You have full text access to this OnlineOpen article

Interconvertibility of lipid- and translocon-bound forms of the bacterial Tat precursor pre-SufI

  1. Umesh K. Bageshwar,
  2. Neal Whitaker,
  3. Fu-Cheng Liang,
  4. Siegfried M. Musser*

Article first published online: 2 SEP 2009

DOI: 10.1111/j.1365-2958.2009.06862.x

Issue

Molecular Microbiology

Molecular Microbiology

Volume 74, Issue 1, pages 209–226, October 2009

Additional Information

How to Cite

Bageshwar, U. K., Whitaker, N., Liang, F.-C. and Musser, S. M. (2009), Interconvertibility of lipid- and translocon-bound forms of the bacterial Tat precursor pre-SufI. Molecular Microbiology, 74: 209–226. doi: 10.1111/j.1365-2958.2009.06862.x

Author Information

  1. Department of Molecular and Cellular Medicine, College of Medicine, Texas A&M Health Science Center, College Station, TX 77843, USA.

* *E-mail smusser@tamu.edu; Tel. (+1) 979 862 4128; Fax (+1) 979 847 9481.

Publication History

  1. Issue published online: 24 SEP 2009
  2. Article first published online: 2 SEP 2009
  3. Accepted 19 August, 2009.

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (1724K)

References

  • 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.
  • Bageshwar, U.K., And Musser, S.M. (2007) Two electrical potential-dependent steps are required for transport by the Escherichia coli Tat machinery. J Cell Biol 179: 87–99.
  • Barrett, C.M., Ray, N., Thomas, J.D., Robinson, C., and Bolhuis, A. (2003) Quantitative export of a reporter protein, GFP, by the twin-arginine translocation pathway in Escherichia coli. Biochem Biophys Res Commun 304: 279–284.
  • Beck, D.A., Bennion, B.J., Alonso, D.O., and Daggett, V. (2007) Simulations of macromolecules in protective and denaturing osmolytes: properties of mixed solvent systems and their effects on water and protein structure and dynamics. Methods Enzymol 428: 373–396.
  • Bendtsen, J.D., Nielsen, H., Widdick, D., Palmer, T., and Brunak, S. (2005) Prediction of twin-arginine signal peptides. BMC Bioinformatics 6: 167.
  • Berks, B.C. (1996) A common export pathway for proteins binding complex redox cofactors? Mol Microbiol 22: 393–404.
  • Berks, B.C., Palmer, T., and Sargent, F. (2003) The Tat protein translocation pathway and its role in microbial physiology. Adv Microbiol Physiol 47: 187–254.
  • Berks, B.C., Palmer, T., and Sargent, F. (2005) Protein targeting by the bacterial twin-arginine translocation (Tat) pathway. Curr Opin Microbiol 8: 174–181.
  • Bolhuis, A., Mathers, J.E., Thomas, J.D., Barrett, C.M.L., and Robinson, C. (2001) TatB and TatC form a functional and structural unit of the twin-arginine translocase from Escherichia coli. J Biol Chem 276: 20213–20219.
  • Brüser, T., and Sanders, C. (2003) An alternative model of the twin arginine translocation system. Microbiol Res 158: 7–17.
  • Brüser, T., Yano, T., Brune, D.C., and Daldal, F. (2003) Membrane targeting of a folded and cofactor-containing protein. Eur J Biochem 270: 1211–1221.
  • Casadaban, M.J., and Cohen, S.N. (1979) Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc Natl Acad Sci USA 76: 4530–4533.
  • Chaddock, A.M., Mant, A., Karnauchov, I., Brink, S., Herrmann, R.G., Klosgen, R.B., and Robinson, C. (1995) A new type of signal peptide: central role of a twin-arginine motif in transfer signals for the delta pH-dependent thylakoidal protein translocase. EMBO J 14: 2715–2722.
  • Cline, K., and Mori, H. (2001) Thylakoid ΔpH-dependent precursor proteins bind to a cpTatC-Hcf106 complex before Tha4-dependent transport. J Cell Biol 154: 719–729.
  • Cristóbal, S., De Gier, J.W., Nielsen, H., and Von Heijne, G. (1999) Competition between Sec- and TAT-dependent protein translocation in Escherichia coli. EMBO J 18: 2982–2990.
  • Dabney-Smith, C., Mori, H., and Cline, K. (2006) Oligomers of Tha4 organize at the thylakoid Tat translocase during protein transport. J Biol Chem 281: 5476–5483.
  • De Leeuw, E., Porcelli, I., Sargent, F., Palmer, T., and Berks, B.C. (2001) Membrane interactions and self association of the TatA and TatB components of the twin-arginine translocation pathway. FEBS Lett 506: 143–148.
  • DeLisa, M.P., Lee, P., Palmer, T., and Georgiou, G. (2004) Phage shock protein PspA of Escherichia coli relieves saturation of protein export via the Tat pathway. J Bacteriol 186: 366–373.
  • Driessen, A.J., and Nouwen, N. (2008) Protein translocation across the bacterial cytoplasmic membrane. Annu Rev Biochem 77: 643–667.
  • Dubini, A., and Sargent, F. (2003) Assembly of Tat-dependent [NiFe] hydrogenases: identification of precursor-binding accessory proteins. FEBS Lett 549: 141–146.
  • Gérard, F., and Cline, K. (2006) Efficient twin arginine translocation (Tat) pathway transport of a precursor protein covalently anchored to its initial cpTatC binding site. J Biol Chem 281: 6130–6135.
  • Gérard, F., and Cline, K. (2007) The thylakoid proton gradient promotes an advanced stage of signal peptide binding deep within the Tat pathway receptor complex. J Biol Chem 282: 5263–5272.
  • Gohlke, U., Pullan, L., McDevitt, C.A., Porcelli, I., De Leeuw, E., Palmer, T., et al. (2005) The TatA component of the twin-arginine protein transport system forms channel complexes of variable diameter. Proc Natl Acad Sci USA 102: 10482–10486.
  • Graubner, W., Schierhorn, A., and Bruser, T. (2007) DnaK plays a pivotal role in Tat targeting of CueO and functions beside SlyD as a general Tat signal binding chaperone. J Biol Chem 282: 7116–7124.
  • Harlow, E., and Lane, D. (1999) Using Antibodies: A Laboratory Manual. New York: Cold Spring Harbor Laboratory Press.
  • Hinsley, A.P., Stanley, N.R., Palmer, T., and Berks, B.C. (2001) A naturally occurring bacterial Tat signal peptide lacking one of the ‘invariant’ arginine residues of the consensus targeting motif. FEBS Lett 497: 45–49.
  • Holzapfel, E., Eisner, G., Alami, M., Barrett, C.M., Buchanan, G., Luke, I., et al. (2007) The entire N-terminal half of TatC is involved in twin-arginine precursor binding. Biochemistry 46: 2892–2898.
  • Holzapfel, E., Moser, M., Schiltz, E., Ueda, T., Betton, J.-M., and Muller, M. (2009) Twin-arginine-dependent translocation of SufI in the absence of cytosolic helper proteins. Biochemistry 48: 5096–5105.
  • Hou, B., Frielingsdorf, S., and Klösgen, R.B. (2006) Unassisted membrane insertion as the initial step in ΔpH/Tat-dependent protein transport. J Mol Biol 355: 957–967.
  • Hua, L., Zhou, R., Thirumalai, D., and Berne, B.J. (2008) Urea denaturation by stronger dispersion interactions with proteins than water implies a 2-stage unfolding. Proc Natl Acad Sci USA 105: 16928–16933.
  • Jack, R.L., Buchanan, G., Dubini, A., Hatzixanthis, K., Palmer, T., and Sargent, F. (2004) Coordinating assembly and export of complex bacterial proteins. EMBO J 23: 3962–3972.
  • Kyte, J., and Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157: 105–132.
  • Li, H., Faury, D., and Morosoli, R. (2006) Impact of amino acid changes in the signal peptide on the secretion of the Tat-dependent xylanase C from Streptomyces lividans. FEMS Microbiol Lett 255: 268–274.
  • Liang, F.-C., Bageshwar, U.K., and Musser, S.M. (2009) Bacterial Sec protein transport is rate-limited by precursor length: a single turnover study. Mol Biol Cell 20: 4256–4266.
  • Lorence, R.M., Carter, K., Gennis, R.B., Matsushita, K., and Kaback, H.R. (1988) Trypsin proteolysis of the cytochrome d complex of Escherichia coli selectively inhibits ubiquinol oxidase activity while not affecting N,N,N′,N′-tetramethyl-p-phenylenediamine oxidase activity. J Biol Chem 263: 5271–5276.
  • McDevitt, C.A., Buchanan, G., Sargent, F., Palmer, T., and Berks, B.C. (2006) Subunit composition and in vivo substrate-binding characteristics of Escherichia coli Tat protein complexes expressed at native levels. FEBS J 273: 5656–5668.
  • Maillard, J., Spronk, C.A., Buchanan, G., Lyall, V., Richardson, D.J., Palmer, T., et al. (2007) Structural diversity in twin-arginine signal peptide-binding proteins. Proc Natl Acad Sci USA 104: 15641–15646.
  • Matos, C.F., Robinson, C., and Di Cola, A. (2008) The Tat system proofreads FeS protein substrates and directly initiates the disposal of rejected molecules. EMBO J 27: 2055–2063.
  • Molik, S., Karnauchov, I., Weidlich, C., Herrmann, R.G., and Klosgen, R.B. (2001) The Rieske Fe/S protein of the cytochrome b6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? J Biol Chem 276: 42761–42766.
  • Musser, S.M., and Theg, S.M. (2000) Characterization of the early steps of OE17 precursor transport by the thylakoid ΔpH/Tat machinery. Eur J Biochem 267: 2588–2598.
  • Natale, P., Brüser, T., and Driessen, A.J. (2008) Sec- and Tat-mediated protein secretion across the bacterial cytoplasmic membrane – distinct translocases and mechanisms. Biochim Biophys Acta 1778: 1735–1756.
  • Oresnik, I.J., Ladner, C.L., and Turner, R.J. (2001) Identification of a twin-arginine leader-binding protein. Mol Microbiol 40: 323–331.
  • Pace, C.N. (1995) Evaluating contribution of hydrogen bonding and hydrophobic bonding to protein folding. Methods Enzymol 259: 538–554.
  • Panahandeh, S., Maurer, C., Moser, M., Delisa, M.P., and Müller, M. (2008) Following the path of a twin-arginine precursor along the TatABC translocase of Escherichia coli. J Biol Chem 283: 33267–33275.
  • Papish, A.L., Ladner, C.L., and Turner, R.J. (2003) The twin-arginine leader-binding protein, DmsD, interacts with the TatB and TatC subunits of the Escherichia coli twin-arginine translocase. J Biol Chem 278: 32501–32506.
  • Radzicka, A., Pedersen, L., and Wolfenden, R. (1988) Influences of solvent water on protein folding: free energies of solvation of cis and trans peptides are nearly identical. Biochemistry 27: 4538–4541.
  • Rusch, S.L., and Kendall, D.A. (2007) Interactions that drive Sec-dependent bacterial protein transport. Biochemistry 46: 9665–9673.
  • Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Press.
  • Santini, C.L., Bernadac, A., Zhang, M., Chanal, A., Ize, B., Blanco, C., and 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 Chem 276: 8159–8164.
  • Sargent, F. (2007) The twin-arginine transport system: moving folded proteins across membranes. Biochem Soc Trans 35: 835–847.
  • Sargent, F., Stanley, N.R., Berks, B.C., and Palmer, T. (1999) Sec-independent protein translocation in Escherichia coli: a distinct and pivotal role for the TatB protein. J Biol Chem 274: 36073–36082.
  • Shanmugham, A., Wong Fong Sang, H.W., Bollen, Y.J., and Lill, H. (2006) Membrane binding of twin arginine preproteins as an early step in translocation. Biochemistry 45: 2243–2249.
  • Stanley, N.R., Palmer, T., and 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 Chem 275: 11591–11596.
  • Studier, F.W., Rosenberg, A.H., Dunn, J.J., and Dubendorff, J.W. (1990) Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 185: 60–89.
  • Stumpe, M.C., and Grubmüller, H. (2007) Interaction of urea with amino acids: implications for urea-induced protein denaturation. J Am Chem Soc 129: 16126–16131.
  • Stumpe, M.C., and Grubmüller, H. (2008) Polar or apolar – the role of polarity for urea-induced protein denaturation. PLoS Comput Biol 4: e1000221.
  • Tarry, M.J., Schäfer, E., Chen, S., Buchanan, G., Greene, N.P., and Lea, S.M., et al. (2009) Structural analysis of substrate binding by the TatBC component of the twin-arginine protein transport system. Proc Natl Acad Sci USA 106: 13284–13289.
  • Thomas, J.D., Daniel, R.A., Errington, J., and Robinson, C. (2001) Export of active green fluorescent protein to the periplasm by the twin-arginine translocase (Tat) pathway in Escherichia coli. Mol Microbiol 39: 47–53.
  • Wexler, M., Sargent, F., Jack, R.L., Stanley, N.R., Bogsch, E.G., Robinson, C., et al. (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.
  • Wimley, W.C., and White, S.H. (1996) Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 3: 842–848.
  • Yahr, T.L., and Wickner, W.T. (2001) Functional reconstitution of bacterial Tat translocation in vitro. EMBO J 20: 2472–2479.
  • Yanisch-Perron, C., Vieira, J., and Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103–119.
View Full Article with Supporting Information (HTML) Get PDF (1724K)