2.A.64 The Twin Arginine Targeting (Tat) Family

The TatABCE system of E. coli has been both sequenced and functionally characterized (Berks, 1996; Berks et al., 2000a,b). This system forms a large (~600 kDa) complex which interacts with fully folded redox proteins that have an N-terminal S/TRRXFLK 'twin arginine' leader motif (Sargent et al., 2001). It translocates several redox enzymes to the E. coli periplasm including nitrate reductase (NapA) and trimethylamine N-oxide reductase (TorA) which have this leader motif (Bogsch et al., 1998; Santini et al., 1998; Sargent et al., 1998). Hydrogenases, formate dehydrogenases and several non-redox proteins (about two dozen in E. coli), including virulence factors, periplasmic binding proteins, and enzymes involved in envelope biogenesis, have the 'twin R' motif and probably use this pathway. Among these substrate enzyme complexes are several that contain integral membrane proteins (Sargent et al., 2002). These proteins associate with their cofactors in the cell cytoplasm before translocation. TatABCE is also required for the assembly of the E. coli dimethyl sulfoxide reductase (DmsABC) (Weiner et al., 1998; Sambasivarao et al., 2001). The Tat system functions independently of other types of protein secretory systems present in E. coli. However, Tat signal sequences exhibit overlap with Sec signal sequences and can direct proteins to both secretory systems (Tullman-Ercek et al., 2007; Kreutzenbeck et al., 2007). One report suggests that Tat systems can transport small unstructured hydrophilic proteins although hydrophobic patches can abort transport at a late stage (Richter et al., 2007). Fan et al. (2010) have reputed that one signal is sufficient for the stepwise transport of two distinct passenger proteins across the thylakoid membrane.  The 2012 view of how the Tat system works is provided in (Palmer and Berks 2012). The pore-forming part of TatA has been resolved by NMR(Walther et al. 2010).  TatC helix 5 and the TatB transmembrane helix interact (Kneuper et al. 2012) and cooperate to produce recognition of Tat signal peptides in E. coli (Lausberg et al. 2012).  Transmembrane insertion of Tat peptides is driven by TatC and regulated by TatB (Fröbel et al. 2012).  In the TatBC receptor complex, the transmembrane helix of each TatB is sandwiched between two TatCs, with one of the inter-subunit interfaces incorporating a functionally important cluster of interacting polar residues. TatA also associates with TatC at the polar cluster site (Alcock et al. 2016).

The TatA, TatB, TatC and TatE proteins have 1, 1, 6 and 1 putative transmembrane α-helical spanners (TMSs), respectively (sizes of 98, 171, 258 and 67 amino acyl residues, respectively) (Punginelli et al., 2007). TatA, TatB and TatE are homologous, and TatA and TatE, which are more similar to each other than they are to TatB, can partially substitute for each other and form heterooligomers (Eimer et al. 2015).  Both TatA and TatB have the N- out and C- in orientation (Koch et al. 2012). They can be mutationally modified so only one of these proteins is required (Barrett et al., 2007). The transmembrane and amphipathic helical regions of TatA, B and E are critical for function, but their C-terminal domains are not (Lee et al., 2002). Chan et al. (2007) have reported that the N-terminus of TatA is located in the cytoplasm rather than the periplasm. The C-terminus might have a dual topology; its orientation in the membrane could be dependent on the membrane potential. Thus, two architectures of TatA may exist in the membrane: one with a single transmembrane helix and the other with two transmembrane helices. The double transmembrane helix topology might be the building block for the translocation channel. However this suggestion was not supported by more recent work (Koch et al. 2012).  Multimeric TatA may form an expandable protein-conducting channel (Lange et al., 2007 ). The NMR solution structure of TatA has been published (Hu et al., 2010). Structural and biophysical studies of the amphipathic α-helical region of TatA from E. coli have been conducted (Chan et al., 2011).  TatB functions as an oligomeric binding site for folded Tat precursor proteins (Maurer et al. 2010). 

For the Tat system of E. coli, like TatB, but different from TatA, TatE contacts a Tat signal peptide independently of the proton-motive force and restricts the premature processing of a Tat signal peptide. TatE embarks at the transmembrane helix five of TatC where it becomes so closely spaced to TatB that both proteins can be covalently linked by a zero-space cross-linker. This suggests that in addition to TatB and TatC, TatE is a functionally distinct component of the Tat substrate receptor complex (Eimer et al. 2018).

TatC is required for interaction of TatA with TatB (Bolhuis et al., 2001) and has 6 established TMSs with both the N- and C-termini in the cytoplasm (Drew et al., 2002). Interaction and assembly of the substrate protein with the Tat complex appears to occur in several steps (Alami et al., 2003). First, the twin arginine precursor associates with TatC. Second, TatB associates with TatC. Third, TatA association occurs only in the presence of a transmembrane pH gradient. The TatA/B protein-translocating complex channel, of variable size, accommodates and transports the substrate protein complex (Dabney-Smith, 2006; Gerard and Cline, 2006; Gohlke et al., 2005; Hicks et al., 2005). TatB may mediate transfer of the folded substrate from TatC to the Tat pore (Alami et al., 2003). TatC may be peripheral to the TatA/B/C channel which accomodates proteins via the hydrophilic lining of amphipathic α-helices (Greene et al., 2007). TatB and TatC both recognize the twin arginine signal sequence (Strauch and Georgiou, 2007), and TatB thus forms an oligomeric binding site that transiently accomodates folded Tat precursors (Maurer et al., 2010). A TatC dimer is probably at the core of the Tat complex (Maldonado et al., 2011).

Gram-negative bacteria with fully sequenced genomes exhibit only a single TatC homologue, but many Gram-positive bacteria and archaea encode two (Yen et al., 2002). Gram-positive bacteria such as Bacillus subtilis have two independently functioning systems (TatAyCy and TatAdCd in B. subtilis). Expression of the bifunctional B. subtilis TatAd protein in E. coli revealed distinct TatA/B-family and TatB-specific domains (Barnett et al., 2011). Plants have both mitochondrial and chloroplast homologues; for example, Arabidopsis thaliana has one chloroplast TatC homologue and two TatA homologues as well as two putative mitochondrial TatC homologues. These proteins are not found in yeast and animals. A few bacteria (i.e., Rickettsia prowazekii) have only one TatA homologue, but most have two, and several have three (α-proteobacteria and Bacillus subtilis). There are usually two sequence dissimilar paralogues (e.g., TatA and TatB in E. coli) and sometimes one sequence similar paralogue (e.g., TatE) (Yen et al., 2002).

The energetics of the chloroplast Tat system (Alder and Theg, 2003; Berks et al., 2005; Theg et al., 2005) suggest a protein:H+ antiport mechanism with about 100,000 H+ released per transported protein (equivalent to about 104 ATP). The Tat pathway may use about 3% of the total chloroplast energy yield. In chloroplasts, cptatC and Hcf106 form a signal peptide precursor-bound receptor complex which assembles the oligomeric Tha4 translocation pore (Dabney-Smith et al., 2006; Gérard and Cline, 2006). A 'trap door' mechanism was proposed in which oligomers of Tha4 amphipathic helices fold into the membrane to allow form-fitting passage of the substrate precursor protein (Dabney-Smith et al., 2006). After translocation, the complex dissociates (Gérard and Cline, 2006). Tha4 oligomers may dock with a precursor-receptor complex and undergo a conformational switch that results in activation for protein transport. This possibly involves accretion of additional Tha4 subunits into a larger transport-active homo-oligomer (Dabney-Smith and Cline, 2009). Multiple precursor proteins bound to a single receptor complex can be transported together (Ma and Cline, 2010).

Three components are required for Tat transport, cpTatC, Hcf106, and Tha4, in thylakoids (the orthologous TatC, TatB, and TatA, respectively, in bacteria). The thylakoid Tat system has been experimentally staged into several steps. (1) The precursor protein binds to a cpTatC-Hcf106 receptor complex, (2) a Tha4 oligomer assembles with the precursor-receptor complex to form the putative translocase, (3) and the precursor is transported into the lumen. After transport, Tha4 dissociates from the receptor complex, resetting the system for another round of transport (Gérard and Cline, 2007). Tha4 has been shown to undergo conformational changes that accompany protein transport (Aldridge et al. 2012).

A genomic survey indicates that the TAT pathway is utilized to varying extents depending on the bacterium, from 0 to 20% of the total secreted proteins (Dilks et al., 2003). While many prokaryotes use it primarily for the secretion of redox protein complexes, some Gram-positive and Gram-negative bacteria as well as archaea, use it to export non-redox proteins. The composition of the TAT protein complex does not correlate with numbers of substrates but does with organismal phylogeny (Dilks et al., 2003). One report suggests that the TAT pathway can export outer membrane proteins without a cleavable signal sequence (Ferrandez and Condemine, 2008). Streptomyces species have TatA, B and C (Yen et al., 2002) and translocate large numbers of lipoproteins out via the Tat pathway. Lipoprotein biogenesis is essential in S. coelicolor (Thompson et al., 2010).  Tight accommodation of the folded mature region of a substrate protein by TatB contributes to the productive binding of Tat substrates to TatBC (Ulfig and Freudl 2018).

TatC has been shown to serve as a specificity determinant for protein secretion via the Tat system (Jongbloed et al., 2000). However, other proteins may play a role in recognition of the 'twin arginine' motif (Oresnik et al., 2001). For example, DmsD is a Tat leader binding protein that interacts with TatB and TatC (Papish et al., 2003). The energy-coupling mechanism for transport involves the pmf in both chloroplasts and E. coli (Dalbey and Robinson, 1999; Settles et al., 1997; 1998). The E. coli TatA may be capable of flipping orientation in the membrane so that its C-terminus is either in the cytoplasm or in the periplasm (Gouffi et al., 2004), but the physiological significance of this observation is not known.

The heteromultimeric TatAd/TatCd of B. subtilis has been studied with respect to the functions of its two subunits (Schreiber et al., 2006). TatAd localizes to the cytosol or membrane. Soluble TatA can bind to the twin arg signal peptide of pre-PhoD prior to membrane integration. It recruits the substrate protein to the membrane by interaction with TatC. TatC (1) facilitates the membrane association of TatA and (2) stabilizes it (Schreiber et al., 2006). B. subtilis has two Tat complexes, each with two Tat subunits, TatA and TatC. TatAdCd and TatAyCy transport different substrate proteins (Barnett et al., 2009). PhoD is secreted by the TatAdCd complex whereas YwbN is secreted by the TatAyCy complex (Eijlander et al., 2009).

The Tat systems in most Gram-positive bacteria consists of TatA and TatC. TatA is a bifunctional subunit, which can form a protein-conducting channel by self-oligomerization and can also participate in substrate recognition. Hu et al. (2010) reported the solution structure of the TatA(d) protein from Bacillus subtilis by NMR spectroscopy, the first structure of the Tat system at atomic resolution. TatA(d) shows an L-shaped structure formed by a transmembrane helix and an amphipathic helix, while the C-terminal tail is largely unstructured. These results support the postulated topology of TatA(d) in which the transmembrane helix is inserted into the lipid bilayer while the amphipathic helix lies at the membrane-water interface. Moreover, the structure of TatA(d) revealed the structural importance of several conserved residues at the hinge region, thus shedding new light on further elucidation of the protein transport mechanism.  The Tat system in Streptomyces species functions in the assembly of the cytochrome bc1 complex (Hopkins et al. 2013).

In E. coli, substrate proteins initially bind to the integral membrane TatBC complex which then recruits the protein TatA to effect translocation. Substrates bind on the periphery of the TatBC complex, causing a reduction in the diameter of TatBC. Although the TatBC complex contains multiple copies of the signal peptide-binding TatC protomer, purified TatBC-SufI complexes contain only 1 or 2 SufI molecules according to Tarry et al., 2009.  The Tat system of E. coli has been reviewed (Palmer and Berks 2012; Fröbel et al. 2012).  TatBC complexes, localized to the cell poles, function with the chaparone protein, DmsD (Kostecki et al. 2010).  TatA assembly and oligomerization occurs in response to substrate availability and can be reversed only by substrate transport. In contrast to TatA, the oligomeric states of TatB and TatC are not affected by substrate or the PMF, although TatB oligomerization requires TatC (Alcock et al. 2013).

A TatBC subcomplex and a homomeric TatA subcomplex comprise the TatABC complex (Fröbel et al., 2012). TatB and TatC coordinately recognize twin-arginine signal peptides and accommodate them in membrane-embedded binding pockets. Binding of the signal sequence to the Tat translocase requires the proton-motive force (PMF). When targeted in this manner, folded twin-arginine precursors induce homo-oligomerization of TatB and TatA. Ultimately, this leads to the formation of a transmembrane protein conduit that possibly consists of a pore-like TatA structure. The translocation step again is dependent on the PMF. The E. coli TatA and TatB proteins have a stable N-out C-in topology in intact cells (Koch et al., 2012).  It has been proposed that the TatA transmembrane pore could self-assemble via intra- and intermolecular salt bridges (Walther et al. 2013).

Membrane protein assembly is a fundamental process in all cells. The membrane-bound Rieske iron-sulfur protein is an essential component of the cytochrome bc(1) and cytochrome b(6)f complexes, and it is exported across the energy-coupling membranes of bacteria and plants in a folded conformation in the (Tat) pathway. Although the Rieske protein in most organisms is a monotopic membrane protein, in actinobacteria, it is a polytopic protein with three TMSs. The Rieske protein of Streptomyces coelicolor requires both the Sec and the Tat pathways for assembly: the initial two TMSs integrated into the membrane in a Sec-dependent manner, whereas integration of the third TMS, and thus the correct orientation of the iron-sulfur domain, require the activity of the Tat translocase (Keller et al., 2012). 

Electron microscopy displayed TatA complexes in direct contact with the membrane-stabilizing PspA protein. PspB and PspC were important for the TatA-PspA contact, but the activator protein PspF was not involved in the PspA-TatA interaction, demonstrating that basal levels of PspA already interact with TatA (Mehner et al. 2012). Elevated TatA levels caused membrane stress that induced a strictly PspBC- and PspF-dependent up-regulation of PspA. TatA complexes were found to destabilize membranes under these conditions. At native TatA levels, PspA deficiency clearly affected anaerobic TMAO respiratory growth, suggesting that energetic costs for transport of large Tat substrates such as TMAO reductase can become growth limiting in the absence of PspA (Mehner et al. 2012). The physiological role of PspA recruitment to TatA may therefore be the control of membrane stress at active translocons.

Each subunit of TatA consists of a transmembrane segment, an amphiphilic helix (APH), and a C-terminal densely charged region (DCR). The sequence of charges in the DCR is complementary to the charge pattern on the APH, suggesting that the protein can be 'zipped up' by a ladder of seven salt bridges (Walther et al. 2013). The length of the resulting hairpin matches the lipid bilayer thickness; hence a transmembrane pore could self-assemble via intra- and intermolecular salt bridges. The monomer-oligomer equilibrium of specific charge mutants was monitored (Walther et al. 2013). Similar 'charge zippers' were proposed for other membrane-associated proteins, e.g., the biofilm-inducing peptide TisB, the human antimicrobial peptide dermcidin, and the pestiviral E(RNS) protein. 

Tat-mediated protein translocation initiates by signal peptide recognition and substrate binding to the TatBC complex. Upon formation of the TatBC-substrate protein complex, TatA subunits are recruited and form the protein translocation pore. TatB forms a tight complex with TatC at 1:1 molar ratio with multiple copies of both proteins. Cross-linking experiments demonstrate that TatB functions in tetrameric units and interacts with both TatC and substrate proteins. The solution structure of TatB in DPC micelles has been determined by Nuclear Magnetic Resonance (NMR) spectroscopy (Zhang et al. 2014). The structure shows an extended 'L-shape' conformation comprising four helices: a transmembrane helix (TMH) alpha1, an amphipathic helix (APH) alpha2, and two solvent exposed helices alpha3 and alpha4. The packing of TMH and APH is relatively rigid, whereas helices alpha3 and alpha4 display notably higher mobility. The observed floppiness of helices alpha3 and alpha4 allows TatB to sample a large conformational space, thus providing high structural plasticity to interact with substrate proteins of different sizes and shapes (Zhang et al. 2014).

Redox Enzyme Maturation Proteins (REMPs) are system specific chaperones, which play roles in the maturation of Tat-dependent respiratory enzymes. Kuzniatsova et al. 2016 applied the in vivo bacterial two-hybrid technique to investigate interaction of REMPs with the TatBC proteins, finding that all but the formate dehydrogenase REMP dock to TatB or TatC. They focused on the NarJ subfamily; DmsD, the REMP for dimethyl sulfoxide reductase in E. coli, had previously been shown to interact with TatB and TatC. These REMPs interact with TatC cytoplasmic loops 1, 2 and 4 with the exception of NarJ that only interacts with loops 1 and 4. An in vitro isothermal titration calorimetry study was applied to confirm the evidence of interactions between TatC fragments and DmsD chaperone. Using a peptide overlapping array, it was shown that the different NarJ subfamily REMPs interact with different regions of the TatB cytoplasmic domains. Thus, REMP chaperones play a role in targeting respiratory enzymes to the Tat system (Kuzniatsova et al. 2016). 

In E. coli, TatBC comprise the substrate receptor complex, and active Tat translocases are formed by the substrate-induced association of TatA oligomers with this receptor. Proteins are targeted to TatBC by their twin arginine signal peptides.  Huang et al. 2017 isolated substitutions, locating to the transmembrane helix of TatB, that restored transport activity to Tat signal peptides with inactivating twin arginine substitutions. A subset of these variants also suppressed inactivating substitutions in the signal peptide binding site on TatC. The suppressors did not function by restoring detectable signal peptide binding to the TatBC complex. Instead, site-specific cross-linking experiments indicated that the suppressor substitutions induced conformational changes in the complex and movement of the TatB subunit. The TatB F13Y substitution was associated with the strongest suppressing activity, even allowing transport of a Tat substrate lacking a signal peptide. In vivo analysis using a TatA-YFP fusion showed that the TatB F13Y substitution resulted in signal peptide-independent assembly of the Tat translocase. Huang et al. 2017 concluded that Tat signal peptides play roles in substrate targeting and in triggering assembly of the active translocase. TatA organization in the inner membrane changes in response to changes in Tat A, B, and C subunit stoichiometries (Smith et al. 2017).

A subset of membrane proteins have globular, cofactor-containing extracytoplasmic domains requiring the dual action of the co-translational Sec and post-translational Tat pathways for integration. Tooke et al. 2017 identified new families of membrane proteins that are dual Sec-Tat-targeted. A predicted heme-molybdenum cofactor-containing protein, and a complex polyferredoxin protein each requires the concerted action of these two translocases for assembly. The mechanism of handover from he Sec to the Tat pathway requires relatively low hydrophobicity of the Tat-dependent transmembrane domain. This, coupled with the presence of C-terminal positive charges, results in abortive insertion of this transmembrane domain by the Sec pathway and its subsequent release at the cytoplasmic side of the membrane. These results point to a simple unifying mechanism governing the assembly of dual targeted membrane proteins (Tooke et al. 2017).

The generalized transport reaction is:

Folded protein or protein domain (cytoplasm) + energy → Folded protein or protein domain (out) (periplasm of Gram-negative bacteria)



This family belongs to the .

 

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Jongbloed, J.D., Grieger, U., Antelmann, H., Hecker, M., Nijland, R., Bron, S., and van Dijl, J.M. (2004). Two minimal Tat translocases in Bacillus. Mol. Microbiol. 54: 1319-1325.

Jongbloed, J.D.H., U. Martin, H. Antelmann, M. Hecker, H. Tjalsma, G. Venema, S. Bron, J.M. van Dijl, and J. Müller. (2000). TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J. Biol. Chem. 275: 41350-41357.

Keller, R., J. de Keyzer, A.J. Driessen, and T. Palmer. (2012). Co-operation between different targeting pathways during integration of a membrane protein. J. Cell Biol. 199: 303-315.

Kimura, Y., H. Saiga, H. Hamanaka, and H. Matoba. (2006). Myxococcus xanthus twin-arginine translocation system is important for growth and development. Arch. Microbiol. 184: 387-396.

Kneuper, H., B. Maldonado, F. Jäger, M. Krehenbrink, G. Buchanan, R. Keller, M. Müller, B.C. Berks, and T. Palmer. (2012). Molecular dissection of TatC defines critical regions essential for protein transport and a TatB-TatC contact site. Mol. Microbiol. 85: 945-961.

Koch, S., M.J. Fritsch, G. Buchanan, and T. Palmer. (2012). Escherichia coli TatA and TatB proteins have N-out, C-in topology in intact cells. J. Biol. Chem. 287: 14420-14431.

Kostecki, J.S., H. Li, R.J. Turner, and M.P. DeLisa. (2010). Visualizing interactions along the Escherichia coli twin-arginine translocation pathway using protein fragment complementation. PLoS One 5: e9225.

Kreutzenbeck, P., C. Kröger, F. Lausberg, N. Blaudeck, G.A. Sprenger, and R. Freudl. (2007). Escherichia coli twin arginine (Tat) mutant translocases possessing relaxed signal peptide recognition specificities. J. Biol. Chem. 282: 7903-7911.

Kuzniatsova, L., T.M. Winstone, and R.J. Turner. (2016). Identification of protein-protein interactions between the TatB and TatC subunits of the twin-arginine translocase system and respiratory enzyme specific chaperones. Biochim. Biophys. Acta. 1858: 767-775.

Lange, C., S.D. Müller, T.H. Walther, J. Bürck, and A.S. Ulrich. (2007). Structure analysis of the protein translocating channel TatA in membranes using a multi-construct approach. Biochim. Biophys. Acta. 1768: 2627-2634.

Lausberg, F., S. Fleckenstein, P. Kreutzenbeck, J. Fröbel, P. Rose, M. Müller, and R. Freudl. (2012). Genetic evidence for a tight cooperation of TatB and TatC during productive recognition of twin-arginine (Tat) signal peptides in Escherichia coli. PLoS One 7: e39867.

Lee, P.A., G. Buchanan, N.R. Stanley, B.C. Berks, and T. Palmer. (2002). Truncation analysis of TatA and TatB defines the minimal functional units required for protein translocation. J. Bacteriol. 184: 5871-5879.

Luo, D.X., D.L. Cao, Y. Xiong, X.H. Peng, and D.F. Liao. (2010). A novel model of cholesterol efflux from lipid-loaded cells. Acta Pharmacol Sin 31: 1243-1257.

Ma X. and Cline K. (2010). Multiple precursor proteins bind individual Tat receptor complexes and are collectively transported. EMBO J. 29(9):1477-88.

Maldonado B., Buchanan G., Muller M., Berks BC. and Palmer T. (201). Genetic evidence for a TatC dimer at the core of the Escherichia coli twin arginine (Tat) protein translocase. J Mol Microbiol Biotechnol. 20(3):168-75.

Maurer, C., S. Panahandeh, A.C. Jungkamp, M. Moser, and M. Müller. (2010). TatB functions as an oligomeric binding site for folded Tat precursor proteins. Mol. Biol. Cell 21: 4151-4161.

Mehner, D., H. Osadnik, H. Lünsdorf, and T. Brüser. (2012). The Tat system for membrane translocation of folded proteins recruits the membrane-stabilizing Psp machinery in Escherichia coli. J. Biol. Chem. 287: 27834-27842.

Minshall, R.D. and A.B. Malik. (2006). Transport across the endothelium: regulation of endothelial permeability. Handb Exp Pharmacol 107-144.

Mori, H., E.J. Summer, and K. Cline. (2001). Chloroplast TatC plays a direct role in thylakoid δpH-dependent protein transport. FEBS Lett. 501: 65-68.

Oresnik, I.J., C.L. Ladner, and R.J. Turner. (2001). Identification of a twin-arginine leader-binding protein. Molec. Microbiol. 40: 323-331.

Pal D., Fite K. and Dabney-Smith C. (2013). Direct interaction between a precursor mature domain and transport component Tha4 during twin arginine transport of chloroplasts. Plant Physiol. 161(2):990-1001.

Palmer, T. and B.C. Berks. (2012). The twin-arginine translocation (Tat) protein export pathway. Nat. Rev. Microbiol. 10: 483-496.

Papish, A.L., C.L. Ladner, and R.J. Turner. (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.

Petrů, M., J. Wideman, K. Moore, F. Alcock, T. Palmer, and P. Doležal. (2018). Evolution of mitochondrial TAT translocases illustrates the loss of bacterial protein transport machines in mitochondria. BMC Biol 16: 141.

Punginelli, C., B. Maldonado, S. Grahl, R. Jack, M. Alami, J. Schröder, B.C. Berks, and T. Palmer. (2007). Cysteine scanning mutagenesis and topological mapping of the Escherichia coli twin-arginine translocase TatC Component. J. Bacteriol. 189: 5482-5494.

Quest, A.F., J.L. Gutierrez-Pajares, and V.A. Torres. (2008). Caveolin-1: an ambiguous partner in cell signalling and cancer. J Cell Mol Med 12: 1130-1150.

Richter, S., U. Lindenstrauss, C. Lücke, R. Bayliss, and T. Brüser. (2007). Functional Tat Transport of Unstructured, Small, Hydrophilic Proteins. J. Biol. Chem. 282(46): 33257-33264.

Sambasivarao, D., H.A. Dawson, G. Zhang, G. Shaw, J. Hu, and J.H. Weiner. (2001). Investigation of Escherichia coli dimethyl sulfoxide reductase: assembly and processing in strains defective for the sec-independent protein translocation system membrane targeting and translocation. J. Biol. Chem. 276: 20167-20174.

Santini, C., I. Bérengère, A. Chanal, M. Müller, G. Giordano, and L. Wu. (1998). A novel Sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17: 101-112.

Sargent, F., B.C. Berks, and T. Palmer. (2002). Assembly of membrane-bound respiratory complexes by the Tat protein-transport system. Arch. Microbiol. 178: 77-84.

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.

Sargent, F., U. Gohlke, E. De Leeuw, N.R. Stanley, T. Palmer, H.R. Saibil, and B.C. Berks. (2001). Purified components of the Escherichia coli Tat protein transport system form a double-layered ring structure. Eur. J. Biochem. 268: 3361-3367.

Schreiber, S., R. Stengel, M. Westermann, R. Volkmer-Engert, O.I. Pop, and J.P. Muller. (2006). Affinity of TatCd for TatAd elucidates its receptor function in the Bacillus subtilis twin arginine translocation (Tat) translocase system. J. Biol. Chem. 281: 19977-19984.

Settles, A.M. and R. Martienssen. (1998). Old and new pathways of protein export in chloroplasts and bacteria. Trends Cell Biol. 8: 494-501.

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. Science 278: 1467-1470.

Smith, S.M., A. Yarwood, R.A. Fleck, C. Robinson, and C.J. Smith. (2017). TatA complexes exhibit a marked change in organisation in response to expression of the TatBC complex. Biochem. J. 474: 1495-1508.

Strauch, E.M. and G. Georgiou. (2007). Escherichia coli tatC mutations that suppress defective twin-arginine transporter signal peptides. J. Mol. Biol. 374(2):283-291.

Sun, Y., R.D. Minshall, and G. Hu. (2011). Role of caveolin-1 in the regulation of pulmonary endothelial permeability. Methods Mol Biol 763: 303-317.

Sutherland, G.A., K.J. Grayson, N.B.P. Adams, D.M.J. Mermans, A.S. Jones, A.J. Robertson, D.B. Auman, A.A. Brindley, F. Sterpone, P. Tuffery, P. Derreumaux, P.L. Dutton, C. Robinson, A. Hitchcock, and C.N. Hunter. (2018). Probing the quality control mechanism of thetwin-arginine translocase with folding variants of a-designed heme protein. J. Biol. Chem. [Epub: Ahead of Print]

Szabo, Z. and M. Pohlschroder. (2012). Diversity and subcellular distribution of archaeal secreted proteins. Front Microbiol 3: 207.

Tarry, M.J., E. Schäfer, S. Chen, G. Buchanan, N.P. Greene, S.M. Lea, T. Palmer, H.R. Saibil, and B.C. Berks. (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.

Theg, S.M., Cline, K., Finazzi, G., and Wollman, F.A. (2005). The energetics of the chloroplast Tat protein transport pathway revisited. Trends Plant Sci. 10: 153-154.

Thompson BJ., Widdick DA., Hicks MG., Chandra G., Sutcliffe IC., Palmer T. and Hutchings MI. (2010). Investigating lipoprotein biogenesis and function in the model Gram-positive bacterium Streptomyces coelicolor. Mol Microbiol. 77(4):943-57.

Tooke, F.J., M. Babot, G. Chandra, G. Buchanan, and T. Palmer. (2017). A unifying mechanism for the biogenesis of membrane proteins co-operatively integrated by the Sec and Tat pathways. Elife 6:.

Tullman-Ercek, D., M.P. DeLisa, Y. Kawarasaki, P. Iranpour, B. Ribnicky, T. Palmer, and G. Georgiou. (2007). Export pathway selectivity of Escherichia coli twin arginine translocation signal peptides. J. Biol. Chem. 282: 8309-8316.

Ulfig, A. and R. Freudl. (2018). The early mature part of bacterial twin-arginine translocation (Tat) precursor proteins contributes to TatBC receptor binding. J. Biol. Chem. [Epub: Ahead of Print]

Walther, T.H., C. Gottselig, S.L. Grage, M. Wolf, A.V. Vargiu, M.J. Klein, S. Vollmer, S. Prock, M. Hartmann, S. Afonin, E. Stockwald, H. Heinzmann, O.V. Nolandt, W. Wenzel, P. Ruggerone, and A.S. Ulrich. (2013). Folding and self-assembly of the TatA translocation pore based on a charge zipper mechanism. Cell 152: 316-326.

Walther, T.H., S.L. Grage, N. Roth, and A.S. Ulrich. (2010). Membrane alignment of the pore-forming component TatA(d) of the twin-arginine translocase from Bacillus subtilis resolved by solid-state NMR spectroscopy. J. Am. Chem. Soc. 132: 15945-15956.

Weiner, J.H., P.T. Bilous, G.M. Shaw, S.P. Lubitz, G.H. Thomas, J.A. Cole, and R.J. Turner. (1998). A novel and ubiquitous system for membrane targeting and secretion of proteins in the folded state. Cell 93: 93-101.

Wexler, M., F. Sargent, R.L. Jack, N.R. Stanley, E.G. Bogsch, C. Robinson, B.C. Berks, and T. Palmer. (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.

Widdick, D.A., K. Dilks, G. Chandra, A. Bottrill, M. Naldrett, M. Pohlschröder, and T. Palmer. (2006). The twin-arginine translocation pathway is a major route of protein export in Streptomyces coelicolor. Proc. Natl. Acad. Sci. USA 103: 17927-17932.

Yamashita, K., Y. Kawai, Y. Tanaka, N. Hirano, J. Kaneko, N. Tomita, M. Ohta, Y. Kamio, M. Yao, and I. Tanaka. (2011). Crystal structure of the octameric pore of staphylococcal γ-hemolysin reveals the β-barrel pore formation mechanism by two components. Proc. Natl. Acad. Sci. USA 108: 17314-17319.

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.

Zhang L., Liu L., Maltsev S., Lorigan GA. and Dabney-Smith C. (2013). Solid-state NMR investigations of peptide-lipid interactions of the transmembrane domain of a plant-derived protein, Hcf106. Chem Phys Lipids. 175-176:123-30.

Zhang L., Liu L., Maltsev S., Lorigan GA. and Dabney-Smith C. (2014). Investigating the interaction between peptides of the amphipathic helix of Hcf106 and the phospholipid bilayer by solid-state NMR spectroscopy. Biochim Biophys Acta. 1838(1 Pt B):413-8.

Zhang Y., Wang L., Hu Y. and Jin C. (2014). Solution structure of the TatB component of the twin-arginine translocation system. Biochim Biophys Acta. 1838(7):1881-8.

Examples:

TC#NameOrganismal TypeExample
2.A.64.1.1

TatABCE translocase. Early contacts between substrate proteins and TatA have been demonstrated (Fröbel et al., 2011). TatC helix 5 and the TatB transmembrane helix interact (Kneuper et al., 2012).  TatC functions as an obligate oligomer (Cleon et al. 2015). TatA is the most abundant component of the complex and facilitates assembly of this complex.It exhibits a uniform distribution throughout the inner membrane, but forms linear clusters upon increased expression of TatBC (Smith et al. 2017).  TatA and TatB both have the capacity to bind at two TatC sites, one in TMS5 and one in TMS6 (Habersetzer et al. 2017). However in vivo this is regulated according to the activation state of the complex. In the resting-state system, TatB binds the polar cluster site in TMS 5 with TatA occupying the site in TMS 6. However, when the system is activated by overproduction of a substrate, TatA and TatB switch binding sites. Habersetzer et al. 2017 proposed that this substrate-triggered positional exchange is a key step in the assembly of an active Tat translocase. A  highly conserved glutamate residue in the transmembrane region of E. coli TatC, which, when modified by DCCD, interferes with the deep insertion of a Tat signal peptide into the TatBC receptor complex (Blümmel et al. 2017). Different from TatA but rather like TatB, TatE contacts a Tat signal peptide independently of the proton-motive force and restricts the premature processing of a Tat signal peptide (Eimer et al. 2018). Furthermore, TatE embarks at the transmembrane helix five of TatC where it becomes so closely spaced to TatB that both proteins can be covalently linked by a zero-space cross-linker. This suggests that in addition to TatB and TatC, TatE is a component of the Tat substrate receptor complex. A bioinformatic analysis revealed a relatively broad distribution of tatE genes in bacterial phyla and highlights unique protein sequence features of TatE orthologs (Eimer et al. 2018).

Proteobacteria (also present in archaea and eukaryotic organelles)

TatABCE of E. coli

 
2.A.64.1.2

Twin arginine targeting protein translocase, TatABC (Kimura et al. 2006).

Proteobacteria

TatABC (MXAN_2960, MXAN5905-4) of Myxococcus xanthus.

 
2.A.64.1.3

TatABCE.  The twin-arginine translocation (Tat) system transports large folded proteins containing a characteristic twin-arginine motif in their signal peptide across membranes. Together with TatB, TatC is part of a receptor directly interacting with Tat signal peptides (Eimer et al. 2015; Kuzniatsova et al. 2016; Cléon et al. 2015).

TatABCE of Bdellovibrio bacteriovorus

 
2.A.64.1.4

Mitochondrial twin arginine (TatA/TatC) protein translocase.  This system has been shown to be active in E. coli (Petrů et al. 2018). Many mitochondria have lost the Tat system, while some retain only the TatC subunit.  Only those that have both TatC and TatA seem to be active (Petrů et al. 2018).

TatC/TatA of Andalucia godoyi (Jakobid flagellate)
TatC, 253 aas; M4QCS0
TatA, 52 aas; M4Q9A7

 
Examples:

TC#NameOrganismal TypeExample
2.A.64.2.1

The chloroplast Tat translocase (cpTatC/Hcf106/Tha4) (Gérard and Cline, 2007).  The precursor mature domain of the substrate protein interacts directly with Tha4 (Pal et al. 2012).  Hcf106 is predicted to contain a single amino terminal transmembrane domain followed by a Pro-Gly hinge, a predicted amphipathic alpha-helix (APH), and a loosely structured carboxy terminus.  The amphipathic α-helix interacts with the bilayer (Zhang et al., 2013a; Zhang et al. 2013b)

Plant chloroplasts

cpTatC/Hcf106/Tha4 of Arabidopsis thaliana
cpTatC (TatC or MttB family; APG2; albino and pale green 2; 340 aas) (Q9SJV5)
Hcf106 (TatA or MttA family; 260 aas) (Q9XH75)
Tha4 (TatA or MttA family; 147 aas) (Q9LKU2)

 
2.A.64.2.2

Sec-independent protein translocase, TatABC (Widdick et al. 2006).

Actinobacteria

Sec-independent protein translocase protein TatACB of Streptomyces coelicolor

TatA (Q9RJ68)
TatB (Q9FBK8)
TatC (Q9RJ69)

 
Examples:

TC#NameOrganismal TypeExample
2.A.64.3.1TatAd/Bd translocase (Jongbloed et al., 2004)

Firmicutes

TatAd/Cd of Bacillus subtilis
TatAd (70 aas; O31467)
TatCd (245 aas; P42252)
 
2.A.64.3.2TatAy/Cy translocase (Jongbloed et al., 2004)

Firmicutes

TatAy/Cy of Bacillus subtilis
TatAy (57 aas; O05522)
TatCy (254 aas; O05523)
 
Examples:

TC#NameOrganismal TypeExample
2.A.64.4.1

Twin arginine (TatA0/TatC0) protein translocase (Dilks et al. 2005; Giménez et al. 2007; Szabo and Pohlschroder 2012).

Archaea

Twin arginine translocase, TatAC0 of Haloferax volcanii
TatA0 (D4GVK4)
TatC0 (D4GZD0) 

 
Examples:

TC#NameOrganismal TypeExample
2.A.64.5.1

Twin Arginine (TatAt/TatCt) protein translocase (Dilks et al. 2005; Giménez et al. 2007; Szabo and Pohlschroder 2012).

Archaea

Tat system, TatACt of Haloferax volcanii
TatAt (91aas) (D4GWC8)
TatCt (718aas; duplicated with 8+6=14 putative TMSs) (D4GWC9) 

 
Examples:

TC#NameOrganismal TypeExample
2.A.64.6.1

A Tat system, TatC of 365 aas and 6 TMSs, and a potential TatB of 71 aas and 1 TMS.

Tat (TatBC) system of Candidatus Saccharibacteria bacterium

 

 
2.A.64.6.2

Tat (TatCB) system consisting of TatC (238 aas and 5 or 6 TMSs) and TatB (73 aas and 1 TMS).

TatBC of Candidatus Saccharibacteria bacterium

 
2.A.64.6.3

Tat system consisting of TatC (355 aas and 5 or 6 TMSs) and putative TatB (62 aas and 1 TMS). The tat genes are flanked by a sortase gene (WP_104944876) and a groL chaparone protein-encoding gene (WP_104944880).

TatBC of Candidatus Saccharibacteria bacterium

 
Examples:

TC#NameOrganismal TypeExample