An unsuspected autoregulatory pathway involving apocytochrome TorC and sensor TorS in
            <i>Escherichia coli</i>

Gon, Stéphanie; Jourlin-Castelli, Cécile; Théraulaz, Laurence; Méjean, Vincent

doi:10.1073/pnas.211330598

Cited by 32 publications

(25 citation statements)

References 33 publications

(35 reference statements)

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“…Therefore our study reveals a new regulatory mechanism and illustrates the diversity of signal detection by two-component systems. In fact, signal detection by the Tor regulatory system is much more complex than previously thought, not only because TMAO detection is indirect, but also because immature cytochrome TorC inhibits the kinase activity of TorS by binding to TorS N (28,36). TorS N can thus interact with both TorT and apoTorC.…”

Section: Discussionmentioning

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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Section: Discussionmentioning

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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“…TorC is a membrane-bound protein and carries the catalytic domain containing pentaheme c on the periplasmic surface of the membrane. 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.…”

Section: Prototypical Periplasmic-sensing Histidine Kinasesmentioning

confidence: 99%

“…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). This direct protein-protein interaction involves the C-terminal part of TorC and the periplasmic domain of TorS (83). Bordetella pertussis uses the BctDE TCS for controlling the expression of a citrate uptake system during growth on citrate (9).…”

Section: Prototypical Periplasmic-sensing Histidine Kinasesmentioning

confidence: 99%

Stimulus Perception in Bacterial Signal-Transducing Histidine Kinases

Mascher

Helmann

Unden

2006

Microbiol Mol Biol Rev

615

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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“…The E. coli TorS sensor detects the presence of not only TMAO but also immature TorC to allow optimal production of the structural components of the Tor respiratory system in inducing conditions (1,19). The physiological relevance of this subtle negative autoregulation by apocytochrome TorC is probably that TorC maturation is the limiting step of the Tor system biogenesis (11). Overproduction of the c-type cytochrome maturation machinery relieves the negative autoregulation by increasing the extent of TorC maturation (1).…”

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confidence: 99%

Genes Regulated by TorR, the Trimethylamine Oxide Response Regulator of Shewanella oneidensis

et al. 2004

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The torECAD operon encoding the trimethylamine oxide (TMAO) respiratory system of Shewanella oneidensis is positively controlled by the TorS/TorR two-component system when TMAO is available. Activation of the tor operon occurs upon binding of the phosphorylated response regulator TorR to a single operator site containing the direct repeat nucleotide sequence TTCATAN 4 TTCATA. Here we show that the replacement of any nucleotide of one TTCATA hexamer prevented TorR binding in vitro, meaning that TorR specifically interacts with this DNA target. Identical direct repeat sequences were found in the promoter regions of torR and of the new gene torF (SO4694), and they allowed TorR binding to both promoters. Real-time PCR experiments revealed that torR is negatively autoregulated, whereas torF is strongly induced by TorR in response to TMAO. Transcription start site location and footprinting analysis indicate that the operator site at torR overlaps the promoter ؊10 box, whereas the operator site at torF is centered at ؊74 bp from the start site, in agreement with the opposite role of TorR in the regulation of the two genes. Since torF and torECAD are positively coregulated by TorR, we propose that the TorF protein plays a role related to TMAO respiration.Trimethylamine oxide (TMAO) is a small compound mainly found in aquatic environments (15). In a number of marine animals including fish and crustaceans, it stabilizes proteins against the denaturing effect of stresses such as hydrostatic pressure or high urea or salt concentration (20,31,32). This protective role is not yet clearly established for bacteria, but many of them can use TMAO as a terminal electron acceptor for anaerobic respiration (3, 28). For example, Shewanella strains, which are gram-negative bacteria with wide respiratory capacities, can reduce TMAO efficiently to generate energy during fish spoilage (13,14,16). The main TMAO respiratory pathway of Shewanella species comprises a periplasmic terminal reductase (TorA) containing a molybdenum cofactor and a pentaheme c-type cytochrome (TorC) anchored to the inner membrane (9, 12). The genes encoding the Tor pathway are clustered in the torECAD operon, and this operon is regulated by the TorS/TorR two-component system (6). When TMAO is available in the medium, the sensor TorS transphosphorylates the response regulator TorR which, in turn, activates the torECAD operon by binding to a single operator site in the operon promoter (12).A similar Tor respiratory system is present in Escherichia coli, and its torCAD structural operon is also controlled by a TorS/TorR signal transduction system (18, 24). The E. coli TorS sensor detects the presence of not only TMAO but also immature TorC to allow optimal production of the structural components of the Tor respiratory system in inducing conditions (1, 19). The physiological relevance of this subtle negative autoregulation by apocytochrome TorC is probably that TorC maturation is the limiting step of the Tor system biogenesis (11). Overproduction of the c-type cytochr...

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An unsuspected autoregulatory pathway involving apocytochrome TorC and sensor TorS in Escherichia coli

Cited by 32 publications

References 33 publications

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

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

Stimulus Perception in Bacterial Signal-Transducing Histidine Kinases

Genes Regulated by TorR, the Trimethylamine Oxide Response Regulator of Shewanella oneidensis

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