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Structure of the TatC core of the twin-arginine protein transport system

Nature volume 492, pages 210–214 (2012)Cite this article

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Abstract

The twin-arginine translocation (Tat) pathway is one of two general protein transport systems found in the prokaryotic cytoplasmic membrane and is conserved in the thylakoid membrane of plant chloroplasts. The defining, and highly unusual, property of the Tat pathway is that it transports folded proteins, a task that must be achieved without allowing appreciable ion leakage across the membrane. The integral membrane TatC protein is the central component of the Tat pathway. TatC captures substrate proteins by binding their signal peptides. TatC then recruits TatA family proteins to form the active translocation complex. Here we report the crystal structure of TatC from the hyperthermophilic bacterium Aquifex aeolicus. This structure provides a molecular description of the core of the Tat translocation system and a framework for understanding the unique Tat transport mechanism.

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Figure 1: Purified A. aeolicus TatC binds Tat signal peptides.
Figure 2: Structure of A. aeolicus TatC.
Figure 3: Identification of the signal peptide binding site on TatC.
Figure 4: Sites of interaction with other Tat components.
Figure 5: A conceptual model for the environment of TatC in the substrate-bound translocation site.

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Protein Data Bank

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The coordinates and experimental data have been deposited at the Protein Data Bank with accession code 4b4a.

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Acknowledgements

We thank D. Byrne, G. Orriss and R. Owens for their contributions to the early stages of this project; R. Keller for advice; and J. Willem de Gier, D. Daley and R. Huber for providing strains and reagents. This work was supported by the Wellcome Trust (studentships to S.E.R., J.E.G. and M.A.M.; grant 083599, P.R.; grant 092970MA, M.S.P.S.), the Swedish Foundation for Strategic Research (‘Future research leaders 4’ to M.H.), the Swedish Research Council (grant 2010-5061 to M.H.), the E .P. Abrahams Cephalosporin Trust (M.K. and F.R.), the Biotechnology and Biological Sciences Research Council (studentship, M.J.L.; grant BB/E023347/1, S-M.L.; grant BB/1019855/1, P.J.S.), the Medical Research Council (grant G1001640, F.J.; grant G0900888, S.J.), and the European Research Council (Advanced Grant IMPRESS, J.M. and C.V.R.). Work in S.M.L.’s group is funded by the James Martin 21st Century School Vaccine Design Institute.

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  1. Michael J. Tarry, James E. Graham, Michael J. Lukey & Pietro Roversi

    Present address: Present addresses: Department of Biochemistry, McGill University Room 457, Bellini Life Science Complex, 3649 Promenade Sir William Osler, Montreal, Quebec H3G 0B1, Canada (M.J.T.); 306 Briggs Hall, Department of Microbiology, University of California Davis, One Shields Avenue, Davis, California 95616-2866, USA (J.E.G.); Department of Molecular Medicine, Cornell University, Ithaca, New York 14853, USA (M.J.L.); CIC bioGUNE, Parque Tecnologico de Bizkaia, 48160 Dorio, Bizkaia, Spain (P.R.).,

Authors and Affiliations

  1. Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford OX1 3RE, UK,

    Sarah E. Rollauer, James E. Graham, Steven Johnson, Sai-Man Liu, Michael J. Lukey, Melanie A. McDowell, Pietro Roversi & Susan M. Lea

  2. Department of Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, UK,

    Sarah E. Rollauer, James E. Graham, Martin Krehenbrink, Sai-Man Liu, Michael J. Lukey, Fernanda Rodriguez, Phillip J. Stansfeld, Mark S. P. Sansom & Ben C. Berks

  3. Department of Biochemistry and Biophysics, Stockholm Center for Biomembrane Research, Stockholm University, S-106 91 Stockholm, Sweden,

    Michael J. Tarry, Mari Jääskeläinen & Martin Högbom

  4. Division of Molecular Microbiology, College of Life Sciences, University of Dundee, Dundee DD1 5EH, UK,

    Franziska Jäger & Tracy Palmer

  5. Department of Chemistry, Physical & Theoretical Chemistry Laboratory, University of Oxford, South Parks Road, Oxford OX1 3QZ, UK,

    Julien Marcoux & Carol V. Robinson

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Contributions

The experiments were designed and manuscript written by S.E.R., M.J.T., B.C.B, S.M.L., M.H. and T.P. Experimental work was performed as follows: crystallization trials: S.E.R. and M.J.T.; structure determination: S.E.R., P.R. and S.M.L.; cloning and expression screening: J.E.G., M.J.T., M.J., S-M.L. and M.J.L.; homogeneity screening: M.J.T., M.J., S.E.R., M.A.M. and S.J.; MD simulations: P.J.S. and M.S.P.S; disulphide crosslinking: F.J. and T.P.; signal peptide binding and BN-PAGE: S.E.R., M.K. and F.R.; mass spectrometry: J.M. and C.V.R.

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Correspondence to Ben C. Berks or Susan M. Lea.

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Rollauer, S., Tarry, M., Graham, J. et al. Structure of the TatC core of the twin-arginine protein transport system. Nature 492, 210–214 (2012). https://doi.org/10.1038/nature11683

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