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Catabolite Repression and Activation in Bacillus subtilis: Dependency on CcpA, HPr, and HprK

Graciela L. Lorca,^1, Yong Joon Chung,^1, Ravi D. Barabote,¹ Walter Weyler,² Christophe H. Schilling,^1, and Milton H. Saier Jr^1*

Division of Biological Sciences, University of California at San Diego, La Jolla, California 92093,¹ Genencor International, Inc., Palo Alto, California 94304²

Received 1 July 2005/ Accepted 22 August 2005

Previous studies have suggested that the transcription factor CcpA, as well as the coeffectors HPr and Crh, both phosphorylated by the HprK kinase/phosphorylase, are primary mediators of catabolite repression and catabolite activation in Bacillus subtilis. We here report whole transcriptome analyses that characterize glucose-dependent gene expression in wild-type cells and in isogenic mutants lacking CcpA, HprK, or the HprK phosphorylatable serine in HPr. Binding site identification revealed which genes are likely to be primarily or secondarily regulated by CcpA. Most genes subject to CcpA-dependent regulation are regulated fully by HprK and partially by serine-phosphorylated HPr [HPr(Ser-P)]. A positive linear correlation was noted between the dependencies of catabolite-repressible gene expression on CcpA and HprK, but no such relationship was observed for catabolite-activated genes, suggesting that large numbers of the latter genes are not regulated by the CcpA-HPr(Ser-P) complex. Many genes that mediate nitrogen or phosphorus metabolism as well as those that function in stress responses proved to be subject to CcpA-dependent glucose control. While nitrogen-metabolic genes may be subject to either glucose repression or activation, depending on the gene, almost all glucose-responsive phosphorus-metabolic genes exhibit activation while almost all glucose-responsive stress genes show repression. These responses are discussed from physiological standpoints. These studies expand our appreciation of CcpA-mediated catabolite control and provide insight into potential interregulon control mechanisms in gram-positive bacteria.

Present address: Banting and Best, Department of Medical Research, Room 24, 112 College Street, Toronto, Ontario M5G 1L6, Canada.

Present and permanent address: Department of Life Science, Jeonju University, Chonju, Korea.

Present address: Genomatica, Inc., 5405 Morehouse, Suite 210, San Diego, CA 92121.

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