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Published online 19 April 2004. doi:10.1083/jcb.200402100
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 165, Number 2, 213-222
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Article

F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis

Martin van der Laan, Philipp Bechtluft, Stef Kol, Nico Nouwen, and Arnold J.M. Driessen

Department of Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, 9751 NN Haren, Netherlands

Address correspondence to Arnold J.M. Driessen, Dept. of Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Kerklaan 30, 9751 NN Haren, Netherlands. Tel.: 31-50-3632164. Fax: 31-50-3632154. email: a.j.m.driessen{at}biol.rug.nl

The Escherichia coli YidC protein belongs to the Oxa1 family of membrane proteins that have been suggested to facilitate the insertion and assembly of membrane proteins either in cooperation with the Sec translocase or as a separate entity. Recently, we have shown that depletion of YidC causes a specific defect in the functional assembly of F1F0 ATP synthase and cytochrome o oxidase. We now demonstrate that the insertion of in vitro–synthesized F1F0 ATP synthase subunit c (F0c) into inner membrane vesicles requires YidC. Insertion is independent of the proton motive force, and proteoliposomes containing only YidC catalyze the membrane insertion of F0c in its native transmembrane topology whereupon it assembles into large oligomers. Co-reconstituted SecYEG has no significant effect on the insertion efficiency. Remarkably, signal recognition particle and its membrane-bound receptor FtsY are not required for the membrane insertion of F0c. In conclusion, a novel membrane protein insertion pathway in E. coli is described in which YidC plays an exclusive role.

Key Words: YidC; F1F0 ATP synthase; membrane insertion; membrane targeting; complex assembly


Abbreviations used in this paper: AMdiS, 4-acetamido-4'-maleimidylstilbene-2,2'-disulfonic acid; F0a, F0 subunit a; F0c, F0 subunit c; IMV, inner membrane vesicle; PMF, proton motive force; SRP, signal recognition particle.


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