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J. Biol. Chem., Vol. 279, Issue 13, 12588-12597, March 26, 2004
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Probing the ArcA-P Modulon of Escherichia coli by Whole Genome Transcriptional Analysis and Sequence Recognition Profiling*
From the Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115
The ArcB/ArcA two-component signal transduction system of Escherichia coli regulates gene expression in response to the redox conditions of growth. Over the years, genetic screens have lead to the identification of about 30 ArcA-P-controlled operons that are involved in redox metabolism. However, the discovery of 3 targets that are not implicated in respiratory metabolism (the tra operon for plasmid conjugation, psi site for Xer-based recombination, and oriC site for chromosome replication) suggests that the Arc modulon may comprise additional operons that are involved in a myriad of functions. To identify these operons, we derived the ArcA-P-dependent transcription profile of E. coli using oligonucleotide-based microarray analysis. The findings indicated that 9% of all open reading frames in E. coli are affected either directly or indirectly by ArcA-P. To identify which operons are under the direct control of ArcA-P, we developed the ArcA-P recognition weight matrix from footprinting data and used it to scan the genome, yielding an ArcA-P sequence affinity map. By overlaying both methods, we identified 55 new Arc-regulated operons that are implicated in energy metabolism, transport, survival, catabolism, and transcriptional regulation. The data also suggest that the Arc response pathway, which translates into a net global downscaling of gene expression, overlaps partly with the FNR regulatory network. A conservative but reasonable assessment is that the Arc pathway recruits 100–150 operons to mediate a role in cellular adaptation that is more extensive than hitherto anticipated.
Received for publication, December 9, 2003
* This work was supported by United States Public Health Service Grant GM40993 from the NIGMS, National Institutes of Health. 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.
To whom correspondence should be addressed: Dept. of Biology, Massachusetts Institute of Technology, 77 Massachusetts Ave., Cambridge, MA 02139. Tel.: 617-452-4938; Fax: 617-253-8550; E-mail: dewulf{at}mit.edu.
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