1887

Abstract

The Tat protein export system is located in the bacterial cytoplasmic membrane and operates in parallel to the well-known Sec pathway. While the Sec system only transports unstructured substrates, the function of the Tat pathway is to translocate folded proteins. The Tat translocase thus faces the formidable challenge of moving structured macromolecular substrates across the bacterial cytoplasmic membrane without rendering the membrane freely permeable to protons and other ions. The substrates of the Tat pathway are often proteins that bind cofactor molecules in the cytoplasm, and are thus folded, prior to export. Such periplasmic cofactor-containing proteins are essential for most types of bacterial respiratory and photosynthetic energy metabolism. In addition, the Tat pathway is involved in outer membrane biosynthesis and in bacterial pathogenesis. Substrates are targeted to the Tat pathway by amino-terminal signal sequences harbouring consecutive, essentially invariant, arginine residues, and movement of proteins through the Tat system is energized by the transmembrane proton electrochemical gradient. The TatA protein probably forms the transport channel while the TatBC proteins act as a receptor complex that recognizes the signal peptide of the substrate protein.

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2003-03-01
2020-03-31
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References

  1. Alami M, Trescher D, Wu L.-F., Müller M. 2002; Separate analysis of twin-arginine translocation (Tat)-specific membrane binding and translocation in Escherichia coli . J Biol Chem277:20499–20503
    [Google Scholar]
  2. Allen S. C. H, Barrett C. M. L, Ray N., Robinson C. 2002; Essential cytoplasmic domains in the Escherichia coli TatC protein. J Biol Chem277:10362–10366
    [Google Scholar]
  3. Berks B. C. 1996; A common export pathway for proteins binding complex redox cofactors?. Mol Microbiol22:393–404
    [Google Scholar]
  4. Berks B. C, Sargent F., Palmer T. 2000a; The Tat protein export pathway. Mol Microbiol35:260–274
    [Google Scholar]
  5. Berks B. C, Sargent F, de Leeuw E, Hinsley A. P, Stanley N. R, Jack R. L, Buchanan G., Palmer T. 2000b; A novel protein transport system involved in the biogenesis of bacterial electron transfer chains. Biochim Biophys Acta 1459;325–330
    [Google Scholar]
  6. Blaudeck N, Sprenger G. A, Freudl R., Wiegert T. 2001; Specificity of signal peptide recognition in Tat-dependent bacterial protein translocation . J Bacteriol 183:604–610
    [Google Scholar]
  7. Bogsch E, Brink S., Robinson C. 1997; Pathway specificity for a Δ pH-dependent precursor thylakoid lumen protein is governed by a ‘Sec-avoidance’ motif in the transfer peptide and a ‘Sec-incompatible’ mature protein. EMBO J16:3851–3859
    [Google Scholar]
  8. Bogsch E, Sargent F, Stanley N. R, Berks B. C, Robinson C., Palmer T. 1998; An essential component of a novel bacterial protein export system with homologues in plastids and mitochondria. J Biol Chem273:18003–18006
    [Google Scholar]
  9. Bolhuis A, Mathers J. E, Thomas J. D, Barrett C. E. M., Robinson C. 2001; TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli . J Biol Chem276:20213–20219
    [Google Scholar]
  10. Buchanan G, Sargent F, Berks B. C., Palmer T. 2001; A genetic screen for suppressors of Escherichia coli Tat signal peptide mutations establishes a critical role for the second arginine within the twin-arginine motif. Arch Microbiol177:107–112
    [Google Scholar]
  11. Buchanan G, de Leeuw E, Stanley N. R, Wexler M, Berks B. C, Sargent F., Palmer T. 2002; Functional complexity of the twin-arginine translocase TatC component revealed by site-directed mutagenesis. Mol Microbiol43:1457–1470
    [Google Scholar]
  12. Clark S. A., Theg S. M. 1997; A folded protein can be transported across the chloroplast envelope and thylakoid membranes. Mol Biol Cell8:923–934
    [Google Scholar]
  13. Cline K., Mori H. 2001; Thylakoid Δ pH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J Cell Biol154:719–729
    [Google Scholar]
  14. Cristóbal S, de Gier J.-W, Nielsen H., von Heijne G. 1999; Competition between Sec- and Tat-dependent protein translocation in Escherichia coli . EMBO J18:2982–2990
    [Google Scholar]
  15. de Leeuw E, Porcelli I, Sargent F, Palmer T., Berks B. C. 2001; Membrane interactions and self-association of the TatA and TatB components of the twin-arginine translocation pathway. FEBS Lett506:143–148
    [Google Scholar]
  16. de Leeuw E, Granjon T, Porcelli I, Alami M, Carr S. B, Müller M, Sargent F, Palmer T., Berks B. C. 2002; Oligomeric properties and signal peptide binding by Escherichia coli Tat protein transport complexes. J Mol Biol322:1135–1146
    [Google Scholar]
  17. DeLisa M. P, Samuelson P, Palmer T., Georgiou G. 2002; Genetic analysis of the twin-arginine translocator secretion pathway in bacteria. J Biol Chem277:29825–29831
    [Google Scholar]
  18. Dreusch A, Bürgisser D. M, Heizmann C. W., Zumft W. G. 1997; Lack of copper insertion into unprocessed cytoplasmic nitrous oxide reductase generated by an R20D substitution in the arginine consensus motif of the signal peptide. Biochim Biophys Acta1319:311–318
    [Google Scholar]
  19. Drew D, Sjöstrand D, Nilsson J, Urbig T, Chin C, de Gier J.-W., von Heijne G. 2002; Rapid topology mapping of Escherichia coli inner-membrane proteins by prediction and PhoA/GFP fusion analysis. Proc Natl Acad Sci U S A99:2690–2695
    [Google Scholar]
  20. Gouffi K, Santini C.-L., Wu L.-F. 2002; Topology determination and functional analysis of the Escherichia coli TatC protein. FEBS Lett525:65–70
    [Google Scholar]
  21. Gross R, Simon J., Kröger A. 1999; The role of the twin-arginine motif in the signal peptide encoded by the hydA gene of the hydrogenase from Wolinella succinogenes . Arch Microbiol172:227–232
    [Google Scholar]
  22. Halbig D, Wiegert T, Blaudeck N, Freudl R., Sprenger G. A. 1999; The efficient export of NADP-containing glucose-fructose oxidoreductase to the periplasm of Zymomonas mobilis depends both on an intact twin-arginine motif in the signal peptide and on the generation of a structural export signal induced by cofactor binding. Eur J Biochem263:543–551
    [Google Scholar]
  23. Hinsley A. P, Stanley N. R, Palmer T., Berks B. C. 2001; A naturally occurring bacterial Tat signal peptide lacking one of the ‘invariant’ arginine residues of the consensus motif. FEBS Lett497:45–49
    [Google Scholar]
  24. Hynds P. J, Robinson D., Robinson C. 1998; The Sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane. J Biol Chem273:34868–34874
    [Google Scholar]
  25. Ignatova Z, Hörnle C, Nurk A., Kasche V. 2002; Unusual signal peptide directs penicillin amidase from Escherichia coli to the Tat translocation machinery. Biochem Biophys Res Commun291:146–149
    [Google Scholar]
  26. Ize B, Gérard F, Zhang M, Chanal A, Voulhoux R, Palmer T, Filloux A., Wu L.-F. 2002; In vivo dissection of the Tat translocation pathway in Escherichia coli . J Mol Biol317:327–335
    [Google Scholar]
  27. Jack R. L, Sargent F, Berks B. C, Sawers G., Palmer T. 2001; Constitutive expression of the Escherichia coli tat genes indicates an important role for the twin-arginine translocase during aerobic and anaerobic growth. J Bacteriol183:1801–1804
    [Google Scholar]
  28. Johnson A. E., Haigh N. G. 2000; The ER translocon and retrotranslocation: is the shift into reverse manual or automatic?. Cell102:709–712
    [Google Scholar]
  29. Jongbloed J. D. H, Martin U, Antelman H, Hecker M, Tjalsma H, Venema G, Bron S, van Dijl J. M., Müller J. 2000; TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J Biol Chem275:41350–41357
    [Google Scholar]
  30. Lee P. A, Buchanan G, Stanley N. R, Berks B. C., Palmer T. 2002; Truncation analysis of TatA and TatB defines the minimal functional units required for protein translocation. J Bacteriol184:5871–5879
    [Google Scholar]
  31. Ma X., Cline K. 2000; Precursors bind to specific sites on thylakoid membranes prior to transport on the delta pH protein translocation system. J Biol Chem275:10016–10022
    [Google Scholar]
  32. Manting E. H., Driessen A. J. M. 2000; Escherichia coli translocase: the unravelling of a molecular machine. Mol Microbiol37:226–238
    [Google Scholar]
  33. Mori H., Cline K. 2001; Post-translational protein translocation into thylakoids by the Sec and Δ pH-dependent pathways. Biochim Biophys Acta 1541;80–90
    [Google Scholar]
  34. Mori H., Cline K. 2002; A twin arginine signal peptide and the pH gradient trigger reversible assembly of the thylakoid Δ pH/Tat translocase. J Cell Biol157:205–210
    [Google Scholar]
  35. Mould R. M., Robinson C. 1991; A proton gradient is required for the transport of two lumenal oxygen-evolving proteins across the thylakoid membrane. J Biol Chem266:12189–12193
    [Google Scholar]
  36. Musser S. M., Theg S. M. 2000; Characterization of the early steps of OE17 precursor transport by the thylakoid Δ pH/Tat machinery. Eur J Biochem167:2588–2598
    [Google Scholar]
  37. Nivière V, Wong S.-L., Voordouw G. 1992; Site-directed mutagenesis of the hydrogenase signal peptide consensus box prevents export of a β -lactamase fusion protein. J Gen Microbiol138:2173–2183
    [Google Scholar]
  38. Ochsner U. A, Snyder A, Vasil A. I., Vasil M. L. 2002; Effects of the twin-arginine translocase on secretion of virulence factors, stress response and pathogenesis. Proc Natl Acad Sci U S A99:8312–8317
    [Google Scholar]
  39. Oresnik I. J, Ladner C. L., Turner R. J. 2001; Identification of a twin-arginine leader binding protein. Mol Microbiol40:323–331
    [Google Scholar]
  40. Pommier J, Mejean V, Giordano G., Iobbi-Nivol C. 1998; TorD, a cytoplasmic chaperone that interacts with the unfolded trimethylamine-N-oxide reductase enzyme (TorA) in Escherichia coli. J Biol Chem273:16615–16620
    [Google Scholar]
  41. Pop O, Martin U, Abel C., Müller J. P. 2002; The twin-arginine signal peptide of PhoD and the TatAd/Cd proteins of Bacillus subtilis form an autonomous Tat translocation system. J Biol Chem277:3268–3273
    [Google Scholar]
  42. Porcelli I, de Leeuw E, Wallis R, van den Brink-van der Laan E, de Kruijff B, Wallace B. A, Palmer T., Berks B. C. 2002; Characterisation and membrane assembly of the TatA component of the Escherichia coli twin-arginine protein transport system. Biochemistry41:13690–13697
    [Google Scholar]
  43. Pugsley A. P. 1993; The complete general-secretory pathway in Gram-negative bacteria. Microbiol Rev57:50–108
    [Google Scholar]
  44. Rodrigue A, Chanal A, Beck K, Müller M., Wu L.-F. 1999; Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial Tat pathway. J Biol Chem274:13223–13228
    [Google Scholar]
  45. Roffey R. A., Theg S. M. 1996; Analysis of the import of carboxyl-terminal truncations of the 23-kilodalton subunit of the oxygen-evolving complex suggests that its structure is an important determinant for thylakoid transport. Plant Physiol111:1329–1338
    [Google Scholar]
  46. Sambasivarao D, Turner R. J, Simala-Grant J. L, Shaw G, Hu J., Weiner J. H. 2000; Multiple roles for the twin arginine leader sequence of dimethyl sulfoxide reductase of Escherichia coli. J Biol Chem275:22526–22531
    [Google Scholar]
  47. Sanders C, Wethkamp N., Lill H. 2001; Transport of cytochrome c derivatives by the bacterial Tat protein translocation system. Mol Microbiol41:241–246
    [Google Scholar]
  48. Santini C.-L, Ize B, Chanal A, Müller M, Giordano G., Wu L.-F. 1998; A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli . EMBO J17:101–112
    [Google Scholar]
  49. Santini C.-L, Bernadac A, Zhang M, Chanal A, Ize B, Blanco C., Wu L.-F. 2001; Translocation of jellyfish green fluorescent protein via the TAT system of Escherichia coli and change of its periplasmic localization in response to osmotic up-shock. J Biol Chem276:8159–8164
    [Google Scholar]
  50. Sargent F, Bogsch E, Stanley N. R, Wexler M, Robinson C, Berks B. C., Palmer T. 1998; Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J17:3640–3650
    [Google Scholar]
  51. Sargent F, Stanley N. R, Berks B. C., Palmer T. 1999; Sec-independent protein translocation in Escherichia coli : a distinct and pivotal role for the TatB protein. J Biol Chem274:36073–36083
    [Google Scholar]
  52. Sargent F, Gohlke U, de Leeuw E, Stanley N. R, Palmer T, Saibil H. R., Berks B. C. 2001; Purified components of the Tat protein transport system of Escherichia coli form a double-layered ring structure. Eur J Biochem268:3361–3367
    [Google Scholar]
  53. Sargent F, Berks B. C., Palmer T. 2002; Assembly of membrane-bound respiratory complexes by the Tat protein targeting system. Arch Microbiol178:77–84
    [Google Scholar]
  54. Settles A. M, Yonetani A, Baron A, Bush D. R, Cline K., Martienssen R. 1997; Sec-independent protein translocation by the maize Hcf106 protein. Science278:1467–1470
    [Google Scholar]
  55. Stanley N. R, Palmer T., Berks B. C. 2000; The twin arginine consensus motif of Tat signal peptides is involved in Sec-independent protein targeting in Escherichia coli . J Biol Chem275:11591–11596
    [Google Scholar]
  56. Stanley N. R, Findlay K, Berks B. C., Palmer T. 2001; Escherichia coli strains blocked in Tat-dependent protein export exhibit pleiotropic defects in the cell envelope. J Bacteriol183:139–144
    [Google Scholar]
  57. Stanley N. R, Sargent F, Buchanan G, Shi J, Stewart V, Palmer T., Berks B. C. 2002; Behaviour of topological marker proteins targeted to the Tat protein transport pathway. Mol Microbiol43:1005–1021
    [Google Scholar]
  58. Thomas J. D, Daniel R. A, Errington J., Robinson C. 2001; Export of active green fluorescent protein to the periplasm by the twin-arginine translocase (Tat) pathway in Escherichia coli. Mol Microbiol39:47–53
    [Google Scholar]
  59. Thony-Meyer L. 2000; Haem-polypeptide interactions during cytochrome c maturation. Biochim Biophys Acta1459:316–324
    [Google Scholar]
  60. Voordouw G. 2000; A universal system for the transport of redox proteins: early roots and latest developments. Biophys Chem86:131–140
    [Google Scholar]
  61. Voulhoux R, Ball G, Ize B, Vasil M. L, Lazdunski A, Wu L.-F., Filloux A. 2001; Involvement of the twin-arginine translocation system in protein translocation via the type II pathway. EMBO J20:6735–6741
    [Google Scholar]
  62. Weiner J. H, Bilous P. T, Shaw G. M, Lubitz S. P, Frost L, Thomas G. H, Cole J. A., Turner R. J. 1998; A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell93:93–101
    [Google Scholar]
  63. Wexler M, Bogsch E, Klösgen R. B, Palmer T, Robinson C., Berks B. C. 1998; Targeting signals for a bacterial Sec-independent export system direct plant thylakoid import by the Δ pH pathway. FEBS Lett431:339–342
    [Google Scholar]
  64. Wexler M, Sargent F, Jack R. L, Stanley N. R, Bogsch E. G, Robinson C, Berks B. C., Palmer T. 2000; TatD is a cytoplasmic protein with DNase activity: no requirement for TatD-family proteins in Sec-independent protein export. J Biol Chem275:16717–16722
    [Google Scholar]
  65. Whiteley M, Bangera M. G, Bumgarner R. E, Parsek M. R, Teitzel G. M, Lory S., Greenberg E. P. 2001; Gene expression in Pseudomonas aeruginosa biofilms. Nature413:860–864
    [Google Scholar]
  66. Wu L.-F, Ize B, Chanal A, Quentin Y., Fichant G. 2000; Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. J Mol Microbiol Biotechnol2:179–189
    [Google Scholar]
  67. Yahr T. L., Wickner W. T. 2001; Functional reconstitution of bacterial Tat translocation in vitro . EMBO J20:2472–2479
    [Google Scholar]
  68. Yen M. R, Tseng Y. H, Nguyen E. H, Wu L.-F., Saier M. H. Jr. 2002; Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch Microbiol177:441–450
    [Google Scholar]
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