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J. Biol. Chem., Vol. 280, Issue 16, 15921-15927, April 22, 2005

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Global Transcriptional Programs Reveal a Carbon Source Foraging Strategy by Escherichia coli^*

Mingzhu Liu, Tim Durfee, Julio E. Cabrera, Kai Zhao¶, Ding J. Jin, and Frederick R. Blattner||

From the Department of Genetics and ^¶McArdle Laboratory for Cancer Research, University of Wisconsin, Madison, Wisconsin 53706 and the Transcription Control Section, Gene Regulation and Chromosome Biology Laboratory, Center for Cancer Research, NCI at Frederick, National Institutes of Health, Frederick, Maryland 21702

By exploring global gene expression of Escherichia coli growing on six different carbon sources, we discovered a striking genome transcription pattern: as carbon substrate quality declines, cells systematically increase the number of genes expressed. Gene induction occurs in a hierarchical manner and includes many factors for uptake and metabolism of better but currently unavailable carbon sources. Concomitantly, cells also increase their motility. Thus, as the growth potential of the environment decreases, cells appear to devote progressively more energy on the mere possibility of improving conditions. This adaptation is not what would be predicated by classic regulatory models alone. We also observe an inverse correlation between gene activation and rRNA synthesis suggesting that reapportioning RNA polymerase (RNAP) contributes to the expanded genome activation. Significant differences in RNAP distribution in vivo, monitored using an RNAP-green fluorescent protein fusion, from energy-rich and energy-poor carbon source cultures support this hypothesis. Together, these findings represent the integration of both substrate-specific and global regulatory systems, and may be a bacterial approximation to metazoan risk-prone foraging behavior.

Received for publication, December 14, 2004 , and in revised form, January 26, 2005.

^* This work was supported by National Institutes of Health/NIGMS Grant GM35682-17S1 (to F. R. B.). Frederick R. Blattner has financial interest in NimbleGen Systems, Inc., DNASTAR, Inc. and Scarab Genomics, Inc. 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 Table 1.

This article was selected as a Paper of the Week.

^|| To whom correspondence should be addressed: Dept. of Genetics, University of Wisconsin-Madison, 445 Henry Mall, Madison, WI 53706. Tel.: 608-890-0191; Fax: 608-890-0167; E-mail: fred{at}genome.wisc.edu.

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