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J. Biol. Chem., Vol. 278, Issue 51, 51277-51284, December 19, 2003

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The N-terminal Input Domain of the Sensor Kinase KdpD of Escherichia coli Stabilizes the Interaction between the Cognate Response Regulator KdpE and the Corresponding DNA-binding Site^*

Ralf Heermann, Karlheinz Altendorf, and Kirsten Jung¶

From the Universität Osnabrück, Fachbereich Biologie/Chemie, Abteilung Mikrobiologie, D-49069 Osnabrück and Technische Universität Darmstadt, Institut für Mikrobiologie und Genetik, Schnittspahnstrasse 10, D-64287 Darmstadt, Germany

The sensor kinase/response regulator system KdpD/KdpE of Escherichia coli regulates expression of the kdpFABC operon, which encodes the high affinity K⁺ transport system KdpFABC. The membrane-bound sensor kinase KdpD consists of an N-terminal input domain (comprising a large cytoplasmic domain and four transmembrane domains) and a cytoplasmic C-terminal transmitter domain. Here we show that the cytoplasmic N-terminal domain of KdpD (KdpD/1-395) alone supports semi-constitutive kdpFABC expression, which becomes dependent on the extracellular K⁺ concentration under K⁺-limiting growth conditions. However, it should be noted that the non-phosphorylatable derivative KdpD/H673Q or the absence of KdpD abolishes kdpFABC expression completely. KdpD/1-395 mediated kdpFABC expression requires the corresponding response regulator KdpE with an intact phosphorylation site. Experiments with an Escherichia coli mutant unable to synthesize acetyl phosphate as well as transposon mutagenesis suggest that KdpE is phosphorylated in vivo by low molecular weight phosphodonors in the absence of the full-length sensor kinase. Various biochemical approaches provide first evidence that kdpFABC expression mediated by KdpD/1-395 is due to a stabilizing effect of this domain on the binding of KdpEP to its corresponding DNA-binding site. Such a stabilizing effect of a sensor kinase domain on the DNA-protein interaction of the cognate response regulator has never been observed before for any other sensor kinase. It describes a new mechanism in bacterial two-component signal transduction.

Received for publication, April 11, 2003 , and in revised form, September 17, 2003.

^* This work was supported by the Deutsche Forschungsgemeinschaft Grant SFB431, P7 and the Fonds der Chemischen Industrie. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

^¶ To whom correspondence should be addressed. Tel.: 49-6151-16-5105; Fax: 49-6151-16-2956; E-mail: jung{at}bio.tu-darmstadt.de.

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