Abstract
The xylR and xylS genes are divergent and control transcription of the TOL plasmid catabolic pathways for toluene metabolism. Four promoters are found in the 300-bp intergenic region: Pr1 and Pr2 are constitutive sigma70-dependent tandem promoters that drive expression of xylR, while expression of the xylS gene is driven from Ps2, a constitutive sigma70-dependent promoter, and by the regulatable sigma54 class Ps1 promoter. In Ps1 the XylR targets (upstream activator sequences [UASs]) overlap the Pr promoters, and two sites for integration host factor (IHF) binding are located at the region from positions -2 to -30 (-2/-30 region) and the -137/-156 region, the latter overlapping the Pr promoters. When the XylR protein binds to the UASs in the absence of effector, it represses expression from Pr promoters. In the XylR-plus background and in the absence of an effector, the level of expression from Ps1 is low, although detectable, whereas Ps2 is active. In this background and in the presence of an effector, XylR increases autorepression. In a sigma54-deficient Pseudomonas putida background, no expression occurred from Ps1 regardless of the presence of an effector. However, in the presence of an effector, the amount of RNA produced from Pr promoters was almost undetectable. This finding suggests that when no transcription occurred at the Ps1 promoter, clearance of XylR from the UASs was almost negligible. In this background, expression from Ps2 was very high regardless of the presence of an effector; this finding suggests that RNA polymerase containing sigma54 modulates expression from the downstream Ps2 sigma70-dependent promoter. In a P. putida IHF-minus background and in the presence of effector, Ps1 expression was the highest found; in contrast, the basal levels of this promoter were the lowest observed. This finding suggests that IHF acts in vivo as a repressor of the sigma54-dependent Ps1 promoter. In an IHF-deficient host background, expression from Ps2 in the presence of effector was negligible. Thus, binding of RNA polymerase containing sigma54 at the upstream promoter may modulate expression from the Ps2 promoter.
MeSH Terms
Bacterial Proteins/metabolism
Base Sequence
Benzyl Alcohol
DNA-Binding Proteins/genetics
DNA-Directed RNA Polymerases/physiology
Escherichia coli/genetics
Escherichia coli Proteins
Gene Expression Regulation, Bacterial/genetics
Genes, Bacterial/genetics
Homeostasis/genetics
Integration Host Factors
Molecular Sequence Data
Plasmids/genetics
Promoter Regions, Genetic/genetics
Pseudomonas putida/genetics,metabolism
RNA Polymerase Sigma 54
Sigma Factor/physiology
Toluene/metabolism
Trans-Activators/genetics
Transcription Factors/genetics
Transcription, Genetic/genetics
Transcriptional Activation/genetics
Chemicals
Bacterial Proteins
DNA-Binding Proteins
Escherichia coli Proteins
Integration Host Factors
Sigma Factor
Trans-Activators
Transcription Factors
XylR protein, Pseudomonas
XylS protein, Pseudomonas putida
integration host factor, Pseudomonas
rpoN protein, E coli
Toluene
DNA-Directed RNA Polymerases
RNA Polymerase Sigma 54
Benzyl Alcohol
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Marqués S
Consejo Superior de Investigaciones Científicas, Estación Experimental del Zaidín, Department of Biochemistry, E-18008 Granada, Spain.
Gallegos M T
Manzanera M
Holtel A
Timmis K N
Ramos J L
References (32)
32 references, click to expand
-
An upstream XylR- and IHF-induced nucleoprotein complex regulates the sigma 54-dependent Pu promoter of TOL plasmid.
EMBO J. 1991 May;10(5):1159-67
PMID: 2022186
-
Promoter-upstream activator sequences are required for expression of the xylS gene and upper-pathway operon on the Pseudomonas TOL plasmid.
Mol Microbiol. 1990 Sep;4(9):1551-6
PMID: 2287278
-
Upstream binding sequences of the XylR activator protein and integration host factor in the xylS gene promoter region of the Pseudomonas TOL plasmid.
Nucleic Acids Res. 1992 Apr 11;20(7):1755-62
PMID: 1579469
-
Analysis of an upstream regulatory sequence required for activation of the regulatory gene xylS in xylene metabolism directed by the TOL plasmid of Pseudomonas putida.
Mol Gen Genet. 1992 Jun;233(3):419-26
PMID: 1620097
-
Analysis of the mRNA structure of the Pseudomonas putida TOL meta fission pathway operon around the transcription initiation point, the xylTE and the xylFJ regions.
Biochim Biophys Acta. 1993 Nov 16;1216(2):227-36
PMID: 8241263
-
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
-
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
-
Co-regulation by bent DNA. Functional substitutions of the integration host factor site at sigma 54-dependent promoter Pu of the upper-TOL operon by intrinsically curved sequences.
J Biol Chem. 1994 Sep 9;269(36):22657-62
PMID: 8077217
-
Involvement of IHF protein in expression of the Ps promoter of the Pseudomonas putida TOL plasmid.
J Bacteriol. 1995 Jun;177(11):3312-5
PMID: 7768832
-
The sigma 54-dependent promoter Ps of the TOL plasmid of Pseudomonas putida requires HU for transcriptional activation in vivo by XylR.
J Bacteriol. 1995 Jul;177(13):3758-63
PMID: 7601841
-
The bacterial enhancer-binding protein NTRC is a molecular machine: ATP hydrolysis is coupled to transcriptional activation.
Genes Dev. 1995 Aug 15;9(16):2042-52
PMID: 7649482
-
The amino-terminal domain of the prokaryotic enhancer-binding protein XylR is a specific intramolecular repressor.
Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9392-6
PMID: 7568139
-
Expression of the TOL plasmid xylS gene in Pseudomonas putida occurs from a alpha 70-dependent promoter or from alpha 70- and alpha 54-dependent tandem promoters according to the compound used for growth.
J Bacteriol. 1996 Apr;178(8):2356-61
PMID: 8636038
-
ATP binding to the sigma 54-dependent activator XylR triggers a protein multimerization cycle catalyzed by UAS DNA.
Cell. 1996 Jul 26;86(2):331-9
PMID: 8706137
-
Structure and function of the Pseudomonas putida integration host factor.
J Bacteriol. 1996 Nov;178(21):6319-26
PMID: 8892836
-
Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators.
Annu Rev Microbiol. 1997;51:341-73
PMID: 9343354
-
A complementation analysis of the restriction and modification of DNA in Escherichia coli.
J Mol Biol. 1969 May 14;41(3):459-72
PMID: 4896022
-
Metabolism of toluene and xylenes by Pseudomonas (putida (arvilla) mt-2: evidence for a new function of the TOL plasmid.
J Bacteriol. 1975 Oct;124(1):7-13
PMID: 1176436
-
Molecular cloning of gene xylS of the TOL plasmid: evidence for positive regulation of the xylDEGF operon by xylS.
J Bacteriol. 1981 Nov;148(2):413-8
PMID: 6271729
-
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
-
Molecular cloning of regulatory gene xylR and operator-promoter regions of the xylABC and xylDEGF operons of the TOL plasmid.
J Bacteriol. 1983 Sep;155(3):1192-9
PMID: 6885718
-
Determination of the transcription initiation site and identification of the protein product of the regulatory gene xylR for xyl operons on the TOL plasmid.
J Bacteriol. 1985 Sep;163(3):863-9
PMID: 2993247
-
Altered effector specificities in regulators of gene expression: TOL plasmid xylS mutants and their use to engineer expansion of the range of aromatics degraded by bacteria.
Proc Natl Acad Sci U S A. 1986 Nov;83(22):8467-71
PMID: 3022293
-
Expression of the regulatory gene xylS on the TOL plasmid is positively controlled by the xylR gene product.
Proc Natl Acad Sci U S A. 1987 Aug;84(15):5182-6
PMID: 2440045
-
Interposon mutagenesis of soil and water bacteria: a family of DNA fragments designed for in vitro insertional mutagenesis of gram-negative bacteria.
Gene. 1987;52(2-3):147-54
PMID: 3038679
-
Regulatory circuits controlling transcription of TOL plasmid operon encoding meta-cleavage pathway for degradation of alkylbenzoates by Pseudomonas.
Mol Microbiol. 1987 Nov;1(3):293-300
PMID: 3448461
-
Nucleotide sequence of the regulatory gene xylR of the TOL plasmid from Pseudomonas putida.
Gene. 1988 Jun 30;66(2):301-6
PMID: 3169574
-
Involvement of Pseudomonas putida RpoN sigma factor in regulation of various metabolic functions.
J Bacteriol. 1989 Aug;171(8):4326-33
PMID: 2666396
-
Expression of sigma 54 (ntrA)-dependent genes is probably united by a common mechanism.
Microbiol Rev. 1989 Sep;53(3):367-76
PMID: 2677638
-
Regulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate range of the pathway.
J Bacteriol. 1989 Dec;171(12):6782-90
PMID: 2687253
-
DNA-looping and enhancer activity: association between DNA-bound NtrC activator and RNA polymerase at the bacterial glnA promoter.
Proc Natl Acad Sci U S A. 1990 Jul;87(14):5504-8
PMID: 2164685
-
Activation of the Pseudomonas TOL plasmid upper pathway operon. Identification of binding sites for the positive regulator XylR and for integration host factor protein.
J Biol Chem. 1991 Aug 25;266(24):15832-8
PMID: 1874736