Home LiteratureArticle Details
PMID: 14563870 Published · ppublish English Comparative Study Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Recognition of DNA by three ferric uptake regulator (Fur) homologs in Bacillus subtilis.

Journal of bacteriology ·Vol. 185 ·No. 21 ·2003-11-00 ·Pages 6348-57

Fuangthong M, Helmann JD

Abstract

Bacillus subtilis contains three Fur homologs: Fur, PerR, and Zur. Despite significant sequence similarities, they respond to different stimuli and regulate different sets of genes. DNA target site comparisons indicate that all three paralogs recognize operators with a core 7-1-7 inverted repeat. The corresponding consensus sequences are identical at five or more of the seven defined positions. Using site-directed mutagenesis, the Per box at the mrgA promoter was altered to mimic the core 7-1-7 motif of the Fur and Zur boxes. In vitro, the mrgA promoter containing a Zur box was only recognized by Zur, as demonstrated by DNase I footprinting assays. In contrast, both Fur and PerR bound to the mrgA promoter region containing a consensus Fur box. Expression analysis of these promoters is consistent with the in vitro data demonstrating as few as 1 or 2 base changes per half-site are sufficient to alter regulation. Similarly, the Fur box at the feuA promoter can be converted into a Per or a Zur box by appropriate mutations. While both Fur and PerR could recognize some of the same synthetic operator sequences, no naturally occurring sites are known that are subject to dual regulation. However, the PerR-regulated zosA gene is controlled from a regulatory region that contains both Per and Fur boxes. Although purified Fur protein bound to the candidate Fur boxes, Fur has little effect on zosA expression-possibly due to the location of the Fur boxes relative to the zosA promoter. Together, our results identify two nucleotide positions that are important for the ability of PerR, Fur, and Zur to distinguish among the many closely related operator sites present in the B. subtilis genome.

MeSH Terms
Bacillus subtilis/genetics,metabolism Bacterial Proteins/analysis,genetics,metabolism Binding Sites DNA Footprinting DNA Mutational Analysis DNA, Bacterial/genetics,metabolism DNA-Binding Proteins/analysis,genetics,metabolism Escherichia coli Proteins Promoter Regions, Genetic Repressor Proteins/metabolism Trans-Activators/metabolism Transcription Factors/metabolism
Chemicals
Bacterial Proteins DNA, Bacterial DNA-Binding Proteins Escherichia coli Proteins MrgA protein, Bacillus subtilis Repressor Proteins Trans-Activators Transcription Factors Zur protein, E coli ferric uptake regulating proteins, bacterial peroxide repressor proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Fuangthong Mayuree
Department of Microbiology, Cornell University, Ithaca, New York 14853-8101, USA.
Helmann John D
References (46)
46 references, click to expand
  1. The global transcriptional response of Bacillus subtilis to manganese involves the MntR, Fur, TnrA and sigmaB regulons.
    Mol Microbiol. 2003 Sep;49(6):1477-91 PMID: 12950915
  2. Role of AbrB in Spo0A- and Spo0B-dependent utilization of a sporulation promoter in Bacillus subtilis.
    J Bacteriol. 1987 May;169(5):2223-30 PMID: 2437099
  3. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor.
    J Bacteriol. 1987 Jun;169(6):2624-30 PMID: 3294800
  4. Cloning of binding sequences for the Escherichia coli transcription activators, FNR and CRP: location of bases involved in discrimination between FNR and CRP.
    Nucleic Acids Res. 1989 May 25;17(10):3865-74 PMID: 2543955
  5. Promoter discrimination by the related transcriptional activators MarA and SoxS: differential regulation by differential binding.
    Mol Microbiol. 2000 Feb;35(3):623-34 PMID: 10672184
  6. Fur positive regulation of iron superoxide dismutase in Escherichia coli: functional analysis of the sodB promoter.
    J Bacteriol. 2000 Jul;182(13):3802-8 PMID: 10850997
  7. The -10 region is a key promoter specificity determinant for the Bacillus subtilis extracytoplasmic-function sigma factors sigma(X) and sigma(W).
    J Bacteriol. 2001 Mar;183(6):1921-7 PMID: 11222589
  8. Iron and metal regulation in bacteria.
    Curr Opin Microbiol. 2001 Apr;4(2):172-7 PMID: 11282473
  9. Functional versatility in the CRP-FNR superfamily of transcription factors: FNR and FLP.
    Adv Microb Physiol. 2001;44:1-34 PMID: 11407111
  10. Roles of metal ions and hydrogen peroxide in modulating the interaction of the Bacillus subtilis PerR peroxide regulon repressor with operator DNA.
    Mol Microbiol. 2001 Aug;41(4):849-59 PMID: 11532148
  11. Global transcriptional response of Bacillus subtilis to heat shock.
    J Bacteriol. 2001 Dec;183(24):7318-28 PMID: 11717291
  12. Promoter recognition and discrimination by EsigmaS RNA polymerase.
    Mol Microbiol. 2001 Nov;42(4):939-54 PMID: 11737638
  13. Regulation of the Bacillus subtilis fur and perR genes by PerR: not all members of the PerR regulon are peroxide inducible.
    J Bacteriol. 2002 Jun;184(12):3276-86 PMID: 12029044
  14. A peroxide-induced zinc uptake system plays an important role in protection against oxidative stress in Bacillus subtilis.
    Mol Microbiol. 2002 Aug;45(4):997-1005 PMID: 12180919
  15. The bacterial regulatory protein H-NS--a versatile modulator of nucleic acid structures.
    Biol Chem. 2002 Jun;383(6):945-60 PMID: 12222684
  16. Global analysis of the Bacillus subtilis Fur regulon and the iron starvation stimulon.
    Mol Microbiol. 2002 Sep;45(6):1613-29 PMID: 12354229
  17. Fur-DNA interactions at the bidirectional fepDGC-entS promoter region in Escherichia coli.
    J Mol Biol. 2002 Oct 4;322(5):983-95 PMID: 12367523
  18. HU: promoting or counteracting DNA compaction?
    FEBS Lett. 2002 Oct 9;529(2-3):151-6 PMID: 12372591
  19. Iron and oxidative stress in bacteria.
    Arch Biochem Biophys. 2000 Jan 1;373(1):1-6 PMID: 10620317
  20. Recognition of DNA by Fur: a reinterpretation of the Fur box consensus sequence.
    J Bacteriol. 2002 Nov;184(21):5826-32 PMID: 12374814
  21. Regulation of the Bacillus subtilis bcrC bacitracin resistance gene by two extracytoplasmic function sigma factors.
    J Bacteriol. 2002 Nov;184(22):6123-9 PMID: 12399481
  22. Functional analysis of the Bacillus subtilis Zur regulon.
    J Bacteriol. 2002 Dec;184(23):6508-14 PMID: 12426338
  23. The global transcriptional response of Bacillus subtilis to peroxide stress is coordinated by three transcription factors.
    J Bacteriol. 2003 Jan;185(1):243-53 PMID: 12486061
  24. Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator.
    Mol Microbiol. 2003 Feb;47(4):903-15 PMID: 12581348
  25. Global characterization of disulfide stress in Bacillus subtilis.
    J Bacteriol. 2003 Mar;185(6):1967-75 PMID: 12618461
  26. Architecture of a fur binding site: a comparative analysis.
    J Bacteriol. 2003 Apr;185(7):2194-202 PMID: 12644489
  27. Origins of metal ion selectivity in the DtxR/MntR family of metalloregulators.
    Mol Microbiol. 2003 Apr;48(2):495-506 PMID: 12675807
  28. Sequence logos: a new way to display consensus sequences.
    Nucleic Acids Res. 1990 Oct 25;18(20):6097-100 PMID: 2172928
  29. Mutations that relieve nutritional repression of the Bacillus subtilis dipeptide permease operon.
    J Bacteriol. 1993 Aug;175(15):4605-14 PMID: 8335620
  30. Metalloregulation in Bacillus subtilis: isolation and characterization of two genes differentially repressed by metal ions.
    J Bacteriol. 1993 Sep;175(17):5428-37 PMID: 8396117
  31. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  32. The oxidative stress response in Bacillus subtilis.
    FEMS Microbiol Lett. 1994 Dec 15;124(3):255-63 PMID: 7851732
  33. Coordinate regulation of Bacillus subtilis peroxide stress genes by hydrogen peroxide and metal ions.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8190-4 PMID: 7667267
  34. Mutation of the Bacillus subtilis alkyl hydroperoxide reductase (ahpCF) operon reveals compensatory interactions among hydrogen peroxide stress genes.
    J Bacteriol. 1996 Nov;178(22):6579-86 PMID: 8932315
  35. Transcriptional activation by FNR and CRP: reciprocity of binding-site recognition.
    Mol Microbiol. 1997 Feb;23(4):835-45 PMID: 9157253
  36. Regulation of the Salmonella typhimurium pepT gene by cyclic AMP receptor protein (CRP) and FNR acting at a hybrid CRP-FNR site.
    J Bacteriol. 1997 Mar;179(6):1909-17 PMID: 9068635
  37. H-NS: a modulator of environmentally regulated gene expression.
    Mol Microbiol. 1997 Apr;24(1):7-17 PMID: 9140961
  38. Sequence and analysis of a 31 kb segment of the Bacillus subtilis chromosome in the area of the rrnH and rrnG operons.
    Microbiology. 1997 Aug;143 ( Pt 8):2763-7 PMID: 9274029
  39. Three-minute G + A specific reaction for DNA sequencing.
    Anal Biochem. 1998 Jan 1;255(1):158-9 PMID: 9448856
  40. Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors.
    Mol Microbiol. 1998 Jul;29(1):189-98 PMID: 9701813
  41. Identification of an UP element consensus sequence for bacterial promoters.
    Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):9761-6 PMID: 9707549
  42. Binding of the fur (ferric uptake regulator) repressor of Escherichia coli to arrays of the GATAAT sequence.
    J Mol Biol. 1998 Oct 30;283(3):537-47 PMID: 9784364
  43. Identification of a zinc-specific metalloregulatory protein, Zur, controlling zinc transport operons in Bacillus subtilis.
    J Bacteriol. 1998 Nov;180(22):5815-21 PMID: 9811636
  44. Interaction of Bacillus subtilis Fur (ferric uptake repressor) with the dhb operator in vitro and in vivo.
    J Bacteriol. 1999 Jul;181(14):4299-307 PMID: 10400588
  45. Bacillus subtilis MrgA is a Dps(PexB) homologue: evidence for metalloregulation of an oxidative-stress gene.
    Mol Microbiol. 1995 Oct;18(2):295-300 PMID: 8709848
  46. FNR-DNA interactions at natural and semi-synthetic promoters.
    Mol Microbiol. 1996 Jan;19(1):125-37 PMID: 8821942
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2003-11-00
Pages
6348-57
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC219410
Subset
IM
Grants
NIGMS NIH HHS · R01 GM059323 · United States
NIGMS NIH HHS · GM59323 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com