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J. Biol. Chem., Vol. 282, Issue 9, 6463-6472, March 2, 2007

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A New Membrane-bound Cytochrome c Works as an Electron Donor to the Photosynthetic Reaction Center Complex in the Purple Bacterium, Rhodovulum sulfidophilum^*

Yasuaki Kimura, Jean Alric, André Verméglio^¶, Shinji Masuda^||, Yuuki Hagiwara, Katsumi Matsuura, Keizo Shimada, and Kenji V. P. Nagashima¹

From the Department of Biological Science, Tokyo Metropolitan University, Minamiohsawa 1-1, Hachioji, Tokyo 192-0397, Japan, the Institut de Biologie Physico-Chimique, CNRS UMR 7141, 13 rue P. et M. Curie, 75005 Paris, France, the ^¶CEA/Cadarache DEVM-Laboratoire de Bioénergétique Cellulaire, UMR 6191 CNRS-CEA-Aix-Marseille II, 13108 Saint Paul lez Durance Cedex, France, and the ^||Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama 226-8501, Japan

A new type of membrane-bound cytochrome c was found in a marine purple photosynthetic bacterium, Rhodovulum sulfidophilum. This cytochrome c was significantly accumulated in cells growing under anaerobic photosynthetic conditions and showed an apparent molecular mass of 100 kDa when purified and analyzed by SDS-PAGE. The midpoint potential of this cytochrome c was 369 mV. Flash-induced kinetic measurements showed that this new cytochrome c can work as an electron donor to the photosynthetic reaction center. The gene coding for this cytochrome c was cloned and analyzed. The deduced molecular mass was nearly equal to 50 kDa. Its C-terminal heme-containing region showed the highest sequence identity to the water-soluble cytochrome c₂, although its predicted secondary structure resembles that of cytochrome c_y. Phylogenetic analyses suggested that this new cytochrome c has evolved from cytochrome c₂. We, thus, propose its designation as cytochrome c_2m. Mutants lacking this cytochrome or cytochrome c₂ showed the same growth rate as the wild type. However, a double mutant lacking both cytochrome c₂ and c_2m showed no growth under photosynthetic conditions. It was concluded that either the membrane-bound cytochrome c_2m or the water-soluble cytochrome c₂ work as a physiological electron carrier in the photosynthetic electron transfer pathway of Rvu. sulfidophilum.

Received for publication, May 10, 2006 , and in revised form, December 28, 2006.

The nucleotide sequence(s) reported in this paper has been submitted to the DDBJ/GenBank^TM/EBI Data Bank with accession number(s) AB257852 [GenBank] .

^* This work was supported in part by a grant-in-aid from the Ministry of Education, Culture, Sports, Science, and Technology, Japan. 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 To whom correspondence should be addressed: Dept. of Biological Science, Tokyo Metropolitan University, Minamiohsawa 1-1, Hachioji, Tokyo 192-0397, Japan. Tel.: 81-426-77-2583; Fax: 81-426-77-2559; E-mail: nagashima-kenji{at}c.metro-u.ac.jp.

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