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Volume 151, Issue 12

The manganese-responsive repressor Mur of is a member of the Fur-superfamily that recognizes an unusual operator sequence Free

Abstract

The anganese ptake egulator Mur of is a close homologue of the global iron regulatory protein Fur. Mur represses the operon, which encodes a Mn transport system, specifically in response to Mn but not Fe. In previous work the authors mapped the 5′ ends of two operon transcripts, termed TS1 and TS2, which were co-ordinately regulated by Mn-Mur, but this paper now shows that only TS1 is a primary transcript. DNase I protection analyses showed that purified Mur bound, with similar affinity, to two sites in the regulatory region of , but only when Mn was present in the reaction buffer. These Mn-Mur-binding sites, termed MRS1 and MRS2 (ur-esponsive equence), were closely related in sequence to each other and were separated by 16 bp, spanning the transcription initiation site TS1. The extent of the protected DNA was 34 and 31 bp for MRS1 and MRS2, respectively, which is in accord with other members of the Fur family. The DNA sequences recognized by Mn-Mur are wholly different from conventional Fur boxes, but some similarities to a recognition sequence for the Fur regulator from were noted. Transcription analysis of the gene showed its expression to be independent of Mn-Mur. Thus, Mur is a sequence-specific DNA-binding protein that responds to manganese, and thus can occlude RNA polymerase access to the promoter. Moreover, Mur recognizes a DNA sequence atypical for the Fur superfamily and, like Fur from , defines a new subclass of Fur-like transcriptional regulators.

  • Received:
  • Accepted:
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  • Published Online:
Keyword(s): DP, 2,2′-dipyridyl , Fur, ferric uptake regulator , MRS, Mur-responsive sequence and Mur, manganese uptake regulator
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2005-12-01
2024-04-25
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References

  1. Andrews S. C., Robinson A. K., Rodríguez-Quiñones F. 2003; Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237 [CrossRef]
     [Google Scholar]
  2. Baichoo N., Helmann J. D. 2002; Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence. J Bacteriol 184:5826–5832 [CrossRef]
     [Google Scholar]
  3. Beringer J. E. 1974; R factor transfer in Rhizobium leguminosarum . J Gen Microbiol 84:188–198 [CrossRef]
     [Google Scholar]
  4. Chao T.-C., Becker A., Buhrmester J., Pühler A., Weidner S. 2004; The Sinorhizobium meliloti fur gene regulates in dependence of Mn(II) the transcription of the sitABCD operon encoding a metal type transporter. J Bacteriol 186:3609–3620 [CrossRef]
     [Google Scholar]
  5. de Luca N. G., Wexler M., Pereira M. J., Yeoman K. H., Johnston A. W. B. 1998; Is the fur gene of Rhizobium leguminosarum essential?. FEMS Microbiol Lett 168:289–295 [CrossRef]
     [Google Scholar]
  6. Díaz-Mireles E., Wexler M., Sawers G., Bellini D., Todd J. D., Johnston A. W. B. 2004; The Fur-like protein Mur of Rhizobium leguminosarum is a Mn2+-responsive transcriptional regulator. Microbiology 150:1447–1456 [CrossRef]
     [Google Scholar]
  7. Escolar L., Pérez-Martín J., de Lorenzo V. 1999; Opening the iron box: transcriptional metalloregulation by the Fur protein. J Bacteriol 181:6223–6229
     [Google Scholar]
  8. Friedman Y. E., O'Brian M. R. 2003; A novel DNA-binding site for the ferric uptake regulator (Fur) protein from Bradyrhizobium japonicum . J Biol Chem 278:38395–38401 [CrossRef]
     [Google Scholar]
  9. Friedman Y. E., O'Brian M. R. 2004; The ferric uptake regulator (Fur) protein from Bradyrhizobium japonicum is an iron-responsive transcriptional repressor in vitro . J Biol Chem 279:32100–32105 [CrossRef]
     [Google Scholar]
  10. Fuangthong M., Helmann J. D. 2003; Recognition of DNA by three ferric uptake regulator (Fur) homologs in Bacillus subtilis . J Bacteriol 185:6348–6357 [CrossRef]
     [Google Scholar]
  11. Hamza I., Qi Z., King N. D., O'Brian M. R. 2000; Fur-independent regulation of iron metabolism by Irr in Bradyrhizobium japonicum . Microbiology 146:669–676
     [Google Scholar]
  12. Hantke K. 2001; Iron and metal regulation in bacteria. Curr Opin Microbiol 4:172–177 [CrossRef]
     [Google Scholar]
  13. Johnston A. W. B. 2004; Mechanisms and regulation of iron uptake in the rhizobia. In Iron Transport in Bacteria pp 469–488 Edited by Crosa J. H., Mey A. R., Payne S. M. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  14. 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 A 99:4520–4625 [CrossRef]
     [Google Scholar]
  15. Park S. Y., Kelminson K. L., Lee A. K., Zhang P., Warner R. E., Rehkopf D. H., Calderwood S. B., Koehler J. E. 2001; Identification, characterization, and functional analysis of a gene encoding the ferric uptake regulation protein in Bartonella species. J Bacteriol 183:5751–5755 [CrossRef]
     [Google Scholar]
  16. Platero R., Peixoto L., O'Brian M. R., Fabiano E. 2004; Fur is involved in manganese-dependent regulation of mntA ( sitA ) expression in Sinorhizobium meliloti . Appl Environ Microbiol 70:4349–4355 [CrossRef]
     [Google Scholar]
  17. 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 Microbiol 47:903–915 [CrossRef]
     [Google Scholar]
  18. Rossen L., Shearman C. A., Johnston A. W. B., Downie J. A. 1985; The nodD gene of Rhizobium leguminosarum is autoregulatory and in the presence of plant root exudate induces the nodABC genes. EMBO J 4:3369–3374
     [Google Scholar]
  19. Sawers G., Böck A. 1989; Novel transcriptional control of the pyruvate formate-lyase gene: upstream regulatory sequences and multiple promoters regulate anaerobic expression. J Bacteriol 171:2485–2498
     [Google Scholar]
  20. Spaink H. P., Okker R. J. H., Wijffelman C. A., Pees E., Lugtenberg B. J. J. 1987; Promoters in the nodulation region of the Rhizobium leguminosarum symbiotic plasmid pRL1JI. Plant Mol Biol 9:27–39 [CrossRef]
     [Google Scholar]
  21. Todd J. D., Wexler M., Sawers G., Yeoman K. H., Poole P. S., Johnston A. W. B. 2002; RirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarum . Microbiology 148:4059–4071
     [Google Scholar]
  22. Todd J. D., Sawers G., Johnston A. W. 2005; Proteomic analysis reveals the wide-ranging effects of the novel, iron-responsive regulator RirA in Rhizobium leguminosarum bv. viciae . Mol Genet Genomics 273:197–206 [CrossRef]
     [Google Scholar]
  23. Tucker N. P., D'Autreaux B., Studholme D. J., Spiro S., Dixon R. 2004; DNA binding activity of the Escherichia coli nitric oxide sensor NorR suggests a conserved target sequence in diverse proteobacteria. J Bacteriol 186:6656–6660 [CrossRef]
     [Google Scholar]
  24. Viguier C. O., Cuiv P., Clarke P., O'Connell M. 2005; RirA is the iron response regulator of the rhizobactin 1021 biosynthesis and transport genes in Sinorhizobium meliloti 2011. FEMS Microbiol Lett 246:235–242 [CrossRef]
     [Google Scholar]
  25. Wexler M., Yeoman K. H., Stevens J. B., de Luca N. G., Sawers G., Johnston A. W. B. 2001; The Rhizobium leguminosarum tonB gene is required for the uptake of siderophore and haem as sources of iron. Mol Microbiol 41:801–816
     [Google Scholar]
  26. Wexler M., Todd J. D., Kolade O., Bellini D., Hemmings A. M., Sawers G., Johnston A. W. B. 2003; Fur is not the global regulator of iron uptake genes in Rhizobium leguminosarum . Microbiology 149:1357–1365 [CrossRef]
     [Google Scholar]
  27. Wood W. B. 1966; Host specificity of DNA produced by Escherichia coli ; bacterial mutations affecting the restriction and modification of DNA. Mol Biol 16:118–133 [CrossRef]
     [Google Scholar]
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The manganese-responsive repressor Mur of Rhizobium leguminosarum is a member of the Fur-superfamily that recognizes an unusual operator sequence
Microbiology 151, 4071 (2005); https://doi.org/10.1099/mic.0.28342-0
/content/journal/micro/10.1099/mic.0.28342-0
/content/journal/micro/10.1099/mic.0.28342-0
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