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J. Biol. Chem., Vol. 280, Issue 43, 36079-36087, October 28, 2005

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A Global Regulatory Role of Gluconeogenic Genes in Escherichia coli Revealed by Transcriptome Network Analysis^*

From the Department of Chemical and Biomolecular Engineering, University of California, Los Angeles, California 90095

In bacterial adaptation to the dynamic environment, metabolic genes are typically thought to be the executors, whereas global transcription regulators are regarded as the decision makers. Although the feedback from metabolic consequence is believed to be important, much less is understood. This work demonstrates that the gluconeogenic genes in Escherichia coli, ppsA, sfcA, and maeB, provide a feedback loop to the global regulator, cAMP receptor protein (CRP), in carbon source transition. Disruption of one of the gluconeogenic pathways has no phenotype in balanced growth, but causes a significant delay in the diauxic transition from glucose to acetate. To investigate the underlying mechanism, we measured the transcriptome profiles during the transition using DNA microarray, and network component analysis was employed to obtain the transcription factor activities. Results showed that one of the global regulators, CRP, was insufficiently activated during the transition in the ppsA deletion mutant. Indeed, addition of cAMP partially rescued the delay in transition. These results suggest that the gluconeogenic flux to phosphoenolpyruvate is important for full activation of adenylate cyclase through the phosphorylated enzyme IIA^glu of the phosphotransferase system. Reduction of this flux causes insufficient activation of CRP and a global metabolic deficiency, which exemplifies a significant feedback interaction from metabolism to the a global regulatory system.

Received for publication, July 27, 2005

^* This work was supported in part by National Science Foundation ITR program Grant CCF-0326605 and the UCLA IGERT Bioinformatics program supported by National Science Foundation Grant DGE9987641. 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.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Tables A1 and A2.

¹ To whom correspondence should be addressed: UCLA, 420 Westwood Plaza, Los Angeles, CA 90095. Tel.: 310-825-1656; Fax: 310-206-4107; E-mail: liaoj{at}ucla.edu.

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