An unorthodox sensor protein (TorS) mediates the induction of the tor structural genes in response to trimethylamine N‐oxide in Escherichia coli

Jourlin, Cécile; Bengrine, Abderrahmane; Chippaux, Marc; Méjean, Vincent

doi:10.1111/j.1365-2958.1996.tb02648.x

Cited by 69 publications

(83 citation statements)

References 49 publications

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“…TorC interacts with the catalytic domain of TorA in the periplasm and forms a functional TorC-TorA respiratory complex of TMAO reductase (83). TorS detects TMAO presumably by its periplasmic region (123) and stimulates the expression of the torCAD operon. In addition, apoTorC lacking the heme C groups binds to the sensor TorS and negatively regulates kinase activity (i.e., when it is inactive and not able to form an active TorC-TorA respiratory complex).…”

Section: Prototypical Periplasmic-sensing Histidine Kinasesmentioning

confidence: 99%

Stimulus Perception in Bacterial Signal-Transducing Histidine Kinases

Mascher

Helmann

Unden

2006

Microbiol Mol Biol Rev

625

652

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SUMMARY Two-component signal-transducing systems are ubiquitously distributed communication interfaces in bacteria. They consist of a histidine kinase that senses a specific environmental stimulus and a cognate response regulator that mediates the cellular response, mostly through differential expression of target genes. Histidine kinases are typically transmembrane proteins harboring at least two domains: an input (or sensor) domain and a cytoplasmic transmitter (or kinase) domain. They can be identified and classified by virtue of their conserved cytoplasmic kinase domains. In contrast, the sensor domains are highly variable, reflecting the plethora of different signals and modes of sensing. In order to gain insight into the mechanisms of stimulus perception by bacterial histidine kinases, we here survey sensor domain architecture and topology within the bacterial membrane, functional aspects related to this topology, and sequence and phylogenetic conservation. Based on these criteria, three groups of histidine kinases can be differentiated. (i) Periplasmic-sensing histidine kinases detect their stimuli (often small solutes) through an extracellular input domain. (ii) Histidine kinases with sensing mechanisms linked to the transmembrane regions detect stimuli (usually membrane-associated stimuli, such as ionic strength, osmolarity, turgor, or functional state of the cell envelope) via their membrane-spanning segments and sometimes via additional short extracellular loops. (iii) Cytoplasmic-sensing histidine kinases (either membrane anchored or soluble) detect cellular or diffusible signals reporting the metabolic or developmental state of the cell. This review provides an overview of mechanisms of stimulus perception for members of all three groups of bacterial signal-transducing histidine kinases.

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Section: Prototypical Periplasmic-sensing Histidine Kinasesmentioning

confidence: 99%

Stimulus Perception in Bacterial Signal-Transducing Histidine Kinases

Mascher

Helmann

Unden

2006

Microbiol Mol Biol Rev

625

652

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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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“…In Escherichia coli, the main anaerobic respiratory pathway responsible for reduction of trimethylamine N-oxyde (TMAO) 1 to TMA (trimethylamine) requires the products of the torCAD operon which, in anaerobiosis, is induced in the presence of TMAO or related compounds via the two-component regulatory system, TorS/TorR (1,2).…”

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confidence: 99%

TorD, A Cytoplasmic Chaperone That Interacts with the Unfolded Trimethylamine N-Oxide Reductase Enzyme (TorA) in Escherichia coli

Pommier

Méjean

Giordano

et al. 1998

Journal of Biological Chemistry

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124

127

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Reduction of trimethylamine N-oxide (TMAO) in Escherichia coli involves the terminal molybdoreductase TorA, located in the periplasm, and the membrane anchored c type cytochrome TorC. In this study, the role of the TorD protein, encoded by the third gene of torCAD operon, is investigated. Construction of a mutant, in which the torD gene is interrupted, showed that the absence of TorD protein leads to a two times decrease of the final amount of TorA enzyme. However, specific activity and biochemical properties of TorA enzyme were similar to those of the enzyme produced in the wild type. Excess of TorD protein restores the normal level of TorA enzyme, and also, leads to the appearance of a new cytoplasmic form of TorA on SDS-polyacrylamide gel electrophoresis using gentle conditions. This probably indicates a new folding state of the cytoplasmic TorA protein when TorD is overexpressed. BIAcore techniques demonstrated direct specific interaction between the TorA and TorD proteins. This interaction was enhanced when TorA was previously unfolded by heating. Finally, as TorA is a molybdoenzyme, we demonstrated that TorD can interact with TorA before the molybdenum cofactor has been inserted. As TorD homologue encoding genes are found in various TMAO reductase loci, we propose that TorD is a chaperone protein specific for the TorA enzyme. It belongs to a family of TorD-like chaperones present in several bacteria, and, probably, involved in TMAO reductase folding.In Escherichia coli, the main anaerobic respiratory pathway responsible for reduction of trimethylamine N-oxyde (TMAO) 1 to TMA (trimethylamine) requires the products of the torCAD operon which, in anaerobiosis, is induced in the presence of TMAO or related compounds via the two-component regulatory system, TorS/TorR (1, 2).TMAO reductase (TorA), the terminal reductase of this system, is a 97-kDa molybdoprotein encoded by the torA gene (3, 4). Based on sequence homologies, TorA belongs to the Me 2 SO/ TMAO reductase family which includes the M 2 SO/TMAO reductases from Rhodobacter capsulatus and Rhodobacter sphaeroides (5) and TMAO reductase of Shewanella species.2 These enzymes share several properties: (i) they are all molybdoenzymes located in the periplasm of the bacterium and (ii) in each case, it has been proposed that a membrane anchored pentahemic c type cytochrome feeds electrons to the terminal enzyme (6, 7). In E. coli, this cytochrome, TorC, is encoded by torC, the first gene of the torCAD operon (4,8). While the role of the TorC and TorA proteins is well documented, the role of the third protein, TorD, predicted in the torCAD operon is not (4). However, the presence of TorD homologue proteins, not only in R. capsulatus and R. sphaeroides Tor systems (6, 7), but also in Shewanella species 2 is intriguing and suggests a similar role for this protein in these systems. As TorD contains two small hydrophobic segments, at its amino and carboxyl ends, respectively, it was proposed to be a membranous b type cytochrome involved in the electron transfer path...

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An unorthodox sensor protein (TorS) mediates the induction of the tor structural genes in response to trimethylamine N‐oxide in Escherichia coli

Cited by 69 publications

References 49 publications

Stimulus Perception in Bacterial Signal-Transducing Histidine Kinases

Stimulus Perception in Bacterial Signal-Transducing Histidine Kinases

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

TorD, A Cytoplasmic Chaperone That Interacts with the Unfolded Trimethylamine N-Oxide Reductase Enzyme (TorA) in Escherichia coli

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