F. Jr Farhad M., Gennis R.B., Kaysser T.M., Maier R.J. 1994; Purification and characterization of the cytochrome bd complex from Azotobacter vinelandii: comparison to the complex from Escherichia coli. . J Bacteriol 176:4177–4181
    [Google Scholar]
  24. Korbashi P., Kohen R., Katzhendler J., Chevion M. 1986; Iron mediates paraquat toxicity in Escherichia coli. . J Biol Chern 261:12472–12476
    [Google Scholar]
  25. Loomis D.L., Raymond K.N. 1991; Solution equilibria of enterobactin and metal-enterobactin complexes.. Inorg Chern 30:906–911
    [Google Scholar]
  26. de Lorenzo V., Wee S., Herrero M., Neilands J.B. 1987; Operator sequences of the aerobactin operon of plasmid ColV- K30 binding the ferric uptake regulation (fur) repressor.. J Bacteriol 169:2624–2630
    [Google Scholar]
  27. Mehrotra M. 1997 Role of iron in the regulation of phenyl- alanyl-tRNA synthetase activity in Azotobacter vinelandii PhD thesis University of Alberta;
    [Google Scholar]
  28. Morgan T.V., Lundell D.J., Burgess B.K. 1988; Azotobacter vinelandii ferredoxin. I. Cloning, sequencing, and mutant analysis.. J Biol Chern 263:1370–1375
    [Google Scholar]
  29. Neilands J.B. 1981; Microbial iron compounds.. Annu Rev Biochem 50:715–731
    [Google Scholar]
  30. Niederhoffer E.C., Naranjo C.M., Bradley K.L., Fee J.A. 1990; Control of Escherichia coli superoxide dismutase (sodA and sodB) genes by ferric uptake regulation (fur) locus.. J Bacteriol 172:1930–1938
    [Google Scholar]
  31. Oberley L.W., Spitz D.R. 1985; Nitroblue tetrazolium.. In CRC Handbook of Methods for Oxygen Radical Research pp. 217–220 Edited by Greenwald R. A. Boca Raton, FL: CRC Press;
    [Google Scholar]
  32. Page W.J., Huyer M. 1984; Derepression of the Azotobacter vinelandii siderophore system, using iron-containing minerals to limit iron repletion.. J Bacteriol 158:496–502
    [Google Scholar]
  33. Page W.J., Shivprasad S. 1995; Iron binding to Azotobacter salinestris melanin, iron mobilization and uptake mediated by siderophores.. BioMetals 8:59–64
    [Google Scholar]
  34. Page W.J., von Tigerstrom M. 1982; Iron- and molybdenum- repressible outer membrane proteins in competent Azotobacter vinelandii. . J Bacteriol 151:237–242
    [Google Scholar]
  35. Page W.J., von Tigerstrom M. 1988; Aminochelin, a catecholamine siderophore produced by Azotobacter vinelandii. . J Gen Microbiol 134:453–460
    [Google Scholar]
  36. Reid R.T., Live D.H., Faulkner D.J., Butler A. 1993; A siderophore from a marine bacterium with an exceptional ferric ion affinity constant.. Nature 336:455–458
    [Google Scholar]
  37. Shivprasad S., Page W.J. 1989; Catechol formation and melanization by Na+-dependent Azotobacter chroococcum: a protective mechanism for aeroadaptation ?. Appl Environ Microbiol 55:1811–1817
    [Google Scholar]
  38. Sinha A.K. 1972; Colormetric assay of catalase.. Anal Biochem 47:389–394
    [Google Scholar]
  39. Stookey L.L. 1970; Ferrozine - a new spectrophotometric reagent for iron.. Anal Chern 42:779–781
    [Google Scholar]
  40. Thompson A.J. 1991; Does ferredoxin I (Azotobacter) represent a novel class of DNA-binding proteins that regulate gene expression in response to cellular iron(II) ?. FEBS Lett 285:230–236
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-144-7-1747
Loading
/content/journal/micro/10.1099/00221287-144-7-1747
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