Home LiteratureArticle Details
PMID: 10692351 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Functional analysis of PvdS, an iron starvation sigma factor of Pseudomonas aeruginosa.

Journal of bacteriology ·Vol. 182 ·No. 6 ·2000-03-00 ·Pages 1481-91

Leoni L, Orsi N, de Lorenzo V, Visca P

Abstract

In Pseudomonas aeruginosa, iron modulates gene expression through a cascade of negative and positive regulatory proteins. The master regulator Fur is involved in iron-dependent repression of several genes. One of these genes, pvdS, was predicted to encode a putative sigma factor responsible for the transcription of a subset of genes of the Fur regulon. PvdS appears to belong to a structurally and functionally distinct subgroup of the extracytoplasmic function family of alternative sigma factors. Members of this subgroup, also including PbrA from Pseudomonas fluorescens, PfrI and PupI from Pseudomonas putida, and FecI from Escherichia coli, are controlled by the Fur repressor, and they activate transcription of genes for the biosynthesis or the uptake of siderophores. Evidence is provided that the PvdS protein of P. aeruginosa is endowed with biochemical properties of eubacterial sigma factors, as it spontaneously forms 1:1 complexes with the core fraction of RNA polymerase (RNAP, alpha(2)betabeta' subunits), thereby promoting in vitro binding of the PvdS-RNAP holoenzyme to the promoter region of the pvdA gene. These functional features of PvdS are consistent with the presence of structural domains predicted to be involved in core RNAP binding, promoter recognition, and open complex formation. The activity of pyoverdin biosynthetic (pvd) promoters was significantly lower in E. coli overexpressing the multicopy pvdS gene than in wild-type P. aeruginosa PAO1 carrying the single gene copy, and pvd::lacZ transcriptional fusions were silent in both pfrI (the pvdS homologue) and pfrA (a positive regulator of pseudobactin biosynthetic genes) mutants of P. putida WCS358, while they are expressed at PAO1 levels in wild-type WCS358. Moreover, the PvdS-RNAP holoenzyme purified from E. coli lacked the ability to generate in vitro transcripts from the pvdA promoter. These observations suggest that at least one additional positive regulator could be required for full activity of the PvdS-dependent transcription complex both in vivo and in vitro. This is consistent with the presence of a putative activator binding site (the iron starvation box) at variable distance from the transcription initiation sites of promoters controlled by the iron starvation sigma factors PvdS, PfrI, and PbrA of fluorescent pseudomonads.

MeSH Terms
Amino Acid Sequence Bacterial Proteins/classification,genetics,metabolism DNA, Bacterial/analysis DNA-Directed RNA Polymerases/metabolism Gene Expression Regulation, Bacterial Iron/metabolism Molecular Sequence Data Oligopeptides Phylogeny Pigments, Biological/genetics,metabolism Promoter Regions, Genetic Pseudomonas aeruginosa/genetics,growth & development,metabolism Repressor Proteins/genetics,metabolism Sequence Analysis, DNA Sequence Homology, Amino Acid Sigma Factor/classification,genetics,metabolism
Chemicals
Bacterial Proteins DNA, Bacterial Oligopeptides Pigments, Biological PvdS protein, Pseudomonas aeruginosa Repressor Proteins Sigma Factor ferric uptake regulating proteins, bacterial pyoverdin Iron DNA-Directed RNA Polymerases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Leoni L
"Istituto Pasteur - Fondazione Cenci Bolognetti" - Istituto di Microbiologia, Università di Roma "La Sapienza", 00100 Rome, Italy.
Orsi N
de Lorenzo V
Visca P
References (48)
48 references, click to expand
  1. Nucleotide sequence of pvdD, a pyoverdine biosynthetic gene from Pseudomonas aeruginosa: PvdD has similarity to peptide synthetases.
    J Bacteriol. 1995 Jan;177(1):252-8 PMID: 7798141
  2. Identification of a DNA sequence motif required for expression of iron-regulated genes in pseudomonads.
    Mol Gen Genet. 1995 Feb 20;246(4):519-28 PMID: 7891666
  3. The rpoE gene encoding the sigma E (sigma 24) heat shock sigma factor of Escherichia coli.
    EMBO J. 1995 Mar 1;14(5):1043-55 PMID: 7889935
  4. Regulation of citrate-dependent iron transport of Escherichia coli: fecR is required for transcription activation by FecI.
    Mol Microbiol. 1995 Jan;15(1):119-32 PMID: 7752886
  5. Promoter recognition by Bacillus subtilis sigmaW: autoregulation and partial overlap with the sigmaX regulon.
    J Bacteriol. 1998 Aug;180(15):3765-70 PMID: 9683469
  6. Subregions of a conserved part of the HIV gp41 transmembrane protein are differentially recognized by antibodies of infected individuals.
    EMBO J. 1986 Nov;5(11):3051-6 PMID: 3491755
  7. The extracytoplasmic function sigma factors: role and regulation.
    Mol Microbiol. 1998 Jun;28(6):1059-66 PMID: 9680198
  8. Functional equivalence of Escherichia coli sigma E and Pseudomonas aeruginosa AlgU: E. coli rpoE restores mucoidy and reduces sensitivity to reactive oxygen intermediates in algU mutants of P. aeruginosa.
    J Bacteriol. 1995 Jun;177(11):3259-68 PMID: 7768826
  9. Iron-regulated transcription of the pvdA gene in Pseudomonas aeruginosa: effect of Fur and PvdS on promoter activity.
    J Bacteriol. 1996 Apr;178(8):2299-313 PMID: 8636031
  10. Characterisation of the pvdE gene which is required for pyoverdine synthesis in Pseudomonas aeruginosa.
    Gene. 1996 Oct 17;176(1-2):55-9 PMID: 8918232
  11. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli.
    J Mol Biol. 1980 Apr;138(2):179-207 PMID: 6997493
  12. Energy metabolism and alginate biosynthesis in Pseudomonas aeruginosa: role of the tricarboxylic acid cycle.
    J Bacteriol. 1994 Oct;176(19):6023-9 PMID: 7928963
  13. SigX of Bacillus subtilis replaces the ECF sigma factor fecI of Escherichia coli and is inhibited by RsiX.
    Mol Gen Genet. 1997 Oct;256(4):416-25 PMID: 9393439
  14. Metalloregulation in vitro of the aerobactin promoter of Escherichia coli by the Fur (ferric uptake regulation) protein.
    Mol Microbiol. 1997 Nov;26(4):799-808 PMID: 9427409
  15. Iron-responsive gene expression in Pseudomonas fluorescens M114: cloning and characterization of a transcription-activating factor, PbrA.
    Mol Microbiol. 1995 Jan;15(2):297-306 PMID: 7746151
  16. Signal transduction and transcriptional and posttranscriptional control of iron-regulated genes in bacteria.
    Microbiol Mol Biol Rev. 1997 Sep;61(3):319-36 PMID: 9293185
  17. Cloning and characterization of pvdS, a gene required for pyoverdine synthesis in Pseudomonas aeruginosa: PvdS is probably an alternative sigma factor.
    J Bacteriol. 1995 May;177(10):2744-50 PMID: 7751284
  18. RNA polymerases from Pseudomonas aeruginosa and Pseudomonas syringae respond to Escherichia coli activator proteins.
    J Bacteriol. 1991 Jan;173(1):394-7 PMID: 1898924
  19. Gene regulation of siderophore-mediated iron acquisition in Pseudomonas: not only the Fur repressor.
    Mol Microbiol. 1995 Aug;17(4):603-10 PMID: 8801415
  20. Positive control of transcription initiation in bacteria.
    Annu Rev Genet. 1984;18:173-206 PMID: 6084980
  21. Initiation of transcription at the bacterial glnAp2 promoter by purified E. coli components is facilitated by enhancers.
    Cell. 1987 Sep 25;50(7):1039-46 PMID: 3304660
  22. Nucleotide sequence of a regulatory region controlling alginate synthesis in Pseudomonas aeruginosa: characterization of the algR2 gene.
    Gene. 1989 Dec 7;84(1):31-8 PMID: 2514124
  23. The sigma 70 family: sequence conservation and evolutionary relationships.
    J Bacteriol. 1992 Jun;174(12):3843-9 PMID: 1597408
  24. Escherichia-Pseudomonas shuttle vectors derived from pUC18/19.
    Gene. 1991 Jan 2;97(1):109-21 PMID: 1899844
  25. The fur-regulated gene encoding the alternative sigma factor PvdS is required for iron-dependent expression of the LysR-type regulator ptxR in Pseudomonas aeruginosa.
    J Bacteriol. 1998 Dec;180(24):6784-8 PMID: 9852033
  26. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI.
    Plant Mol Biol. 1987 Jan;9(1):27-39 PMID: 24276795
  27. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli.
    EMBO J. 1995 Mar 1;14(5):1032-42 PMID: 7889934
  28. Characterization of Pseudomonas aeruginosa mutants that are deficient in exotoxin A synthesis and are altered in expression of regA, a positive regulator of exotoxin A.
    Infect Immun. 1994 Mar;62(3):897-903 PMID: 8112861
  29. Biochemical characterization and posttranslational modification of AlgU, a regulator of stress response in Pseudomonas aeruginosa.
    Biochem Biophys Res Commun. 1995 Nov 22;216(3):874-80 PMID: 7488207
  30. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia.
    Microbiol Rev. 1996 Sep;60(3):539-74 PMID: 8840786
  31. A mycobacterial extracytoplasmic function sigma factor involved in survival following stress.
    J Bacteriol. 1997 May;179(9):2922-9 PMID: 9139909
  32. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans.
    Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648-52 PMID: 377280
  33. Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope.
    EMBO J. 1994 Jun 15;13(12):2805-13 PMID: 8026465
  34. Role of iron in regulation of virulence genes.
    Clin Microbiol Rev. 1993 Apr;6(2):137-49 PMID: 8472246
  35. Iron regulation of siderophore biosynthesis and transport in Pseudomonas putida WCS358: involvement of a transcriptional activator and of the Fur protein.
    Mol Microbiol. 1995 Mar;15(6):1081-93 PMID: 7623664
  36. Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: cycle selection of iron-regulated genes.
    Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):4409-14 PMID: 8633080
  37. Iron-regulated salicylate synthesis by Pseudomonas spp.
    J Gen Microbiol. 1993 Sep;139(9):1995-2001 PMID: 7504066
  38. Transcriptional regulation of ferric citrate transport in Escherichia coli K-12. Fecl belongs to a new subfamily of sigma 70-type factors that respond to extracytoplasmic stimuli.
    Mol Microbiol. 1995 Oct;18(1):163-74 PMID: 8596456
  39. Crystal structure of a sigma 70 subunit fragment from E. coli RNA polymerase.
    Cell. 1996 Oct 4;87(1):127-36 PMID: 8858155
  40. A positive regulatory gene, pvdS, for expression of pyoverdin biosynthetic genes in Pseudomonas aeruginosa PAO.
    Mol Gen Genet. 1995 Jul 22;248(1):17-24 PMID: 7651323
  41. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  42. Transcriptional regulation of the iron-responsive sigma factor gene pbrA.
    Mol Gen Genet. 1996 Jan 15;250(1):50-8 PMID: 8569687
  43. Cloning of genes controlling alginate biosynthesis from a mucoid cystic fibrosis isolate of Pseudomonas aeruginosa.
    J Bacteriol. 1984 Jul;159(1):9-18 PMID: 6330052
  44. Exotoxin A production in Pseudomonas aeruginosa requires the iron-regulated pvdS gene encoding an alternative sigma factor.
    Mol Microbiol. 1996 Sep;21(5):1019-28 PMID: 8885271
  45. Residues of the Bacillus subtilis phage phi 29 transcriptional activator required both to interact with RNA polymerase and to activate transcription.
    J Mol Biol. 1993 Oct 20;233(4):695-704 PMID: 8411175
  46. Identification and characterization of a siderophore regulatory gene (pfrA) of Pseudomonas putida WCS358: homology to the alginate regulatory gene algQ of Pseudomonas aeruginosa.
    Mol Microbiol. 1993 Oct;10(1):63-73 PMID: 7968519
  47. Regulation of the iron uptake genes in Pseudomonas fluorescens M114 by pseudobactin M114: the pbrA sigma factor gene does not mediate the siderophore regulatory response.
    FEMS Microbiol Lett. 1996 Oct 15;144(1):61-6 PMID: 8870253
  48. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7573-7 PMID: 8052622
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2000-03-00
Pages
1481-91
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC94443
Subset
IM
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