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J. Biol. Chem., Vol. 279, Issue 15, 14860-14870, April 9, 2004

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A Threshold Mechanism Governing Activation of the Developmental Regulatory Protein ^F in Bacillus subtilis^*

Karen Carniol, Patrick Eichenberger, and Richard Losick¶

From the Department of Molecular and Cellular Biology, Harvard University, Cambridge, Massachusetts 01238

The RNA polymerase sigma factor ^F is a developmental regulatory protein that is activated in a cell-specific manner following the formation of the polar septum during the process of spore formation in the bacterium Bacillus subtilis. Activation of ^F depends on the membrane-bound phosphatase SpoIIE, which localizes to the septum, and on the formation of the polar septum itself. SpoIIE is responsible for dephosphorylating and thereby activating the phosphoprotein SpoIIAA, which, in turn, triggers the release of ^F from the anti-^F factor SpoIIAB. Paradoxically, however, the presence of unphosphorylated SpoIIAA is insufficient to cause ^F activation as SpoIIAA reaches substantial levels in mutants blocked in polar septation. We now describe mutants of SpoIIE, SpoIIAA, and SpoIIAB that break the dependence of ^F activation on polar division. Analysis of these mutants indicates that unphosphorylated SpoIIAA must reach a threshold concentration in order to trigger the release of ^F from SpoIIAB. Evidence is presented that this threshold is created by the action of SpoIIAB, which can form an alternative, long lived complex with SpoIIAA. We propose that formation of the SpoIIAA-SpoIIAB complex serves as a sink that traps SpoIIAA in an inactive state and that only when unphosphorylated SpoIIAA is in excess to the sink does activation of ^F take place.

Received for publication, December 29, 2003 , and in revised form, January 25, 2004.

^* This work was supported by National Institutes of Health Grant GM18458 (to R. L.). 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 an additional figure.

Supported by a National Science Foundation predoctoral fellowship.

Supported by the Swiss National Science Foundation and a Merck Core Educational Support Program.

^¶ To whom correspondence should be addressed. Tel.: 617-495-1774; Fax: 617-496-4642; E-mail: losick{at}mcb.harvard.edu.

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