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J. Biol. Chem., Vol. 279, Issue 10, 8530-8538, March 5, 2004

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Ammonium Sensing in Escherichia coli

ROLE OF THE AMMONIUM TRANSPORTER AmtB AND AmtB-GlnK COMPLEX FORMATION^*

Arnaud Javelle, Emmanuele Severi, Jeremy Thornton¶, and Mike Merrick¶||

From the Department of Molecular Microbiology, John Innes Centre, Norwich NR4 7UH, United Kingdom

The Amt proteins are high affinity ammonium transporters that are conserved in all domains of life. In bacteria and archaea the Amt structural genes (amtB) are invariably linked to glnK, which encodes a member of the P_II signal transduction protein family, proteins that regulate many facets of nitrogen metabolism. We have now shown that Escherichia coli AmtB is inactivated by formation of a membrane-bound complex with GlnK. Complex formation is reversible and occurs within seconds in response to micromolar changes in the extracellular ammonium concentration. Regulation is mediated by the uridylylation/deuridylylation of GlnK in direct response to fluctuations in the intracellular glutamine pool. Furthermore under physiological conditions AmtB activity is required for GlnK deuridylylation. Hence the transporter is an integral part of the signal transduction cascade, and AmtB can be formally considered to act as an ammonium sensor. This system provides an exquisitely sensitive mechanism to control ammonium flux into the cell, and the conservation of glnK linkage to amtB suggests that this regulatory mechanism may occur throughout prokaryotes.

Received for publication, November 12, 2003 , and in revised form, December 2, 2003.

^* 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.

Supported by a grant from the Biotechnology and Biological Sciences Research Council.

Supported by a John Innes Foundation studentship.

^¶ Supported by a grant-in-aid from the Biotechnology and Biological Sciences Research Council to the John Innes Centre.

^|| To whom correspondence should be addressed. E-mail: mike.merrick{at}bbsrc.ac.uk.

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