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J. Biol. Chem., Vol. 279, Issue 53, 55792-55800, December 31, 2004

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A Homolog of Albino3/OxaI Is Essential for Thylakoid Biogenesis in the Cyanobacterium Synechocystis sp. PCC6803^*

Edward Spence, Shaun Bailey, Anja Nenninger, Simon Geir Møller, and Colin Robinson¶

From the Department of Biological Sciences, University of Warwick, Coventry CV4 7AL, and Department of Biology, Faculty of Medicine and Biological Sciences, University of Leicester, Leicester LE1 7RT, United Kingdom

YidC/OxaI play essential roles in the insertion of a wide range of membrane proteins in Eschericha coli and mitochondria, respectively. In contrast, the chloroplast thylakoid homolog Albino3 (Alb3) facilitates the insertion of only a specialized subset of proteins, and the vast majority insert into thylakoids by a pathway that is so far unique to chloroplasts. In this study, we have analyzed the role of Alb3 in the cyanobacterium Synechocystis sp. PCC6803, which contains internal thylakoids that are similar in some respects to those of chloroplasts. The single alb3 gene (slr1471) was disrupted by the introduction of an antibiotic cassette, and photoautotrophic growth resulted in the generation of a merodiploid species (but not full segregation), indicating an essential role for Alb3 in maintaining the photosynthetic apparatus. Thylakoid organization is lost under these conditions, and the levels of photosynthetic pigments fall to 40% of wild-type levels. Photosynthetic electron transport and oxygen evolution are reduced by a similar extent. Growth on glucose relieves the selective pressure to maintain photosynthetic competence, and under these conditions, the cells become completely bleached, again indicating that Alb3 is essential for thylakoid biogenesis. Full segregation could not be achieved under any growth regime, strongly suggesting that the slr1471 open reading frame is essential for cell viability.

Received for publication, September 27, 2004

^* This work was supported by Biotechnology and Biological Sciences Research Council Project Grants C18608 and P15253 and a Professorial Fellowship (to C. R.). 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. Tel.: 44-2476-523557; Fax: 44-2476-523568; E-mail: Crobinson{at}bio.warwick.ac.uk.

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