1887

Abstract

is a Gram-negative bacterium that lives at pH 2 in high concentrations of soluble ferrous and ferric iron, making it an interesting model for understanding the biological mechanisms of bacterial iron uptake and homeostasis in extremely acid conditions. A candidate (erric ptake egulator) gene was identified in the ATCC 23270 genome. Fur has significant sequence similarity, including conservation of functional motifs, to known Fur orthologues and exhibits cross-reactivity to Fur antiserum. The gene is able to complement deficiency in in an iron-responsive manner. Fur is also able to bind specifically to Fur regulatory regions (Fur boxes) and to a candidate Fur box from , as judged by electrophoretic mobility shift assays. Fur represses gene expression from Fur-responsive promoters and when expressed at high protein levels. However, it increases gene expression from these promoters at low concentrations and possibly from other Fur-regulated promoters involved in iron-responsive oxidative stress responses.

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2005-06-01
2020-08-15
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References

  1. Adrait A., Jacquamet L., Le Pape L., Gonzalez de Peredo A., Aberdam D., Hazemann J. L., Latour J. M., Michaud-Soret I. 1999; Spectroscopic and saturation magnetization properties of the manganese- and cobalt-substituted Fur (ferric uptake regulation) protein from Escherichia coli. Biochemistry38:6248–6260[CrossRef]
    [Google Scholar]
  2. Aiba H., Adhya S., de Crombrugghe B. 1981; Evidence for two functional gal promoters in intact Escherichia coli cells. J Biol Chem256:11905–11910
    [Google Scholar]
  3. Andrews S. C., Robinson A. K., Rodriguez-Quinones F. 2003; Bacterial iron homeostasis. FEMS Microbiol Rev27:215–237[CrossRef]
    [Google Scholar]
  4. Baichoo N., Wang T., Ye R., Helmann J. D. 2002; Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon. Mol Microbiol45:1613–1629[CrossRef]
    [Google Scholar]
  5. Barton H. A., Johnson Z., Cox C. D., Vasil A. I., Vasil M. L. 1996; Ferric uptake regulator mutants of Pseudomonas aeruginosa with distinct alterations in the iron-dependent repression of exotoxin A and siderophores in aerobic and microaerobic environments. Mol Microbiol21:1001–1017[CrossRef]
    [Google Scholar]
  6. Brasseur G., Levican G., Bonnefoy V., Holmes D., Jedlicki E., Lemesle-Meunier D. 2004; Apparent redundancy of electron transfer pathways via bc(1) complexes and terminal oxidases in the extremophilic chemolithoautotrophic Acidithiobacillus ferrooxidans. Biochim Biophys Acta 1656;114–126[CrossRef]
    [Google Scholar]
  7. Braun V., Killmann H. 1999; Bacterial solutions to the iron-supply problem. Trends Biochem Sci24:104–109[CrossRef]
    [Google Scholar]
  8. Bsat N., Helmann J. D. 1999; Interaction of Bacillus subtilis Fur (ferric uptake repressor) with the dhb operator in vitro and in vivo. J Bacteriol181:4299–4307
    [Google Scholar]
  9. Coy M., Doyle C., Besser J., Neilands J. B. 1994; Site-directed mutagenesis of the ferric uptake regulation gene of Escherichia coli. Biometals7:292–298
    [Google Scholar]
  10. de Lorenzo V., Giovannini F., Herrero M., Neilands J. B. 1988; Metal ion regulation of gene expression. Fur repressor-operator interaction at the promoter region of the aerobactin system of pColV-K30. J Mol Biol203:875–884[CrossRef]
    [Google Scholar]
  11. Delany I., Spohn G., Rappuoli R., Scarlato V. 2001; The Fur repressor controls transcription of iron-activated and -repressed genes in Helicobacter pylori. Mol Microbiol42:1297–1309
    [Google Scholar]
  12. Delany I., Spohn G., Pacheco A. B., Ieva R., Alaimo C., Rappuoli R., Scarlato V. 2002; Autoregulation of Helicobacter pylori Fur revealed by functional analysis of the iron-binding site. Mol Microbiol46:1107–1122[CrossRef]
    [Google Scholar]
  13. Delany I., Spohn G., Rappuoli R., Scarlato V. 2003; An anti-repression Fur operator upstream of the promoter is required for iron-mediated transcriptional autoregulation in Helicobacter pylori. Mol Microbiol50:1329–1338[CrossRef]
    [Google Scholar]
  14. Delany I., Rappuoli R., Scarlato V. 2004; Fur functions as an activator and as a repressor of putative virulence genes in Neisseria meningitidis. Mol Microbiol52:1081–1090[CrossRef]
    [Google Scholar]
  15. de Smith M. H., van Duin J. 1990; Secondary structure of the ribosome binding site determines translational efficiency: a quantitative analysis. Proc Natl Acad Sci U S A87:7668–7672[CrossRef]
    [Google Scholar]
  16. Escolar L., de Lorenzo V, Pérez-Martín J.. 1998; Coordinated repression in vitro of the divergent fepAfes promoters of Escherichia coli by the iron uptake regulation (Fur) protein. J Bacteriol180:2579–2582
    [Google Scholar]
  17. Escolar L., de Lorenzo V, Peréz-Martín J.. 1999; Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol181:6223–6229
    [Google Scholar]
  18. Escolar L., de Lorenzo V, Peréz-Martín J.. 2000; Evidence of an unusually long operator for the Fur repressor in the aerobactin promoter of Escherichia coli. J Biol Chem275:24709–24714[CrossRef]
    [Google Scholar]
  19. Gonzalez de Perédo A., Saint-Pierre C., Latour J. M., Michaud-Soret I., Forest E. 2001; Conformational changes of the ferric uptake regulation protein upon metal activation and DNA binding; first evidence of structural homologies with the diphtheria toxin repressor. J Mol Biol310:83–91[CrossRef]
    [Google Scholar]
  20. Gross G., Mielke C., Hollatz I., Blocker H., Frank R. 1990; RNA primary sequence or secondary structure in the translational initiation region controls expression of two variant interferon-beta genes in Escherichia coli. J Biol Chem265:17627–17636
    [Google Scholar]
  21. Guacucano M., Levican G., Holmes D. S., Jedlicki E. 2000; An RT-PCR artifact in the characterization of bacterial operons. EJB Electronic Journal of Biotechnology3:http://www.ejbiotechnology.info/content/vol3/issue3/full/5/
    [Google Scholar]
  22. Hall H. K., Foster J. W. 1996; The role of Fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J Bacteriol178:5683–5691
    [Google Scholar]
  23. Hantke K. 1987; Selection procedure for deregulated iron transport mutants (fur) in Escherichia coli K 12: Fur not only affects iron metabolism. Mol Gen Genet210:135–139[CrossRef]
    [Google Scholar]
  24. Hantke K. 2001; Iron and metal regulation in bacteria. Curr Opin Microbiol4:172–177[CrossRef]
    [Google Scholar]
  25. Hantke K., Braun V. 2000; The art of keeping low and high iron concentrations in balance. In Bacterial Stress Responses pp275–288 Edited by Storz G., Hengge-Aronis R.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  26. Hartz D., McPheeters D. S., Gold L. 1991; Influence of mRNA determinants on translation initiation in Escherichia coli. J Mol Biol218:83–97[CrossRef]
    [Google Scholar]
  27. Hernández J. A., Bes M. T., Fillat M. F., Neira J. L., Peleato M. L. 2002; Biochemical analysis of the recombinant Fur (ferric uptake regulator) protein from Anabaena PCC 7119: factors affecting its oligomerization state. Biochem J366:315–322
    [Google Scholar]
  28. Holm L., Sander C., Ruterjans H., Schnarr M., Fogh R., Boelens R., Kaptein R. 1994; LexA repressor and iron uptake regulator from Escherichia coli: new members of the CAP-like DNA binding domain superfamily. Protein Eng7:1449–1453[CrossRef]
    [Google Scholar]
  29. Jacquamet L., Aberdam D., Adrait A., Hazemann J. L., Latour J. M., Michaud-Soret I. 1998; X-ray absorption spectroscopy of a new zinc site in the Fur protein from Escherichia coli. Biochemistry37:2564–2571[CrossRef]
    [Google Scholar]
  30. Kehres D. G., Zaharik M. L., Finlay B. B., Maguire M. E. 2000; The NRAMP proteins of Salmonella typhimurium and Escherichia coli are selective manganese transporters involved in the response to reactive oxygen. Mol Microbiol36:1085–1100[CrossRef]
    [Google Scholar]
  31. Kehres D. G., Janakiraman A., Slauch J. M., Maguire M. E. 2002; Regulation of Salmonella entericaserovar Typhimurium mntH transcription by H2O2 Fe2+, and Mn2+. J Bacteriol184:3151–3158[CrossRef]
    [Google Scholar]
  32. Liu Z., Guiliani N., Appia-Ayme C., Borne F., Ratouchniak J., Bonnefoy V. 2000; Construction and characterization of a recA mutant of Thiobacillus ferrooxidans by marker exchange mutagenesis. J Bacteriol182:2269–2276[CrossRef]
    [Google Scholar]
  33. Loprasert S., Sallabhan R., Atichartpongkul S., Mongkolsuk S. 1999; Characterization of a ferric uptake regulator (fur) gene from Xanthomonas campestris pv.phaseoli with unusual primary structure, genome organization, and expression patterns. Gene239:251–258[CrossRef]
    [Google Scholar]
  34. Lowe C. A., Asghar A. H., Shalom G., Shaw J. G., Thomas M. S. 2001; The Burkholderia cepacia fur gene: co-localization with omlA and absence of regulation by iron. Microbiology147:1303–1314
    [Google Scholar]
  35. Makui H., Roig E., Cole S. T., Helmann J. D., Gros P., Cellier M. F. 2000; Identification of the Escherichia coli K-12 Nramp orthologue (MntH) as a selective divalent metal ion transporter. Mol Microbiol35:1065–1078[CrossRef]
    [Google Scholar]
  36. Massé E., Gottesman S. 2002; A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A99:4620–4625[CrossRef]
    [Google Scholar]
  37. McHugh J. P., Rodriguez-Quinones F., Abdul-Tehrani H., Svistunenko D. A., Poole R. K., Cooper C. E., Andrews S. C. 2003; Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem278:29478–29486[CrossRef]
    [Google Scholar]
  38. Miller J. H. 1972; Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  39. Ochsner U. A., Vasil A. I., Johnson Z., Vasil M. L. 1999; Pseudomonas aeruginosa fur overlaps with a gene encoding a novel outer membrane lipoprotein. OmlA. J Bacteriol181:1099–1109
    [Google Scholar]
  40. Ochsner U. A., Wilderman P. J., Vasil A. I., Vasil M. L. 2002; GeneChip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol45:1277–1287[CrossRef]
    [Google Scholar]
  41. Pohl E., Haller J. C., Mijovilovich A., Meyer-Klaucke W., Garman E., Vasil M. L. 2003; Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator. Mol Microbiol47:903–915[CrossRef]
    [Google Scholar]
  42. Qi Z., Hamza I., O'Brian M. 1999; Heme is an effector molecule for iron-dependent degradation of the bacterial iron response regulator (Irr) protein. Proc Natl Acad Sci U S A96:13056–13061[CrossRef]
    [Google Scholar]
  43. Rawlings D. E. 2002; Heavy metal mining using microbes. Annu Rev Microbiol56:65–91[CrossRef]
    [Google Scholar]
  44. Sambrook J., Fritsch E. F., Maniatis T. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  45. Stojiljkovic I., Baumler A. J., Hantke K. 1994; Fur regulon in gram-negative bacteria. Identification and characterization of new iron-regulated Escherichia coli genes by a fur titration assay. J Mol Biol236:531–545[CrossRef]
    [Google Scholar]
  46. Thomas C. E., Sparling P. F. 1994; Identification and cloning of a Fur homologue from Neisseria meningitidis. Mol Microbiol11:725–737[CrossRef]
    [Google Scholar]
  47. Thompson D. K., Beliaev A. S., Giometti C. S.. 9 other authors 2002; Transcriptional and proteomic analysis of a ferric uptake regulator (fur) mutant of Shewanella oneidensis: possible involvement of Fur in energy metabolism, transcriptional regulation, and oxidative stress. Appl Environ Microbiol68:881–892[CrossRef]
    [Google Scholar]
  48. Touati D. 2000; Iron and oxidative stress in bacteria. Arch Biochem Biophys373:1–6[CrossRef]
    [Google Scholar]
  49. Touati D., Jacques M., Tardat B., Bouchard L., Despied S. 1995; Lethal oxidative damage and mutagenesis are generated by iron in delta fur mutants of Escherichia coli: protective role of superoxide dismutase. J Bacteriol177:2305–2314
    [Google Scholar]
  50. Vasil M. L., Ochsner U. A. 1999; The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol34:399–413[CrossRef]
    [Google Scholar]
  51. Watnick P. I., Eto T., Takahashi H., Calderwood S. B. 1997; Purification of Vibrio cholerae Fur and estimation of its intracellular abundance by antibody sandwich enzyme-linked immunosorbent assay. J Bacteriol179:243–247
    [Google Scholar]
  52. Yarzábal A., Appia-Ayme C., Ratouchniak J., Bonnefoy V. 2004; Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c, a cytochrome oxidase and rusticyanin. Microbiology150:2113–2123[CrossRef]
    [Google Scholar]
  53. Zheng M., Wang X., Doan B., Lewis K. A., Schneider T. D., Storz G. 2001; Computation-directed identification of OxyR DNA binding sites in Escherichia coli.. J Bacteriol183:4571–4579[CrossRef]
    [Google Scholar]
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