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J. Biol. Chem., Vol. 279, Issue 49, 50818-50828, December 3, 2004

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The Escherichia coli fis Promoter Is Regulated by Changes in the Levels of Its Transcription Initiation Nucleotide CTP^*

Kimberly A. Walker, Prabhat Mallik¶, Timothy S. Pratt¶, and Robert Osuna¶||

From the ^¶Department of Biological Sciences, University at Albany, Albany, New York 12222 and the Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, Missouri 63110

Expression of the Escherichia coli nucleoid-associated protein Fis (factor for inversion stimulation) is controlled at the transcriptional level in accordance with the nutritional availability. It is highly expressed during early logarithmic growth phase in cells growing in rich medium but poorly expressed in late logarithmic and stationary phase. However, fis mRNA expression is prolonged at high levels throughout the logarithmic and early stationary phase when the preferred transcription initiation site (+1C) is replaced with A or G, indicating that initiation with CTP is a required component of the regulation pattern. We show that RNA polymerase-fis promoter complexes are short lived and that transcription is stimulated over 20-fold from linear or supercoiled DNA if CTP is present during formation of initiation complexes, which serves to stabilize these complexes. Use of fis promoter fusions to lacZ indicated that fis promoter transcription is sensitive to the intracellular pool of the predominant initiating NTP. Growth conditions resulting in increases in CTP pools also result in corresponding increases in fis mRNA levels. Measurements of NTP pools performed throughout the growth of the bacterial culture in rich medium revealed a dramatic increase in all four NTP levels during the transition from stationary to logarithmic growth phase, followed by reproducible oscillations in their levels during logarithmic growth, which later decrease during the transition from logarithmic to stationary phase. In particular, CTP pools fluctuate in a manner consistent with a role in regulating fis expression. These observations support a model whereby fis expression is subject to regulation by the availability of its initiating NTP.

Received for publication, June 7, 2004 , and in revised form, September 15, 2004.

^* This work was supported by National Institutes of Health Grant GM52051. 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.

These authors contributed equally to this work.

^|| To whom correspondence should be addressed: Dept. of Biological Sciences, University at Albany, 1400 Washington Ave., Albany, NY 12222. Tel.: 518-437-4492; Fax: 518-442-4767; E-mail: osuna{at}albany.edu.

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