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Transcriptional regulation by BglJ-RcsB, a pleiotropic heteromeric activator in Escherichia coli.

ABSTRACT: The bacterial Rcs phosphorelay signals perturbations of the bacterial cell envelope to its response regulator RcsB, which regulates transcription of multiple loci related to motility, biofilm formation and various stress responses. RcsB is unique, as its set of target loci is modulated by interaction with auxiliary regulators including BglJ. The BglJ-RcsB heteromer is known to activate the HNS repressed leuO and bgl loci independent of RcsB phosphorylation. Here, we show that BglJ-RcsB activates the promoters of 10 additional loci (chiA, molR, sfsB, yecT, yqhG, ygiZ, yidL, ykiA, ynbA and ynjI). Furthermore, we mapped the BglJ-RcsB binding site at seven loci and propose a consensus sequence motif. The data suggest that activation by BglJ-RcsB is DNA phasing dependent at some loci, a feature reminiscent of canonical transcriptional activators, while at other loci BglJ-RcsB activation may be indirect by inhibition of HNS-mediated repression. In addition, we show that BglJ-RcsB activates transcription of bgl synergistically with CRP where it shifts the transcription start by 20 bp from a position typical for class I CRP-dependent promoters to a position typical for class II CRP-dependent promoters. Thus, BglJ-RcsB is a pleiotropic transcriptional activator that coordinates regulation with global regulators including CRP, LeuO and HNS.

SUBMITTER: Salscheider SL

PROVIDER: S-EPMC3950696 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

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Transcriptional regulation by BglJ-RcsB, a pleiotropic heteromeric activator in Escherichia coli.

Salscheider Silja Lucia SL Jahn Andreas A Schnetz Karin K

Nucleic acids research 20131213 5

The bacterial Rcs phosphorelay signals perturbations of the bacterial cell envelope to its response regulator RcsB, which regulates transcription of multiple loci related to motility, biofilm formation and various stress responses. RcsB is unique, as its set of target loci is modulated by interaction with auxiliary regulators including BglJ. The BglJ-RcsB heteromer is known to activate the HNS repressed leuO and bgl loci independent of RcsB phosphorylation. Here, we show that BglJ-RcsB activates ...[more]

PMID: 24335284

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Project description:Colibactin is a nonribosomal peptide/polyketide hybrid natural product expressed by different members of the Enterobacteriaceae which can be correlated with induction of DNA double-strand breaks and interference with cell cycle progression in eukaryotes. Regulatory features of colibactin expression are only incompletely understood. We used Escherichia coli strain M1/5 as a model to investigate regulation of expression of the colibactin determinant at the transcriptional level and to characterize regulatory elements located within the colibactin pathogenicity island itself. We measured clbR transcription in vitro and observed that cultivation in defined minimal media led to increased colibactin expression relative to rich media. Transcription of clbR directly responds to iron availability. We also characterized structural DNA elements inside the colibactin determinant involved in ClbR-dependent regulation, i.e., ClbR binding sites and a variable number of tandem repeats located upstream of clbR We investigated the impact of clbR overexpression or deletion at the transcriptome and proteome levels. Moreover, we compared global gene regulation under these conditions with that occurring upon overexpression or deletion of clbQ, which affects the flux of colibactin production. Combining the results of the transcriptome and proteome analyses with indirect measurements of colibactin levels by cell culture assays and an approximate quantification of colibactin via the second product of colibactin cleavage from precolibactin, N-myristoyl-d-asparagine, we demonstrate that the variable number of tandem repeats plays a significant regulatory role in colibactin expression. We identify ClbR as the only transcriptional activator known so far that is specific and essential for efficient regulation of colibactin production.IMPORTANCE The nonribosomal peptide/polyketide hybrid colibactin can be considered a bacterial virulence factor involved in extraintestinal infection and also a procarcinogen. Nevertheless, and despite its genotoxic effect, colibactin expression can also inhibit bacterial or tumor growth and correlates with probiotic anti-inflammatory and analgesic properties. Although the biological function of this natural compound has been studied extensively, our understanding of the regulation of colibactin expression is still far from complete. We investigated in detail the role of regulatory elements involved in colibactin expression and in the growth conditions that promote colibactin expression. In this way, our data shed light on the regulatory mechanisms involved in colibactin expression and may support the expression and purification of this interesting nonribosomal peptide/polyketide hybrid for further molecular characterization.

Dataset Information

Transcriptional regulation by BglJ-RcsB, a pleiotropic heteromeric activator in Escherichia coli.

Publications

Transcriptional regulation by BglJ-RcsB, a pleiotropic heteromeric activator in Escherichia coli.

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