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J. Biol. Chem., Vol. 283, Issue 7, 4044-4050, February 15, 2008

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The Psb27 Protein Facilitates Manganese Cluster Assembly in Photosystem II^*

From the Department of Biology, Washington University, St. Louis, Missouri 63130

Photosystem II (PSII) is a large membrane protein complex that uses light energy to convert water to molecular oxygen. This enzyme undergoes an intricate assembly process to ensure accurate and efficient positioning of its many components. It has been proposed that the Psb27 protein, a lumenal extrinsic subunit, serves as a PSII assembly factor. Using a psb27 genetic deletion strain (psb27) of the cyanobacterium Synechocystis sp. PCC 6803, we have defined the role of the Psb27 protein in PSII biogenesis. While the Psb27 protein was not essential for photosynthetic activity, various PSII assembly assays revealed that the psb27 mutant was defective in integration of the Mn₄Ca₁Cl_x cluster, the catalytic core of the oxygen-evolving machinery within the PSII complex. The other lumenal extrinsic proteins (PsbO, PsbU, PsbV, and PsbQ) are key components of the fully assembled PSII complex and are important for the water oxidation reaction, but we propose that the Psb27 protein has a distinct function separate from these subunits. We show that the Psb27 protein facilitates Mn₄Ca₁Cl_x cluster assembly in PSII at least in part by preventing the premature association of the other extrinsic proteins. Thus, we propose an exchange of lumenal subunits and cofactors during PSII assembly, in that the Psb27 protein is replaced by the other extrinsic proteins upon assembly of the Mn₄Ca₁Cl_x cluster. Furthermore, we show that the Psb27 protein provides a selective advantage for cyanobacterial cells under conditions such as nutrient deprivation where Mn₄Ca₁Cl_x cluster assembly efficiency is critical for survival.

Received for publication, October 31, 2007 , and in revised form, December 14, 2007.

^* This work was supported in part by the National Science Foundation (MCB 0215359). 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 Fig. S1.

¹ Supported in part by a National Science Foundation individual graduate research fellowship.

² To whom correspondence should be addressed: Dept. of Biology, Campus Box 1137, Washington University, One Brookings Dr., St. Louis, MO 63130. Tel.: 314-935-6853; Fax: 314-935-6803; E-mail: Pakrasi{at}wustl.edu.

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