Prokaryotic Utilization of the Twin-Arginine Translocation Pathway: a Genomic Survey

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.

[1]  D. Bush,et al.  Sec-independent protein translocation by the maize Hcf106 protein. , 1997, Science.

[2]  Romé Voulhoux,et al.  In vivo dissection of the Tat translocation pathway in Escherichia coli. , 2002, Journal of molecular biology.

[3]  M. Vasil,et al.  Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Jon Beckwith,et al.  Protein Translocation in the Three Domains of Life: Variations on a Theme , 1997, Cell.

[5]  M. Hecker,et al.  TatC Is a Specificity Determinant for Protein Secretion via the Twin-arginine Translocation Pathway* , 2000, The Journal of Biological Chemistry.

[6]  Matthias Müller,et al.  Co-translocation of a Periplasmic Enzyme Complex by a Hitchhiker Mechanism through the Bacterial Tat Pathway* , 1999, The Journal of Biological Chemistry.

[7]  Jessica C Kissinger,et al.  Adaptation of protein secretion to extremely high‐salt conditions by extensive use of the twin‐arginine translocation pathway , 2002, Molecular microbiology.

[8]  G. Voordouw,et al.  Site-directed mutagenesis of the hydrogenase signal peptide consensus box prevents export of a beta-lactamase fusion protein. , 1992, Journal of general microbiology.

[9]  B. Barrell,et al.  Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2) , 2002, Nature.

[10]  B. Berks,et al.  A naturally occurring bacterial Tat signal peptide lacking one of the ‘invariant’ arginine residues of the consensus targeting motif , 2001, FEBS letters.

[11]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[12]  S. Brunak,et al.  SHORT COMMUNICATION Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites , 1997 .

[13]  Erik L. L. Sonnhammer,et al.  A Hidden Markov Model for Predicting Transmembrane Helices in Protein Sequences , 1998, ISMB.

[14]  B. Berks,et al.  Escherichia coli Strains Blocked in Tat-Dependent Protein Export Exhibit Pleiotropic Defects in the Cell Envelope , 2001, Journal of bacteriology.

[15]  Koreaki Ito,et al.  The Sec protein-translocation pathway. , 2001, Trends in microbiology.

[16]  B. Berks,et al.  The Twin Arginine Consensus Motif of Tat Signal Peptides Is Involved in Sec-independent Protein Targeting in Escherichia coli * , 2000, The Journal of Biological Chemistry.

[17]  M. Saier,et al.  Sequence and phylogenetic analyses of the twin-arginine targeting (Tat) protein export system , 2002, Archives of Microbiology.

[18]  G. Giordano,et al.  A novel Sec‐independent periplasmic protein translocation pathway in Escherichia coli , 1998, The EMBO journal.

[19]  B. Berks.  A common export pathway for proteins binding complex redox cofactors? , 1996, Molecular microbiology.

[20]  R. Daniel,et al.  Export of active green fluorescent protein to the periplasm by the twin‐arginine translocase (Tat) pathway in Escherichia coli , 2001, Molecular microbiology.

[21]  B. Berks,et al.  Overlapping functions of components of a bacterial Sec‐independent protein export pathway , 1998, The EMBO journal.

[22]  G. von Heijne.  The signal peptide. , 1990, The Journal of membrane biology.

[23]  G. Vonheijne.  The signal peptide. , 1990 .

[24]  A. Barkan,et al.  Two nuclear mutations disrupt distinct pathways for targeting proteins to the chloroplast thylakoid. , 1995, The EMBO journal.

[25]  Long-Fei Wu,et al.  Involvement of the twin‐arginine translocation system in protein secretion via the type II pathway , 2001, The EMBO journal.

[26]  Zoya Ignatova,et al.  Unusual signal peptide directs penicillin amidase from Escherichia coli to the Tat translocation machinery. , 2002, Biochemical and biophysical research communications.

[27]  J. Weiner,et al.  A Novel and Ubiquitous System for Membrane Targeting and Secretion of Cofactor-Containing Proteins , 1998, Cell.

[28]  B. Berks,et al.  Sec-independent Protein Translocation in Escherichia coli , 1999, The Journal of Biological Chemistry.

[29]  B. Berks,et al.  An Essential Component of a Novel Bacterial Protein Export System with Homologues in Plastids and Mitochondria* , 1998, The Journal of Biological Chemistry.

[30]  George Georgiou,et al.  Genetic Analysis of the Twin Arginine Translocator Secretion Pathway in Bacteria* , 2002, The Journal of Biological Chemistry.

[31]  G. Fichant,et al.  Bacterial twin-arginine signal peptide-dependent protein translocation pathway: evolution and mechanism. , 2000, Journal of molecular microbiology and biotechnology.

[32]  T. Rapoport,et al.  Protein Translocation: Tunnel Vision , 1998, Cell.

[33]  R. Herrmann,et al.  A new type of signal peptide: central role of a twin‐arginine motif in transfer signals for the delta pH‐dependent thylakoidal protein translocase. , 1995, The EMBO journal.

[34]  A. Driessen,et al.  Protein Targeting to the Bacterial Cytoplasmic Membrane , 1999, Microbiology and Molecular Biology Reviews.

[35]  A. Bolhuis,et al.  Protein targeting by the twin-arginine translocation pathway , 2001, Nature Reviews Molecular Cell Biology.

[36]  K. Cline,et al.  Protein-specific energy requirements for protein transport across or into thylakoid membranes. Two lumenal proteins are transported in the absence of ATP. , 1992, The Journal of biological chemistry.

[37]  Frank Sargent,et al.  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 , 2001, Archives of Microbiology.

[38]  C. Robinson,et al.  The Sec-independent Twin-arginine Translocation System Can Transport Both Tightly Folded and Malfolded Proteins across the Thylakoid Membrane* , 1998, The Journal of Biological Chemistry.