Home LiteratureArticle Details
PMID: 8682773 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Growth phase-dependent transcription of the sigma(54)-dependent Po promoter controlling the Pseudomonas-derived (methyl)phenol dmp operon of pVI150.

Journal of bacteriology ·Vol. 178 ·No. 13 ·1996-07-00 ·Pages 3727-35

Sze CC, Moore T, Shingler V

Abstract

Transcription from Pseudomonas-derived -24, -12 Po promoter of the pVI150-encoded dmp operon is mediated by the sigma 54-dependent DmpR activator in response to the presence of aromatic pathway substrates in the medium. However, global regulatory mechanisms are superimposed on this regulatory system so that the specific response to aromatic effectors is absent in cultures until the stationary phase is reached. Here we genetically dissect the system to show that the growth phase response is faithfully mimicked by a minimal system composed of the dmpR regulatory gene and the Po promoter regulatory region and can be reproduced in heterologous Escherichia coli. Using this system, we show that the growth phase-dependent DmpR-mediated response to aromatic compounds is limited to fast-growing cultures. Thus, during exponential growth of cultures in minimal media containing different carbon sources, the response to aromatics is immediate, while the response is suppressed in cultures grown on rich media until the exponential-to-stationary phase transition. Elements known to be involved in the DmpR-mediated transcription from Po were analyzed for the ability to influence the growth phase response. Most dramatically, overexpression of DmpR was shown to completely abolish the growth phase response, suggesting that a negatively acting factor may mediate this level of regulation. The possible mechanism of action and integration (of the specific regulation of the dmp operon-encoded catabolic enzymes with the physiological status of the bacteria are discussed.

MeSH Terms
Bacterial Proteins/genetics,metabolism Carrier Proteins/metabolism Culture Media/metabolism DNA-Binding Proteins/metabolism DNA-Directed RNA Polymerases/metabolism Escherichia coli/genetics,growth & development Escherichia coli Proteins Gene Expression Regulation, Bacterial Integration Host Factors Operon Phenol Phenols Plasmids Promoter Regions, Genetic Pseudomonas/genetics,growth & development RNA Polymerase Sigma 54 Sigma Factor/metabolism Trans-Activators/genetics Transcription, Genetic
Chemicals
Bacterial Proteins Carrier Proteins Culture Media DNA-Binding Proteins DmpR protein, Pseudomonas Escherichia coli Proteins Integration Host Factors Phenols Sigma Factor Trans-Activators integration host factor, E coli integration host factor, Pseudomonas rpoN protein, E coli Phenol DNA-Directed RNA Polymerases RNA Polymerase Sigma 54
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sze C C
Department of Cell and Molecular Biology, Umeå University, Sweden.
Moore T
Shingler V
References (42)
42 references, click to expand
  1. Direct regulation of the ATPase activity of the transcriptional activator DmpR by aromatic compounds.
    Mol Microbiol. 1995 Aug;17(3):505-13 PMID: 8559069
  2. The regulation of transcription initiation by integration host factor.
    Mol Microbiol. 1995 Apr;16(1):1-7 PMID: 7651128
  3. Involvement of sigma 54 in exponential silencing of the Pseudomonas putida TOL plasmid Pu promoter.
    Mol Microbiol. 1996 Jan;19(1):7-17 PMID: 8821932
  4. Early and late responses of TOL promoters to pathway inducers: identification of postexponential promoters in Pseudomonas putida with lacZ-tet bicistronic reporters.
    J Bacteriol. 1993 Nov;175(21):6902-7 PMID: 8226632
  5. Phospholipid alterations during growth of Escherichia coli.
    J Bacteriol. 1968 Jun;95(6):2054-61 PMID: 4876126
  6. Analysis of gene control signals by DNA fusion and cloning in Escherichia coli.
    J Mol Biol. 1980 Apr;138(2):179-207 PMID: 6997493
  7. Molecular and functional analysis of the TOL plasmid pWWO from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta cleavage pathway.
    Proc Natl Acad Sci U S A. 1981 Dec;78(12):7458-62 PMID: 6950388
  8. Nucleotide sequence and expression of gene nahH of plasmid NAH7 and homology with gene xylE of TOL pWWO.
    Gene. 1987;55(1):19-28 PMID: 3623105
  9. Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli.
    J Bacteriol. 1987 Oct;169(10):4499-506 PMID: 3308843
  10. Isolation of the gene encoding the Hin recombinational enhancer binding protein.
    Proc Natl Acad Sci U S A. 1988 May;85(10):3484-8 PMID: 2835774
  11. Involvement of integration host factor (IHF) in maintenance of plasmid pSC101 in Escherichia coli: characterization of pSC101 mutants that replicate in the absence of IHF.
    J Bacteriol. 1989 Apr;171(4):2056-65 PMID: 2539358
  12. The use of the luxA gene of the bacterial luciferase operon as a reporter gene.
    Mol Gen Genet. 1988 Dec;215(1):1-9 PMID: 3071733
  13. Molecular analysis of a plasmid-encoded phenol hydroxylase from Pseudomonas CF600.
    J Gen Microbiol. 1989 May;135(5):1083-92 PMID: 2559941
  14. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria.
    J Bacteriol. 1990 Nov;172(11):6568-72 PMID: 2172217
  15. Growth phase-regulated expression of bolA and morphology of stationary-phase Escherichia coli cells are controlled by the novel sigma factor sigma S.
    J Bacteriol. 1991 Jul;173(14):4474-81 PMID: 1648559
  16. The phosphorylated form of the enhancer-binding protein NTRC has an ATPase activity that is essential for activation of transcription.
    Cell. 1991 Oct 4;67(1):155-67 PMID: 1833069
  17. Nucleotide sequence and functional analysis of the complete phenol/3,4-dimethylphenol catabolic pathway of Pseudomonas sp. strain CF600.
    J Bacteriol. 1992 Feb;174(3):711-24 PMID: 1732207
  18. Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by katF (AppR)
    J Bacteriol. 1992 Feb;174(3):889-98 PMID: 1310094
  19. The prokaryotic enhancer binding protein NTRC has an ATPase activity which is phosphorylation and DNA dependent.
    EMBO J. 1992 Jun;11(6):2219-28 PMID: 1534752
  20. The Fis protein: it's not just for DNA inversion anymore.
    Mol Microbiol. 1992 Nov;6(22):3257-65 PMID: 1484481
  21. Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes.
    Gene. 1993 Jan 15;123(1):17-24 PMID: 8380783
  22. Cloning and nucleotide sequence of the gene encoding the positive regulator (DmpR) of the phenol catabolic pathway encoded by pVI150 and identification of DmpR as a member of the NtrC family of transcriptional activators.
    J Bacteriol. 1993 Mar;175(6):1596-604 PMID: 8449869
  23. Microbial competition: Escherichia coli mutants that take over stationary phase cultures.
    Science. 1993 Mar 19;259(5102):1757-60 PMID: 7681219
  24. Prokaryotic enhancer-binding proteins reflect eukaryote-like modularity: the puzzle of nitrogen regulatory protein C.
    J Bacteriol. 1993 Jul;175(14):4267-73 PMID: 8331061
  25. The sigma 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains.
    J Bacteriol. 1993 Oct;175(19):6067-74 PMID: 8407777
  26. Sensing of aromatic compounds by the DmpR transcriptional activator of phenol-catabolizing Pseudomonas sp. strain CF600.
    J Bacteriol. 1994 Mar;176(6):1555-60 PMID: 8132448
  27. Carbon source-dependent inhibition of xyl operon expression of the Pseudomonas putida TOL plasmid.
    J Bacteriol. 1994 Mar;176(6):1773-6 PMID: 8132475
  28. Genetic evidence for activation of the positive transcriptional regulator Xy1R, a member of the NtrC family of regulators, by effector binding.
    J Biol Chem. 1994 Mar 18;269(11):8059-62 PMID: 8132529
  29. Inducibility of the TOL catabolic pathway in Pseudomonas putida (pWW0) growing on succinate in continuous culture: evidence of carbon catabolite repression control.
    J Bacteriol. 1994 Apr;176(8):2354-61 PMID: 8157604
  30. Transcriptional induction kinetics from the promoters of the catabolic pathways of TOL plasmid pWW0 of Pseudomonas putida for metabolism of aromatics.
    J Bacteriol. 1994 May;176(9):2517-24 PMID: 8169200
  31. Growth phase variation of integration host factor level in Escherichia coli.
    J Bacteriol. 1994 Jun;176(12):3738-48 PMID: 8206852
  32. Optimization and maintenance of soluble methane monooxygenase activity in Methylosinus trichosporium OB3b.
    Biodegradation. 1994 Mar;5(1):1-11 PMID: 7764924
  33. Cross-regulation by XylR and DmpR activators of Pseudomonas putida suggests that transcriptional control of biodegradative operons evolves independently of catabolic genes.
    J Bacteriol. 1994 Aug;176(16):5052-8 PMID: 8051017
  34. Promoters responsive to DNA bending: a common theme in prokaryotic gene expression.
    Microbiol Rev. 1994 Jun;58(2):268-90 PMID: 8078436
  35. Rhizobium meliloti DctD, a sigma 54-dependent transcriptional activator, may be negatively controlled by a subdomain in the C-terminal end of its two-component receiver module.
    Mol Microbiol. 1994 Jul;13(1):51-66 PMID: 7984094
  36. An aromatic effector specificity mutant of the transcriptional regulator DmpR overcomes the growth constraints of Pseudomonas sp. strain CF600 on para-substituted methylphenols.
    J Bacteriol. 1994 Dec;176(24):7550-7 PMID: 8002579
  37. The role of the sigma factor sigma S (KatF) in bacterial global regulation.
    Annu Rev Microbiol. 1994;48:53-80 PMID: 7826018
  38. 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
  39. A carbon starvation survival gene of Pseudomonas putida is regulated by sigma 54.
    J Bacteriol. 1995 Apr;177(7):1850-9 PMID: 7896711
  40. Expression of the genes coding for the Escherichia coli integration host factor are controlled by growth phase, rpoS, ppGpp and by autoregulation.
    Mol Microbiol. 1994 Dec;14(5):1021-31 PMID: 7715442
  41. Effector-mediated stimulation of ATPase activity by the sigma 54-dependent transcriptional activator FHLA from Escherichia coli.
    J Bacteriol. 1995 May;177(10):2798-803 PMID: 7751289
  42. Signal sensing by sigma 54-dependent regulators: derepression as a control mechanism.
    Mol Microbiol. 1996 Feb;19(3):409-16 PMID: 8830233
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1996-07-00
Pages
3727-35
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC232629
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: [email protected]