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J. Biol. Chem., Vol. 280, Issue 7, 5236-5241, February 18, 2005

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Regulation of nif Expression in Methanococcus maripaludis

ROLES OF THE EURYARCHAEAL REPRESSOR NrpR, 2-OXOGLUTARATE, AND TWO OPERATORS^*

Thomas J. Lie, Gwendolyn E. Wood, and John A. Leigh

From the Department of Microbiology, University of Washington, Seattle, Washington 98195

The methanogenic archaean Methanococcus maripaludis can use ammonia, alanine, or dinitrogen as a nitrogen source for growth. The euryarchaeal nitrogen repressor NrpR controls the expression of the nif (nitrogen fixation) operon, resulting in full repression with ammonia, intermediate repression with alanine, and derepression with dinitrogen. NrpR binds to two tandem operators in the nif promoter region, nifOR₁ and nifOR₂. Here we have undertaken both in vivo and in vitro approaches to study the way in which NrpR, nifOR₁, nifOR₂, and the effector 2-oxoglutarate (2OG) combine to regulate nif expression, leading to a comprehensive understanding of this archaeal regulatory system. We show that NrpR binds as a dimer to nifOR₁ and cooperatively as two dimers to both operators. Cooperative binding occurs only with both operators present. nifOR₁ has stronger binding and by itself can mediate the repression of nif transcription during growth on ammonia, unlike the weakly binding nifOR₂. However, nifOR₂ in combination with nifOR₁ is critical for intermediate repression during growth on alanine. Accordingly, NrpR binds to both operators together with higher affinity than to nifOR₁ alone. NrpR responds directly to 2OG, which weakens its binding to the operators. Hence, 2OG is an intracellular indicator of nitrogen deficiency and acts as an inducer of nif transcription via NrpR. This model is upheld by the recent finding (J. A. Dodsworth and J. A. Leigh, submitted for publication) in our laboratory that 2OG levels in M. maripaludis vary with growth on different nitrogen sources.

Received for publication, October 18, 2004 , and in revised form, November 24, 2004.

^* This work was supported by National Institutes of Health Grant GM-55255. 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.

Present address: Dept. of Medicine, Div. of Allergy and Infectious Diseases, University of Washington, Seattle, WA 98104.

To whom correspondence should be addressed: University of Washington, Dept. of Microbiology, Box 357242, Seattle, WA 98195-7242. Tel.: 206-685-1390; Fax: 206-543-8297; E-mail: leighj{at}u.washington.edu.

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