The torR gene of Escherichia coli encodes a response regulator protein involved in the expression of the trimethylamine N-oxide reductase genes

Simon, Gwenola; Méjean, Vincent; Jourlin, Cécile; Chippaux, Marc; Pascal, Marie-Claire

doi:10.1128/jb.176.18.5601-5606.1994

Cited by 74 publications

(64 citation statements)

References 38 publications

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“…The TorI protein was first identified as a TorR response regulator inhibitor (7). TorR is part of the two-component system TorS/TorR required for torCAD operon expression in Escherichia coli (8,9). In response to the presence of trimethylamine-N-oxide (TMAO) in the environment, the TorS sensor kinase autophosphorylates and transfers a phosphoryl group to TorR through a four-step phosphorelay leading to the induction of the torCAD operon, which encodes the TMAO reductase respiratory system (10).…”

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confidence: 99%

Structural and Genetic Analyses Reveal a Key Role in Prophage Excision for the TorI Response Regulator Inhibitor

Elantak

Ansaldi

Guerlesquin

et al. 2005

Journal of Biological Chemistry

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TorI (Tor inhibition protein) has been identified in Escherichia coli as a protein inhibitor acting through protein-protein interaction with the TorR response regulator. This interaction, which does not interfere with TorR DNA binding activity, probably prevents the recruitment of RNA polymerase to the torC promoter. In this study we have solved the solution structure of TorI, which adopts a prokaryotic winged-helix arrangement. Despite no primary sequence similarity, the three-dimensional structure of

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confidence: 99%

Structural and Genetic Analyses Reveal a Key Role in Prophage Excision for the TorI Response Regulator Inhibitor

Elantak

Ansaldi

Guerlesquin

et al. 2005

Journal of Biological Chemistry

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“…The TorR protein in E. coli is a well characterized transcriptional activator of the OmpR response regulator family (10,11). In response to the presence of trimethylamine N-oxide (TMAO) in the environment, the sensor kinase TorS autophosphorylates and transfers a phosphoryl group to TorR through a four-step phosphorelay leading to the expression of the torCAD operon (12).…”

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confidence: 99%

“…Protein Purifications. TorR was overproduced and purified as described (11). TorR N and TorR C were produced from BL21(DE3) harboring plasmids pET-R N or pET-R C , respectively.…”

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confidence: 99%

TorI, a response regulator inhibitor of phage origin inEscherichia coli

Ansaldi¹,

Théraulaz²,

Méjean³

2004

Proc. Natl. Acad. Sci. U.S.A.

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The torI gene has been identified by using a genetic multicopy approach as a negative regulator of the torCAD operon that encodes the trimethylamine N-oxide reductase respiratory system in Escherichia coli. The negative effect was due to a previously unidentified small ORF (66 aa) of phage origin that we called torI for Tor inhibition. Overexpression of torI led to an 8-fold decrease of the torCAD operon transcription. This operon is positively regulated, in the presence of trimethylamine N-oxide, by a fourstep phosphorelay involving the TorS sensor and the TorR response regulator. Epistatic experiments showed that TorI acts downstream of TorS and needs the presence of TorR. In vitro experiments showed that it is neither a TorR phosphatase nor a histidine kinase inhibitor and that it binds to the effector domain of TorR. Unexpectedly, TorI did not impede TorR DNA binding, and we propose that it may prevent RNA polymerase recruitment to the torC promoter. This study thus reveals a previously uncharacterized class of response regulator inhibitors.

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“…Disruption of either one of these genes abolishes tor operon induction. The torS and torR genes encode a two-component regulatory system in which TorS is an unorthodox sensor containing three phosphorylation sites and TorR a response regulator of the OmpR family (8,9). At its N-terminal extremity, TorS contains a large detector region of about 300 residues oriented toward the periplasm and flanked by two transmembrane segments.…”

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confidence: 99%

TorT, a Member of a New Periplasmic Binding Protein Family, Triggers Induction of the Tor Respiratory System upon Trimethylamine N-Oxide Electron-acceptor Binding in Escherichia coli

Baraquet

Théraulaz

Guiral

et al. 2006

Journal of Biological Chemistry

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In anaerobiosis, Escherichia coli can use trimethylamine N-oxide (TMAO) as a terminal electron acceptor. Reduction of TMAO in trimethylamine (TMA) is mainly performed by the respiratory TMAO reductase. This system is encoded by the torCAD operon, which is induced in the presence of TMAO. This regulation involves a two-component system comprising TorS, an unorthodox histidine kinase, and TorR, a response regulator. A third protein, TorT, sharing homologies with periplasmic binding proteins, plays a key role in this regulation because disruption of the torT gene abolishes tor expression. In this study we showed that TMAO protects TorT against degradation by the GluC endoproteinase and modifies its temperature-induced CD spectrum. We also isolated a TorT negative mutant that is no longer protected by TMAO from degradation by GluC. Isothermal titration calorimetry confirmed that TorT binds TMAO with a binding constant of 150 M. Therefore, we conclude that TorT binds TMAO and that this binding promotes a conformational change of TorT. We also showed that TorT interacts with the periplasmic domain of TorS in both the presence and absence of TMAO but the TorT-TMAO complex induces a higher GluC protection of TorS than TorT alone. These results support the idea that TMAO binding to TorT induces a cascade of conformational changes from TorT to TorS, leading to TorS activation. We identified several homologues of the TorT protein that define a new family of periplasmic binding proteins. We thus propose that the members of this family bind TMAO or related compounds and that they are involved in signal transduction or even substrate transport.In anaerobiosis, Escherichia coli can use alternative terminal electron acceptors such as nitrate, nitrite, fumarate, dimethyl sulfoxide (Me 2 SO), or trimethylamine N-oxide (TMAO) 3 for respiration (1). Reduction of TMAO in trimethylamine (TMA) mainly involves the TMAO reductase system. This respiratory system comprises three proteins: TorC, TorA, and TorD. The TorC protein is a pentahemic c-type cytochrome anchored to the membrane and oriented toward the periplasmic compartment. The TorA protein, located in the periplasm, is the terminal reductase and receives the electrons from TorC (2). TorD is a cytoplasmic protein that acts as both a specific chaperone and an escort protein for TorA, allowing TorA maturation and protection before its translocation into the periplasm by the Tat system (3-6).The Tor respiratory system is encoded by the torCAD operon that is induced in the presence of TMAO (7). The TMAO control is strict because there is almost no expression of the tor operon in the absence of TMAO. The three genes torS, torT, and torR, located upstream of the tor operon, are involved in this regulation. Disruption of either one of these genes abolishes tor operon induction. The torS and torR genes encode a two-component regulatory system in which TorS is an unorthodox sensor containing three phosphorylation sites and TorR a response regulator of the OmpR family (8, 9). At its N-term...

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The torR gene of Escherichia coli encodes a response regulator protein involved in the expression of the trimethylamine N-oxide reductase genes

Abstract: Expression of the Escherichia coli torCAD operon encoding the trimethylamine N-oxide (TMAO) reductase system is induced by both TMAO and anaerobiosis. A torR insertion mutant unable to express the torA gene had previously been isolated. (10,13). This

Cited by 74 publications

References 38 publications

Structural and Genetic Analyses Reveal a Key Role in Prophage Excision for the TorI Response Regulator Inhibitor

Structural and Genetic Analyses Reveal a Key Role in Prophage Excision for the TorI Response Regulator Inhibitor

TorI, a response regulator inhibitor of phage origin inEscherichia coli

TorT, a Member of a New Periplasmic Binding Protein Family, Triggers Induction of the Tor Respiratory System upon Trimethylamine N-Oxide Electron-acceptor Binding in Escherichia coli

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