Transphosphorylation of the TorR response regulator requires the three phosphorylation sites of the TorS unorthodox sensor in Escherichia coli

Jourlin, Cécile; Ansaldi, Mireille; Méjean, Vincent

doi:10.1006/jmbi.1997.0919

Cited by 76 publications

(82 citation statements)

References 32 publications

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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%

“…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).…”

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confidence: 99%

“…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 pathway for TMAO reduction (4,9).…”

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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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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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“…tor operon expression is under the positive control of the TorS͞TorR two-component system. TorS is a transmembrane sensor that detects the presence of TMAO in the medium and, in response, transphosphorylates TorR (17). Epistatic experiments have previously shown that the TorC autoregulatory pathway could implicate the TorS͞TorR system (10).…”

Section: Direct Interaction Between Apotorc and The Periplasmic Detectormentioning

confidence: 99%

“…Once activated, TorS transphosphorylates the TorR response regulator by a four-step phosphorelay. In turn, TorR-P binds to and induces the tor operon promoter (17). When TMAO is exhausted, TorR-P is rapidly dephosphorylated by TorS through a truncated reverse phosphorelay (18).…”

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confidence: 99%

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

Gon

Jourlin-Castelli²,

Théraulaz³

et al. 2001

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

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Trimethylamine N-oxide (TMAO) respiration is carried out mainly by the Tor system in Escherichia coli. This system is encoded by the torCAD operon and comprises a periplasmic TMAO reductase (TorA) and a c-type cytochrome (TorC), which shuttles electrons to TorA. Expression of the tor operon is positively controlled by the TorS͞TorR phosphorelay system in response to TMAO availability and negatively regulated by apocytochrome TorC. Interaction studies showed that, when immature, TorC can no longer bind TorA efficiently but can bind the periplasmic detector region of sensor TorS. ApoTorC negative autoregulation and TMAO induction are thus mediated by the same sensor protein. As apocytochromes related to TorC could not down-regulate the tor operon, we concluded that this negative control is highly specific. Moreover, the N-terminal half of apoTorC played no role in this control but the immature C-terminal domain of TorC strongly downregulated the tor operon and interacted with the TorS detector region. This sophisticated autoregulatory pathway thus involves the C-terminal domain of apoTorC and allows optimal TorC biogenesis by preventing from saturation the c-type cytochrome maturation machinery.

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Molecular analysis of the trimethylamine N -oxide (TMAO) reductase respiratory system from a Shewanella species

Santos

Iobbi‐Nivol

Couillault

et al. 1998

Journal of Molecular Biology

100

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Transphosphorylation of the TorR response regulator requires the three phosphorylation sites of the TorS unorthodox sensor in Escherichia coli

Cited by 76 publications

References 32 publications

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

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

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

Molecular analysis of the trimethylamine N -oxide (TMAO) reductase respiratory system from a Shewanella species

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