The periplasmic domain of the histidine autokinase CitA functions as a highly specific citrate receptor

Kaspar, S.; Perozzo, Remo; Reinelt, Stefan; Meyer, Margareta; Pfister, Karin; Scapozza, Léonardo; Bott, Michael

doi:10.1046/j.1365-2958.1999.01536.x

Cited by 92 publications

(117 citation statements)

References 54 publications

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“…The periplasmic detector region of the sensors PhoQ of Salmonella typhimurium, CitA of Klebsiella pneumoniae, and DcuS of E. coli directly binds Mg 2ϩ , citrate, and fumarate, respectively (33)(34)(35). Here we showed that the periplasmic domain of the TorS sensor detects indirectly the presence of TMAO by binding the TorT-TMAO complex.…”

Section: Discussionmentioning

confidence: 75%

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: 75%

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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“…Thus, even though sensor domains are expected to be functionally dimerized in situ on the membrane, they may exhibit quite low dimer affinity when isolated in solution. The E. coli PhoQ sensor domain has been shown to be monomeric in solution by analytical ultracentrifugation with a lower limit of 600 M measured for the K d of dimerization (12), and likewise both the CitA and DcuS sensor domains have also been reported to be mostly monomeric in solution (21,41). It follows that a certain lability may exist in the manner by which sensor domains self-associate, and therefore dimeric interactions within in a crystal-lattice environment may not necessarily be biologically relevant.…”

Section: Discussionmentioning

confidence: 99%

Crystal Structure of a Functional Dimer of the PhoQ Sensor Domain

Cheung

Bingman

Reyngold

et al. 2008

Journal of Biological Chemistry

128

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The PhoP-PhoQ two-component system is a well studied bacterial signaling system that regulates virulence and stress response. Catalytic activity of the histidine kinase sensor protein PhoQ is activated by low extracellular concentrations of divalent cations such as Mg 2؉ , and subsequently the response regulator PhoP is activated in turn through a classic phosphotransfer pathway that is typical in such systems. The PhoQ sensor domains of enteric bacteria contain an acidic cluster of residues (EDDDDAE) that has been implicated in direct binding to divalent cations. We have determined crystal structures of the wildtype Escherichia coli PhoQ periplasmic sensor domain and of a mutant variant in which the acidic cluster was neutralized to conservative uncharged residues (QNNNNAQ). The PhoQ domain structure is similar to that of DcuS and CitA sensor domains, and this PhoQ-DcuS-CitA (PDC) sensor fold is seen to be distinct from the superficially similar PAS domain fold. Analysis of the wild-type structure reveals a dimer that allows for the formation of a salt bridge across the dimer interface between Arg-50 and Asp-179 and with nickel ions bound to aspartate residues in the acidic cluster. The physiological importance of the salt bridge to in vivo PhoQ function has been confirmed by mutagenesis. The mutant structure has an alternative, nonphysiological dimeric association.

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“…The YufL/YufM TCS belongs to the CitA/ CitB family of TCSs. The members of this family that have already been characterized are CitA/CitB from E. coli (Kaspar & Bott, 2002) and Klebsiella pneumoniae (Bott et al, 1995;Kaspar et al, 1999), CitS/CitT from B. subtilis (Yamamoto et al, 2000) and Streptomyces coelicolor, YdbF/ YdbG from B. subtilis (Asai et al, 2000) and DcuS/DcuR from E. coli (Zientz et al, 1998;Golby et al, 1999). All these TCSs are involved in the control of genes required for TCA cycle intermediates import and utilization.…”

Section: Discussionmentioning

confidence: 99%

The Bacillus subtilis ywkA gene encodes a malic enzyme and its transcription is activated by the YufL/YufM two-component system in response to malate

et al. 2003

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A transcriptome comparison of a wild-type Bacillus subtilis strain growing under glycolytic or gluconeogenic conditions was performed. In particular, it revealed that the ywkA gene, one of the four paralogues putatively encoding a malic enzyme, was more transcribed during gluconeogenesis. Using a lacZ reporter fusion to the ywkA promoter, it was shown that ywkA was specifically induced by external malate and not subject to glucose catabolite repression. Northern analysis confirmed this expression pattern and demonstrated that ywkA is cotranscribed with the downstream ywkB gene. The ywkA gene product was purified and biochemical studies demonstrated its malic enzyme activity, which was 10-fold higher with NAD than with NADP (k cat/K m 102 and 10 s−1 mM−1, respectively). However, physiological tests with single and multiple mutant strains affected in ywkA and/or in ywkA paralogues showed that ywkA does not contribute to efficient utilization of malate for growth. Transposon mutagenesis allowed the identification of the uncharacterized YufL/YufM two-component system as being responsible for the control of ywkA expression. Genetic analysis and in vitro studies with purified YufM protein showed that YufM binds just upstream of ywkA promoter and activates ywkA transcription in response to the presence of malate in the extracellular medium, transmitted by YufL. ywkA and yufL/yufM could thus be renamed maeA for malic enzyme and malK/malR for malate kinase sensor/malate response regulator, respectively.

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The periplasmic domain of the histidine autokinase CitA functions as a highly specific citrate receptor

Cited by 92 publications

References 54 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

Crystal Structure of a Functional Dimer of the PhoQ Sensor Domain

The Bacillus subtilis ywkA gene encodes a malic enzyme and its transcription is activated by the YufL/YufM two-component system in response to malate

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