Twin Arginine Translocation in Yersinia

  • Moa Lavander
  • Åke Forsberg
  • Jeanette E. Bröms
  • Solveig K. Ericsson
Part of the Advances In Experimental Medicine And Biology book series (AEMB, volume 603)

Bacteria utilise Twin arginine translocation (Tat) to deliver folded proteins across the cytoplasmic membrane. Disruption of Tat typically results in pleiotropic effects on e.g. growth, stress resistance, bacterial membrane biogenesis, motility and cell morphology. Further, Tat is coupled to virulence in a range of pathogenic bacteria, including species of Pseudomonas, Legionella, Agrobacterium and Mycobacterium. We have investigated this, for Yersinia, previously unexplored system, and have shown that the Tat pathway is functional and absolutely required for virulence of Yersinia pseudotuberculosis. A range of putative Yersinia Tat substrates have been predicted in silico, which together with the Tat system itself may be interesting targets for future development of antimicrobial treatments. Here we present a brief review of bacterial Tat and discuss our results concerning this system in Yersinia.


Yersinia Pestis Twin Arginine Translocation Twin Arginine Isogenic Wild Type Swedish Defence Research Agency 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Achtman, M., Zurth, K., Morelli, G., Torrea, G., Guiyoule, A. and Carniel, E. (1999) Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. U S A 96,14043-8.CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alami, M., Luke, I., Deitermann, S., Eisner, G., Koch, H.G., Brunner, J. and Muller, M. (2003) Differential interactions between a twin-arginine signal peptide and its translocase in Escherichia coli. Mol. Cell 12, 937-946.CrossRefPubMedGoogle Scholar
  3. Behrendt, J., Standar, K., Lindenstrauss, U. and Bruser, T. (2004) Topological studies on the twin-arginine translocase component TatC. FEMS Microbiol Lett 234, 303-308.CrossRefPubMedGoogle Scholar
  4. Bendtsen, J. D., Nielsen, H., Widdick, D., Palmer, T. and Brunak, S. (2005). Prediction of twin-arginine signal peptides. BMC Bioinformatics 6,167CrossRefPubMedPubMedCentralGoogle Scholar
  5. Berks, B.C. (1996) A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol. 22, 393-404.CrossRefPubMedGoogle Scholar
  6. Berks, B. C., Sargent, F. and Palmer, T. (2000). The Tat protein export pathway. Mol. Micro-biol. 35,260-74.CrossRefGoogle Scholar
  7. Berks, B.C., Palmer, T. and Sargent, F. (2003) The Tat protein translocation pathway and its role in microbial physiology. Adv. Microb. Physiol. 47, 187-254.CrossRefPubMedGoogle Scholar
  8. Bogsch, E.G., Sargent, F., Stanley, N.R., Berks, B.C., Robinson, C. and Palmer, T. (1998) An essential component of a novel bacterial protein export system with homologues in plas-tids and mitochondria. J. Biol. Chem. 273, 18003-18006.CrossRefPubMedGoogle Scholar
  9. Bolhuis, A., Bogsch, E.G. and Robinson, C. (2000) Subunit interactions in the twin-arginine translocase complex of Escherichia coli. FEBS Lett. 472, 88-92.CrossRefPubMedGoogle Scholar
  10. Bröms, J.E., Forslund, A.L., Forsberg, Å. and Francis, M.S. (2003a) Dissection of homolo-gous translocon operons reveals a distinct role for YopD in type III secretion by Yersinia pseudotuberculosis. Microbiology 149, 2615-2626.CrossRefPubMedGoogle Scholar
  11. Bröms, J.E., Sundin, C., Francis, M.S. and Forsberg, Å. (2003b) Comparative analysis of type III effector translocation by Yersinia pseudotuberculosis expressing native LcrV or PcrV from Pseudomonas aeruginosa. J. Infect. Dis. 188, 239-249.CrossRefPubMedGoogle Scholar
  12. Chain, P.S., Carniel, E., Larimer, F.W., Lamerdin, J., Stoutland, P.O., Regala, W.M., Georgescu, A.M., Vergez, L.M., Land, M.L., Motin, V.L., Brubaker, R.R., Fowler, J., Hinnebusch, J., Marceau, M., Medigue, C., Simonet, M., Chenal-Francisque, V., Souza, B., Dacheux, D., Elliott, J.M., Derbise, A., Hauser, L.J. and Garcia, E. (2004) Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotu-berculosis. Proc. Natl. Acad. Sci. U S A 101, 13826-13831.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Dalbey, R.E. and Robinson, C. (1999) Protein translocation into and across the bacterial plasma membrane and the plant thylakoid membrane. Trends Biochem. Sci. 24, 17-22.Google Scholar
  14. de Leeuw, E., Granjon, T., Porcelli, I., Alami, M., Carr, S.B., Muller, M., Sargent, F., Palmer, T. and Berks, B.C. (2002) Oligomeric properties and signal peptide binding by Es-cherichia coli Tat protein transport complexes. J. Mol. Biol. 322, 1135-1146.CrossRefPubMedGoogle Scholar
  15. Deng, W., Burland, V., Plunkett, G., 3rd, Boutin, A., Mayhew, G.F., Liss, P., Perna, N.T., Rose, D.J., Mau, B., Zhou, S., Schwartz, D.C., Fetherston, J.D., Lindler, L.E., Brubaker, R.R., Plano, G.V., Straley, S.C., McDonough, K.A., Nilles, M.L., Matson, J.S., Blattner, F.R. and Perry, R.D. (2002) Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184, 4601-4611.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ding, Z. and Christie, P.J. (2003). Agrobacterium tumefaciens twin-arginine-dependent trans-location is important for virulence, flagellation, and chemotaxis but not type IV secretion. J. Bacteriol. 185,760-771.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Fetherston, J.D., Bertolino, V.J. and Perry, R.D. (1999) YbtP and YbtQ: two ABC transporters required for iron uptake in Yersinia pestis. Mol. Microbiol. 32, 289-299.CrossRefPubMedGoogle Scholar
  18. Frithz-Lindsten, E., Holmstrom, A., Jacobsson, L., Soltani, M., Olsson, J., Rosqvist, R. and Forsberg, Å. (1998) Functional conservation of the effector protein translocators PopB/YopB and PopD/YopD of Pseudomonas aeruginosa and Yersinia pseudotuberculo-sis. Mol. Microbiol. 29, 1155-1165.CrossRefPubMedGoogle Scholar
  19. Gohlke, U., Pullan, L., McDevitt, C.A., Porcelli, I., de Leeuw, E., Palmer, T., Saibil, H.R. and Berks, B.C. (2005) The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc. Natl. Acad. Sci. U S A 102, 10482-10486.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Halbig, D., Wiegert, T., Blaudeck, N., Freudl, R. and Sprenger, G.A. (1999) The efficient export of NADP-containing glucose-fructose oxidoreductase to the periplasm of Zymomo-nas 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. Biochem. 263, 543-551.CrossRefPubMedGoogle Scholar
  21. Hatzixanthis, K., Palmer, T. and Sargent, F. (2003) A subset of bacterial inner membrane proteins integrated by the twin-arginine translocase. Mol. Microbiol. 49, 1377-1390.CrossRefPubMedGoogle Scholar
  22. Hinsley, A.P., Stanley, N.R., Palmer, T. and Berks, B.C. (2001) A naturally occurring bacte-rial Tat signal peptide lacking one of the 'invariant' arginine residues of the consensus tar-geting motif. FEBS Lett. 497, 45-49.CrossRefPubMedGoogle Scholar
  23. Hutcheon, G.W. and Bolhuis, A. (2003) The archaeal twin-arginine translocation pathway. Biochem. Soc. Trans. 31, 686-689.CrossRefPubMedGoogle Scholar
  24. Ize, B., Gerard, F., Zhang, M., Chanal, A., Voulhoux, R., Palmer, T., Filloux, A. and Wu, L.F. (2002) In vivo dissection of the Tat translocation pathway in Escherichia coli. J. Mol. Biol. 317, 327-335.CrossRefPubMedGoogle Scholar
  25. Jongbloed, J.D., Martin, U., Antelmann, H., Hecker, M., Tjalsma, H., Venema, G., Bron, S., van Dijl, J.M. and Muller, J. (2000) TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J. Biol. Chem. 275, 41350-41357.CrossRefPubMedGoogle Scholar
  26. Ki, J.J., Kawarasaki, Y., Gam, J., Harvey, B.R., Iverson, B.L. and Georgiou, G. (2004) A periplasmic fluorescent reporter protein and its application in high-throughput membrane protein topology analysis. J. Mol. Biol. 341, 901-909.CrossRefPubMedGoogle Scholar
  27. Lavander, M., Ericsson, S.K., Bröms, J.E. and Forsberg, Å. (2006). The twin arginine translo-cation system is essential for virulence of Yersinia pseudotuberculosis. Infect. Immun. 74,1768-76.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Marcus, E.A., Moshfegh, A.P., Sachs, G. and Scott, D.R. (2005) The periplasmic alpha-carbonic anhydrase activity of Helicobacter pylori is essential for acid acclimation. J. Bac-teriol. 187, 729-738.CrossRefGoogle Scholar
  29. Molik, S., Karnauchov, I., Weidlich, C., Herrmann, R.G. and Klosgen, R.B. (2001) The Ri-eske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evo-lution of protein transport pathways in chloroplasts? J. Biol. Chem. 276, 42761-42766.CrossRefPubMedGoogle Scholar
  30. Oates, J., Mathers, J., Mangels, D., Kuhlbrandt, W., Robinson, C. and Model, K. (2003) Con-sensus structural features of purified bacterial TatABC complexes. J. Mol. Biol. 330, 277-286.CrossRefPubMedGoogle Scholar
  31. Oates, J., Barrett, C.M., Barnett, J.P., Byrne, K.G., Bolhuis, A. and Robinson, C. (2005) The Escherichia coli twin-arginine translocation apparatus incorporates a distinct form of Ta-tABC complex, spectrum of modular TatA complexes and minor TatAB complex. J. Mol. Biol. 346, 295-305. Epub 2004 Dec 2013.CrossRefPubMedGoogle Scholar
  32. Ochsner, U.A., Snyder, A., Vasil, A.I. and 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 A 99, 8312-8317.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Palmer, T. and Berks, B.C. (2003) Moving folded proteins across the bacterial cell membrane. Microbiology 149, 547-556.CrossRefPubMedGoogle Scholar
  34. Palmer, T., Sargent, F. and Berks, B.C. (2005) Export of complex cofactor-containing proteins by the bacterial Tat pathway. Trends Microbiol. 13, 175-180.CrossRefPubMedGoogle Scholar
  35. Porcelli, I., de Leeuw, E., Wallis, R., van den Brink-van der Laan, E., de Kruijff, B., Wallace, B.A., Palmer, T. and Berks, B.C. (2002) Characterization and membrane assembly of the TatA component of the Escherichia coli twin-arginine protein transport system. Biochemistry 41, 13690-13697.Google Scholar
  36. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol. Rev. 57, 50-108.PubMedPubMedCentralGoogle Scholar
  37. Rose, R.W., Bruser, T., Kissinger, J.C. and Pohlschroder, M. (2002) Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine transloca-tion pathway. Mol. Microbiol. 45, 943-950.CrossRefPubMedGoogle Scholar
  38. Rossier, O. and Cianciotto, N.P. (2005) The Legionella pneumophila tatB gene facilitates secretion of phospholipase C, growth under iron-limiting conditions, and intracellular in-fection. Infect. Immun. 73, 2020-2032.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Sargent, F., Bogsch, E.G., Stanley, N.R., Wexler, M., Robinson, C., Berks, B.C. and Palmer, T. (1998) Overlapping functions of components of a bacterial Sec-independent protein export pathway. Embo J. 17, 3640-3650.CrossRefPubMedPubMedCentralGoogle Scholar
  40. Sargent, F., Gohlke, U., De Leeuw, E., Stanley, N.R., Palmer, T., Saibil, H.R. and Berks, B.C. (2001) Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268, 3361-3367.CrossRefPubMedGoogle Scholar
  41. Sargent, F., Berks, B.C. and Palmer, T. (2002) Assembly of membrane-bound respiratory complexes by the Tat protein-transport system. Arch. Microbiol. 178, 77-84.CrossRefPubMedGoogle Scholar
  42. Settles, A.M., Yonetani, A., Baron, A., Bush, D.R., Cline, K. and Martienssen, R. (1997) Sec-independent protein translocation by the maize Hcf106 protein. Science 278, 1467-1470.CrossRefPubMedGoogle Scholar
  43. Settles, A.M. and Martienssen, R. (1998) Old and new pathways of protein export in chloro-plasts and bacteria. Trends Cell Biol. 8, 494-501.CrossRefPubMedGoogle Scholar
  44. Smith, K.S. and Ferry, J.G. (2000) Prokaryotic carbonic anhydrases. FEMS Microbiol. Rev. 24, 335-366.Google Scholar
  45. Weiner, J.H., Bilous, P.T., Shaw, G.M., Lubitz, S.P., Frost, L., Thomas, G.H., Cole, J.A. and Turner, R.J. (1998) A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell 93, 93-101.CrossRefPubMedGoogle Scholar
  46. Wexler, M., Sargent, F., Jack, R.L., Stanley, N.R., Bogsch, E.G., Robinson, C., Berks, B.C. and Palmer, T. (2000) TatD is a cytoplasmic protein with DNase activity. No requirement for TatD family proteins in sec-independent protein export. J. Biol.Chem. 275, 16717-16722.CrossRefPubMedGoogle Scholar
  47. von Heijne, G. (1985) Signal sequences. The limits of variation. J. Mol. Biol. 184, 99-105.CrossRefPubMedGoogle Scholar
  48. Voulhoux, R., Ball, G., Ize, B., Vasil, M.L., Lazdunski, A., Wu, L.F. and Filloux, A. (2001) Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. Embo J. 20, 6735-6741.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Yahr, T.L., Hovey, A.K., Kulich, S.M. and Frank, D.W. (1995) Transcriptional analysis of the Pseudomonas aeruginosa exoenzyme S structural gene. J. Bacteriol. 177, 1169-1178.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Yahr, T.L. and Wickner, W.T. (2001) Functional reconstitution of bacterial Tat translocation in vitro. Embo J. 20, 2472-2479.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2007

Authors and Affiliations

  • Moa Lavander
    • 1
  • Åke Forsberg
    • 2
  • Jeanette E. Bröms
    • 2
  • Solveig K. Ericsson
    • 2
  1. 1.DiseasesSwedish Defence Research AgencySweden
  2. 2.Department of Medical Countermeasures, Division of NBC DefenceSwedish Defence Research AgencySweden

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