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J. Biol. Chem., Vol. 281, Issue 15, 10002-10009, April 14, 2006

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Distinct Requirements for Translocation of the N-tail and C-tail of the Escherichia coli Inner Membrane Protein CyoA^*

Edwin van Bloois¹, Gert-Jan Haan², Jan-Willem de Gier, Bauke Oudega, and Joen Luirink²³

From the Department of Molecular Microbiology, Institute of Molecular Cell Biology, Vrije Universiteit, De Boelelaan 1087, 1081 HV Amsterdam, The Netherlands and Department of Biochemistry and Biophysics, Arrhenius Laboratories, Stockholm University, SE-106 91 Stockholm, Sweden

Inner membrane proteins (IMPs) of Escherichia coli use different pathways for membrane targeting and integration. YidC plays an essential but poorly defined role in the integration and folding of IMPs both in conjunction with the Sec translocon and as a Sec-independent insertase. Depletion of YidC only marginally affects the insertion of Sec-dependent IMPs, whereas it blocks the insertion of a subset of Sec-independent IMPs. Substrates of this latter "YidC-only" pathway include the relatively small IMPs M13 procoat, Pf3 coat protein, and subunit c of the F₁F₀ ATPase. Recently, it has been shown that the steady state level of the larger and more complex CyoA subunit of the cytochrome o oxidase is also severely affected upon depletion of YidC. In the present study we have analyzed the biogenesis of the integral lipoprotein CyoA. Collectively, our data suggest that the first transmembrane segment of CyoA rather than the signal sequence recruits the signal recognition particle for membrane targeting. Membrane integration and assembly appear to occur in two distinct sequential steps. YidC is sufficient to catalyze insertion of the N-terminal domain consisting of the signal sequence, transmembrane segment 1, and the small periplasmic domain in between. Translocation of the large C-terminal periplasmic domain requires the Sec translocon and SecA, suggesting that for this particular IMP the Sec translocon might operate downstream of YidC.

Received for publication, October 19, 2005 , and in revised form, January 26, 2006.

^* 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.

¹ Supported by the Council for Chemical Sciences of the Netherlands Society for Scientific Research.

² Supported by European Union Network Grant QLK-C-T2000-00082.

³ To whom correspondence should be addressed. Tel.: 31-20-5987175; Fax: 31-20-5986979; E-mail: joen.luirink{at}falw.vu.nl.

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