Abstract
ABSTRACT The twin-arginine translocation (Tat) pathway, which has been identified in plant chloroplasts and prokaryotes, allows for the secretion of folded proteins. However, the extent to which this pathway is used among the prokaryotes is not known. By using a genomic approach, a comprehensive list of putative Tat substrates for 84 diverse prokaryotes was established. Strikingly, the results indicate that the Tat pathway is utilized to highly varying extents. Furthermore, while many prokaryotes use this pathway predominantly for the secretion of redox proteins, analyses of the predicted substrates suggest that certain bacteria and archaea secrete mainly nonredox proteins via the Tat pathway. While no correlation was observed between the number of Tat machinery components encoded by an organism and the number of predicted Tat substrates, it was noted that the composition of this machinery was specific to phylogenetic taxa.
References
37
Referenced
221
10.1093/nar/25.17.3389
10.1038/417141a
-
Berks, B. C. 1996. A common export pathway for proteins binding complex redox cofactors? Mol. Microbiol.22:393-404.
(
10.1046/j.1365-2958.1996.00114.x
) / Mol. Microbiol. (1996) -
Bogsch, E. G., F. Sargent, N. R. Stanley, B. C. Berks, C. Robinson, and T. Palmer. 1998. An essential component of a novel bacterial protein export system with homologues in plastid and mitochondria. J. Biol. Chem.273:18003-18006.
(
10.1074/jbc.273.29.18003
) / J. Biol. Chem. (1998) -
Buchanan, G., F. Sargent, B. C. Berks, and T. Palmer. 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. Microbiol.177:107-112.
(
10.1007/s00203-001-0366-2
) / Arch. Microbiol. (2001) -
Chaddock, A. M., A. Mant, I. Karnauchov, S. Brink, R. G. Herrmann, R. B. Klosgen, and C. Robinson. 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.
(
10.1002/j.1460-2075.1995.tb07272.x
) / EMBO J. (1995) -
Cline, K., W. F. Ettinger, and S. M. Theg. 1992. Protein-specific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP. J. Biol. Chem.267:2688-2696.
(
10.1016/S0021-9258(18)45935-2
) / J. Biol. Chem. (1992) -
DeLisa, M. P., P. Samuelson, T. Palmer, and G. Georgiou. 2002. Genetic analysis of the twin arginine translocator secretion pathway in bacteria. J. Biol. Chem.277:29825-29831.
(
10.1074/jbc.M201956200
) / J. Biol. Chem. (2002) 10.1128/MMBR.63.1.161-173.1999
-
Hinsley, A. P., N. R. Stanley, T. Palmer, and B. C. Berks. 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.
(
10.1016/S0014-5793(01)02428-0
) / FEBS Lett. (2001) -
Hynds, P. J., D. Robinson, and C. Robinson. 1998. The sec-independent twin-arginine translocation system can transport both tightly folded and malfolded proteins across the thylakoid membrane. J. Biol. Chem.273:34868-34874.
(
10.1074/jbc.273.52.34868
) / J. Biol. Chem. (1998) -
Ignatova, Z., C. Hornle, A. Nurk, and V. Kasche. 2002. Unusual signal peptide directs penicillin amidase from Escherichia coli to the Tat translocation machinery. Biochem. Biophys. Res. Commun.291:146-149.
(
10.1006/bbrc.2002.6420
) / Biochem. Biophys. Res. Commun. (2002) -
Ize, B., F. Gerard, M. Zhang, A. Chanal, R. Voulhoux, T. Palmer, A. Filloux, and L. F. Wu. 2002. In vivo dissection of the Tat translocation pathway in Escherichia coli. J. Mol. Biol.317:327-335.
(
10.1006/jmbi.2002.5431
) / J. Mol. Biol. (2002) -
Jongbloed, J. D., U. Martin, H. Antelmann, M. Hecker, H. Tjalsma, G. Venema, S. Bron, J. M. van Dijl, and J. Muller. 2000. TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J. Biol. Chem.275:41350-41357.
(
10.1074/jbc.M004887200
) / J. Biol. Chem. (2000) -
Matlack, K., W. Mothes, and T. Rapoport. 1998. Protein translocation: tunnel vision. Cell92:381-390.
(
10.1016/S0092-8674(00)80930-7
) / Cell (1998) -
Mori, H., and K. Ito. 2001. The Sec protein-translocation pathway. Trends Microbiol.9:494-500.
(
10.1016/S0966-842X(01)02174-6
) / Trends Microbiol. (2001) 10.1093/protein/10.1.1
-
Niviere, V., S. L. Wong, and G. Voordouw. 1992. Site-directed mutagenesis of the hydrogenase signal peptide consensus box prevents export of a beta-lactamase fusion protein. J. Gen. Microbiol.138:2173-2183.
(
10.1099/00221287-138-10-2173
) / J. Gen. Microbiol. (1992) -
Ochsner, U. A., A. Snyder, A. I. Vasil, and M. L. Vasil. 2002. Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc. Natl. Acad. Sci. USA99:8312-8317.
(
10.1073/pnas.082238299
) / Proc. Natl. Acad. Sci. USA (2002) -
Pohlschroder, M., W. A. Prinz, E. Hartmann, and J. Beckwith. 1997. Protein translocation in the three domains of life: variations on a theme. Cell91:563-566.
(
10.1016/S0092-8674(00)80443-2
) / Cell (1997) -
Robinson, C., and A. Bolhuis. 2001. Protein targeting by the twin-arginine translocation pathway. Nat. Rev. Mol. Cell Biol.2:350-356.
(
10.1038/35073038
) / Nat. Rev. Mol. Cell Biol. (2001) -
Rodrigue, A., A. Chanal, K. Beck, M. Muller, and L. F. Wu. 1999. Co-translocation of a periplasmic enzyme complex by a hitchhiker mechanism through the bacterial tat pathway. J. Biol. Chem.274:13223-13228.
(
10.1074/jbc.274.19.13223
) / J. Biol. Chem. (1999) -
Rose, R. W., T. Bruser, J. C. Kissinger, and M. Pohlschroder. 2002. Adaptation of protein secretion to extremely high-salt conditions by extensive use of the twin-arginine translocation pathway. Mol. Microbiol.45:943-950.
(
10.1046/j.1365-2958.2002.03090.x
) / Mol. Microbiol. (2002) -
Santini, C. L., B. Ize, A. Chanal, M. Muller, G. Giordano, and L. F. Wu. 1998. A novel sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J.17:101-112.
(
10.1093/emboj/17.1.101
) / EMBO J. (1998) -
Sargent, F., E. G. Bogsch, N. R. Stanley, M. Wexler, C. Robinson, B. C. Berks, and T. Palmer. 1998. Overlapping functions of components of a bacterial Sec-independent protein export pathway. EMBO J.17:3640-3650.
(
10.1093/emboj/17.13.3640
) / EMBO J. (1998) -
Sargent, F., N. R. Stanley, B. C. Berks, and T. Palmer. 1999. Sec-independent protein translocation in Escherichia coli. A distinct and pivotal role for the TatB protein. J. Biol. Chem.274:36073-36082.
(
10.1074/jbc.274.51.36073
) / J. Biol. Chem. (1999) -
Settles, A. M., A. Yonetani, A. Baron, D. R. Bush, K. Cline, and R. Martienssen. 1997. Sec-independent protein translocation by the maize Hcf106 protein. Science278:1467-1470.
(
10.1126/science.278.5342.1467
) / Science (1997) - Sonnhammer, E. L., G. von Heijne, and A. Krogh. 1998. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol.6:175-182. / Proc. Int. Conf. Intell. Syst. Mol. Biol. (1998)
10.1128/JB.183.1.139-144.2001
-
Stanley, N. R., T. Palmer, and B. C. Berks. 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.
(
10.1074/jbc.275.16.11591
) / J. Biol. Chem. (2000) -
Thomas, J. D., R. A. Daniel, J. Errington, and C. Robinson. 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.
(
10.1046/j.1365-2958.2001.02253.x
) / Mol. Microbiol. (2001) -
Voelker, R., and A. Barkan. 1995. Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. EMBO J.14:3905-3914.
(
10.1002/j.1460-2075.1995.tb00062.x
) / EMBO J. (1995) -
von Heijne, G. 1990. The signal peptide. J. Membr. Biol.115:195-201.
(
10.1007/BF01868635
) / J. Membr. Biol. (1990) -
Voulhoux, R., G. Ball, B. Ize, M. L. Vasil, A. Lazdunski, L. F. Wu, and A. Filloux. 2001. Involvement of the twin-arginine translocation system in protein secretion via the type II pathway. EMBO J.20:6735-6741.
(
10.1093/emboj/20.23.6735
) / EMBO J. (2001) -
Weiner, J. H., P. T. Bilous, G. M. Shaw, S. P. Lubitz, L. Frost, G. H. Thomas, J. A. Cole, and R. J. Turner. 1998. A novel and ubiquitous system for membrane targeting and secretion of cofactor-containing proteins. Cell93:93-101.
(
10.1016/S0092-8674(00)81149-6
) / Cell (1998) - Wu, L. F., B. Ize, A. Chanal, Y. Quentin, and G. Fichant. 2000. Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. J. Mol. Microbiol. Biotechnol.2:179-189. / J. Mol. Microbiol. Biotechnol. (2000)
-
Yen, M. R., Y. H. Tseng, E. H. Nguyen, L. F. Wu, and M. H. Saier, Jr. 2002. Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system. Arch. Microbiol.177:441-450.
(
10.1007/s00203-002-0408-4
) / Arch. Microbiol. (2002)
Dates
Type | When |
---|---|
Created | 22 years, 7 months ago (Jan. 31, 2003, 3:03 p.m.) |
Deposited | 4 years, 1 month ago (July 29, 2021, 2:13 p.m.) |
Indexed | 1 month ago (Aug. 2, 2025, 12:57 a.m.) |
Issued | 22 years, 6 months ago (Feb. 15, 2003) |
Published | 22 years, 6 months ago (Feb. 15, 2003) |
Published Print | 22 years, 6 months ago (Feb. 15, 2003) |
@article{Dilks_2003, title={Prokaryotic Utilization of the Twin-Arginine Translocation Pathway: a Genomic Survey}, volume={185}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.185.4.1478-1483.2003}, DOI={10.1128/jb.185.4.1478-1483.2003}, number={4}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Dilks, Kieran and Rose, R. Wesley and Hartmann, Enno and Pohlschröder, Mechthild}, year={2003}, month=feb, pages={1478–1483} }