2.C.1 The TonB-ExbB-ExbD/TolA-TolQ-TolR Outer Membrane Receptor Energizers and Stabilizers (TonB/TolA) Family

The TonB heterotrimeric complexes span the cytoplasmic membrane and the periplasm and interact with outer membrane receptors in Gram-negative bacteria. Homologues have been found only in Gram-negative bacteria and cyanobacteria. E. coli possesses two paralogous systems, the TonB-ExbB-ExbD system and the TolA-TolQ-TolR system. Corresponding proteins have been identified in other Gram-negative bacteria. TonB (239 aas) and TolA (412 aas) of E. coli both span the cytoplasmic membrane once near their N-termini, span the periplasm as α-helices and interact with the outer membrane. They are not demonstrably homologous, but they are believed to serve comparable functions. It has been suggested that TonB or its C-terminal domain shuttles between the cytoplasmic and outer membranes as part of the energy transduction process. ExbB (244 aas) and TolQ (230 aas) are paralogous. They span the membrane 3 times with their N-termini in the periplasm and most of the protein mass localized to the cytoplasmic side of the membrane. ExbD (141 aas) and TolR (142 aas) are also paralogous. They span the membrane near their N-termini with remaining parts of the proteins in the periplasm. The TonB system energizes transport (uptake) via OMR-type porins (TC #1.B.14) of vitamin B12, iron-siderophores, group B colicins and the DNA of filamentous bacteriophage such as φ80 and T1. It may also be involved in the extrusion of drugs and organic solvents from Pseudomonas putida (Godoy et al., 2001), but the mechanism is not known. The TolA system transports group A colicins and the DNA of other filamentous phages. Colicin import requires close proximity of the inner and outer membranes. Loss of one of the TolA-TolQ-TolR proteins results in loss of periplasmic enzymes and increased sensitivity to drugs and bile salts. Surface localization of O-antigen lipopolysaccharide in E. coli depends on the TolA protein, possibly explaining the leakiness of TolA mutants. The TolA/Pal system has also been reported to be necessary for the uptake of certain solutes (sugars, polyols, amino acids) (Llamas et al., 2003), but the mechanism was not investigated. TolR may rotate (Zhang et al. 2009).

Microcin E492 (TC #1.C.58.1.1) kills E. coli and other enterobacteria in a mechanism that depends on TonB, ExbBD, energy, and OMRs such as FepA (Destoumieux-Garzon et al., 2003). This energy-dependent system promotes import acoss the outer membrane and into the inner membrane where microcin E492 exerts its action.  Just how the energy cycle functions is still controversial, but Gresock et al. 2015 have provided evidence that the cycle involves monomer/dimer transitions. They proposed a model in which interaction of TonB homodimers with ExbD homodimers initiates the energy transduction cycle, and, ultimately, the ExbD carboxy terminus modulates interactions of a monomeric TonB carboxy terminus with OM transporters. After TonB exchanges its interaction with ExbD for interaction with a transporter, ExbD homodimers undergo a separate cycle needed to re-energize them (Gresock et al. 2015).

The TolA/TolQR system interacts with other proteins that appear to play a role in transport of colicins such as Colicin A and Colicin E9 (Hands et al., 2005). These include the periplasmic TolB (430 aas; spP19935), the periplasmic YbgF (263 aas; spP45955), and the outer membrane peptidoglycan-associated protein, Pal (173 aas; spP07176). These proteins probably all interact with each other, and several interact with Colicin A (Journet et al., 2001). They probably also interact with trimeric porins and OmpA. TolB interacts with the translocation domain of TolB via the TolB box located in the N-terminal translocation domain of the enzymatic E colicins (Hands et al., 2005). Based on the NMR solution structure, the periplasmic domain of TolR forms a C 2-symmetric dimer consisting of a strongly curved eight-stranded beta-sheet, generating a large deep groove on one side, while four helices cover the other face of the sheet (Parsons et al., 2008). This domain may interact with other components of the Pal/Tol system, particularly TolQ.  Interactions between the Tol subunits have been mapped, and evidence for rotation of the TolR TMS have been presented (Zhang et al. 2009; Zhang et al. 2011).

To penetrate the target cell, colicins bind to an outer membrane receptor at the cell surface and then translocate their N-terminal domain through the outer membrane and the periplasm. Once fully translocated, the N-terminal domain triggers entry of the catalytic C-terminal domain by an unknown process. Colicin K uses the Tsx nucleoside-specific receptor for binding at the cell surface, the OmpA protein for translocation through the outer membrane, and the TolABQR proteins for the transit through the periplasm. Barneoud-Arnoulet et al. (2010) described how the colicin K N-terminal domain (KT) interacts with the components of its transit machine in the periplasm. Upon production of KT in wild-type strains, cells became partly resistant to Tol-dependent colicins and sensitive to detergent and released periplasmic proteins and outer membrane vesicles, suggesting that KT interacts with and titrates components of its import machine (Barnéoud-Arnoulet et al., 2010). KT interacts with TolA, TolB and TolR. TolQ and the colicin translocation domain also interact.

Fission of bacterial cells involves the co-ordinated invagination of the envelope layers. Invagination of the cytoplasmic membrane (IM) and peptidoglycan (PG) layer is likely driven by the septal ring organelle. Invagination of the outer membrane (OM) in Gram-negative species is thought to occur passively via its tethering to the underlying PG layer with generally distributed PG-binding OM (lipo)proteins. The Tol-Pal system is energized by the proton motive force and is well conserved in Gram-negative bacteria. It consists of five proteins that can connect the OM to both the PG and IM layers via protein-PG and protein-protein interactions. As noted above, the system is needed to maintain full OM integrity, and for class A colicins and filamentous phages to enter cells. All five components accumulate at constriction sites in Escherichia coli, and mutants lacking an intact system suffer delayed OM invagination (Gerding et al., 2006). They contain large OM blebs at constriction sites and cell poles. The Tol-Pal system apparently constitutes a dynamic subcomplex of the division apparatus in Gram-negative bacteria that consumes energy to establish transient trans-envelope connections at or near the septal ring to draw the OM onto the invaginating PG and IM layers during constriction (Gerding et al., 2007). ExbD has a periplasmic domain that is structurally similar to siderophore binding proteins (Garcia-Herrero et al., 2007).

ExbB-ExbD are homologous to (but distantly related to) the MotA-MotB proteins of the Mot family (TC# 1.A.45). The latter proteins serve as the motor of the bacterial flagellum. While the MotA-B proteins have been shown to provide a transmembrane proton translocation pathway, the same has not yet been demonstrated for the ExbB-D proteins. It is expected, however, that they will serve this function and thereby energize outer membrane transport. It is likely that all of these proteins can be considered both as proton channel proteins and as pmf-dependent energizers, and that they belong in a single family.

Braun and Herrmann (2004) have proposed that at least three well-conserved transmembrane residues in ExbB (or TolQ) comprise the proton pathway. These proposed channel residues in ExbB are Thr148 in TMS2 and glu176 and Thr181 in TMS3. The first two are strictly conserved in all ExbB and TolQ homologues, and the third is almost strictly conserved in all MotA homologues as well. Asp25 in ExbD may also comprise part of this proton pathway (Braun and Herrmann, 2004). The only protonatable residue in the TMS of TonB, a histidyl residue can be replaced by a non-protonatable Gln without loss of activity. Thus, the TonB TMS is not on a proton conductance pathway. It only indirectly responds to pmf, probably via ExbD (Swayne and Postle, 2011).

Bacteria producing endonuclease colicins are protected against the cytotoxic activity by a small immunity protein that binds with high affinity and specificity to inactivate the endonuclease. This complex is released into the extracellular medium, and the immunity protein is jettisoned upon binding of the complex to susceptible cells. At what stage during infection does immunity protein release occur? Duche et al., (2006) constructed a hybrid immunity protein composed of the enhanced green fluorescent protein (EGFP) fused to the colicin E2 immunity protein (Im2) to enhance its detection. The EGFP-Im2 protein bound the free colicin E2 with a 1:1 stoichiometry and specifically inhibited its DNase activity. The addition of this hybrid complex to susceptible cells revealed that release of the hybrid immunity protein is a time-dependent process, achieved 20 min after the addition of the complex to the cells. Complex dissociation required a functional translocon formed by the BtuB protein and one porin (either OmpF or OmpC) and a functional import machinery formed by the Tol proteins. Cell fractionation and protease susceptibility experiments indicated that the immunity protein does not cross the cell envelope during colicin import. These observations suggest that dissociation of the immunity protein occurs at the outer membrane surface and requires full translocation of the colicin E2 N-terminal domain (Duche et al., 2006).

The structure of BtuB outer membrane receptor (OMR; 1.B.14.3.1) and the FhuA OMR (1.B.14.1.4) complexed with the C-terminal domain of TonB (2.C.1.1.1), the energy transmitter to the OMR from the EBDxb energizer, shows TonB binding to the TonB box in the OMRs. TonB binding causes the TonB box to form a β-strand, forming a β-sheet with TonB's own β-strand. This is consistent with a mechanical 'pulling' mechanism of transport (Shultis et al., 2006). The conserved TonB arginine 166 is oriented to form multiple contacts with the FhuA 'cork', the globublar domain enclosed by the β-barrel (Pawelek et al., 2006).

TonB-dependent transporters bind and transport ferric chelates, vitamin B12, nickel complexes, and carbohydrates. The transport process requires energy in the form of the pmf and the TonB-ExbB-ExbD complex to transduce this energy to the outer membrane. The siderophore substrates range in complexity from simple small molecules such as citrate to large proteins such as serum transferrin and hemoglobin. Expression can be regulated by metal-dependent regulators, σ/anti-σ factors, small RNAs, and a riboswitch (Noinaj et al., 2010). Noinaj et al. (2010) summarized the regulation, structure and function of these systems.

ExbB and ExbD harness the proton gradient to energize TonB, which directly contacts and transmits this energy to ligand-loaded transporters. In E. coli, the periplasmic domain of ExbD appears to transition from proton motive force-independent to proton motive force-dependent interactions with TonB, catalyzing the conformational changes of TonB. While all regions except the extreme amino terminus of ExbD are indispensable for function, distinct roles for the amino and carboxy terminal regions of the ExbD periplasmic domain have been determined (Ollis et al., 2012). Like residue D25 in the ExbD transmembrane domain, periplasmic residues 42-61 facilitate the conformational response of ExbD to proton motive force. This region appears important for transmitting signals between the ExbD transmembrane domain and carboxy terminus. The carboxy terminus, encompassing periplasmic residues 62-141, are required for initial assembly with the periplasmic domain of TonB, a stage of interaction required for ExbD to transmit its conformational response to proton motive force to TonB. Residues 92-121 are important for all three interactions; ExbD homodimers, TonB-ExbD heterodimers, and ExbD-ExbB heterodimers. The distinct requirement of this ExbD region for interaction with ExbB raised the possibility of direct interaction with the few residues of ExbB that occupy the periplasm.

The generalized transport process energized by TonB-type systems is:

substrate (out) substrate (periplasm).



This family belongs to the .

 

References:

Barnéoud-Arnoulet, A., M. Gavioli, R. Lloubès, and E. Cascales. (2010). Interaction of the colicin K bactericidal toxin with components of its import machinery in the periplasm of Escherichia coli. J. Bacteriol. 192: 5934-5942.

Bell, P.E., C.T. Nau, J.T. Brown, J. Konisky, and R.J. Kadner. (1990). Genetic suppression demonstrates interaction of TonB protein with outer membrane transport proteins in Escherichia coli. J. Bacteriol. 172: 3826-3829.

Benevides-Matos, N., C. Wandersman, and F. Biville. (2008). HasB, the Serratia marcescens TonB paralog, is specific to HasR. J. Bacteriol. 190(1):21-7.

Braun, V. and C. Herrmann. (2004). Point mutations in transmembrane helices 2 and 3 of ExbB and TolQ affect their activities in Escherichia coli K-12. J. Bacteriol. 186: 4402-4406.

Braun, V., H. Pilsl, and P. Gross. (1994). Colicins: structures, modes of action, transfer through membranes and evolution. Arch. Microbiol. 161: 199-206.

Destoumieux-Garzón, D., X. Thomas, M. Santamaria, C. Goulard, M. Barthélémy, B. Boscher, Y. Bessin, G. Molle, A.-M. Pons, L. Letellier, J. Peduzzi, and S. Rebuffat. (2003). Microcin E492 antibacterial activity: evidence for a TonB-dependent inner membrane permeabilization on Escherichia coli. Mol. Microbiol. 49: 1031-1041.

Duche D., A. Frenkian, V. Prima, R. Lloubes. (2006). Release of immunity protein requires functional endonuclease colicin import machinery. J Bacteriol. 188: 8593-8600.

Garcia-Herrero, A., R.S. Peacock, S.P. Howard, and H.J. Vogel. (2007). The solution structure of the periplasmic domain of the TonB system ExbD protein reveals structural homology with siderophore-binding proteins. Mol. Microbiol. 66(4): 872-889.

Gaspar, J.A., J.A. Thomas, C.L. Marolda, and M.A. Valvano. (2000). Surface expression of O-specific lipopolysaccharide in Escherichia coli requires the funtion of the TolA protein. Molec. Microbiol. 38: 262-275.

Gerding, M.A., Y. Ogata, N.D. Pecora, H. Niki, and P.A. de Boer PA. (2007). The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol. Microbiol. 63: 1008-1025.

Godoy, P., M.I. Ramos-González, and J.L. Ramos. (2001). Involvement of the TonB system in tolerance to solvents and drugs in Pseudomonas putida DOT-T1E. J. Bacteriol. 183: 5285-5292.

Gouaux, E. (1997). The long and short of colicin action: the molecular basis for the biological activity of channel-forming colicins. Structure 5: 313-317.

Gresock MG., Kastead KA. and Postle K. (2015). From Homodimer to Heterodimer and Back: Elucidating the TonB Energy Transduction Cycle. J Bacteriol. 197(21):3433-45.

Hands, S.L., Holland, L.E., Vankemmelbeke, M., Fraser, L., Macdonald, C.J., Moore, G.R., James, R., and Penfold, C.N. (2005). Interactions of TolB with the translocation domain of colicin E9 require an extended TolB box. J Bacteriol. 187: 6733-6741.

Hernández-Montalvo, V., F. Valle, F. Bolivar, and G. Gosset. (2001). Characterization of sugar mixtures utilization by an Escherichia coli mutant devoid of the phosphotransferase system. Appl. Microbiol. Biotechnol. 57: 186-191.

Journet, L., E. Bouveret, A. Rigal, R. Lloubes, C Lazdunski, and H. Bénédetti. (2001). Import of colicins across the outer membrane of Escherichia coli involves multiple protein interactions in the periplasm. Mol. Microbiol. 42: 331-344.

Kadner, R.J. (1990). Vitamin B12 transport in Escherichia coli: energy coupling between membranes. Mol. Microbiol. 4: 2027-2033.

Klebba, P.E. (2016). ROSET Model of TonB Action in Gram-Negative Bacterial Iron Acquisition. J. Bacteriol. 198: 1013-1021.

Lazdunski, C., E. Bouveret, A. Rigal, L. Journet, R. Lloubès, and H. Bénédetti. (2000). Colicin import into Escherichia coli cells requires the proximity of the inner and outer membranes and other factors. Int. J. Med. Microbiol. 290: 337-344.

Lazzaroni, J.C., P. Germon, M.-C. Ray, and A. Vianney. (1999). The Tol proteins of Escherichia coli and their involvement in the uptake of biomolecules and outer membrane stability. FEMS Microbiol. Lett. 177: 191-197.

Letain, T.E. and K. Postle. (1997). TonB protein appears to transduce energy by shuttling between the cytoplasmic membrane and the outer membrane in Escherichia coli. Mol. Microbiol. 24: 271-283.

Llamas, M.A., J.J. Rodríguez-Herva, R.E.W. Hancock, W. Bitter, J. Tommassen, and J.L. Ramos. (2003). Role of Pseudomonas putida tol-oprL gene products in uptake of solutes through the cytoplasmic membrane. J. Bacteriol. 185: 4707-4716.

Muller, M.M., A. Vianney, J.-C. Lazzaroni, R.E. Webster, and R. Portalier. (1993). Membrane topology of the Escherichia coli TolR protein required for cell envelope intergity. J. Bacteriol. 175: 6059-6061.

Noinaj, N., M. Guillier, T.J. Barnard, and S.K. Buchanan. (2010). TonB-dependent transporters: regulation, structure, and function. Annu. Rev. Microbiol. 64: 43-60.

Ollis AA., Kumar A. and Postle K. (2012). The ExbD periplasmic domain contains distinct functional regions for two stages in TonB energization. J Bacteriol. 194(12):3069-77.

Parsons, L.M., A. Grishaev, and A. Bax. (2008). The periplasmic domain of TolR from Haemophilus influenzae forms a dimer with a large hydrophobic groove: NMR solution structure and comparison to SAXS data. Biochemistry 47: 3131-42.

Pawelek, P.D., N. Croteau, C. Ng-Thow-Hing, C.M. Khursigara, N. Moiseeva, M. Allaire, and J.W. Coulton. (2006). Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312: 1399-1402.

Postle, K. (1993). TonB protein and energy transduction between membranes. J. Bioenerg. Biomembr. 25: 591-601.

Postle, K. and R.J. Kadner. (2003). Touch and go: tying TonB to transport. Mol. Microbiol. 49: 869-882.

Qiu, G.W., W.J. Lou, C.Y. Sun, N. Yang, Z.K. Li, D.L. Li, S.S. Zang, F.X. Fu, D.A. Hutchins, H.B. Jiang, and B.S. Qiu. (2018). Outer Membrane Iron Uptake Pathways in the Model Cyanobacterium Synechocystis sp. Strain PCC 6803. Appl. Environ. Microbiol. 84:.

Rassam, P., K.R. Long, R. Kaminska, D.J. Williams, G. Papadakos, C.G. Baumann, and C. Kleanthous. (2018). Intermembrane crosstalk drives inner-membrane protein organization in Escherichia coli. Nat Commun 9: 1082.

Roof, S.K., J.D. Allard, K.P. Bertrand, and K. Postle. (1991). Analysis of Escherichia coli TonB membrane topology by use of PhoA fusions. J. Bacteriol. 173: 5554-5557.

Santos, T.M., T.Y. Lin, M. Rajendran, S.M. Anderson, and D.B. Weibel. (2014). Polar localization of Escherichia coli chemoreceptors requires an intact Tol-Pal complex. Mol. Microbiol. 92: 985-1004.

Shrivastava, R., X. Jiang, and S.S. Chng. (2017). Outer membrane lipid homeostasis via retrograde phospholipid transport in Escherichia coli. Mol. Microbiol. 106: 395-408.

Shultis, D.D., M.D. Purdy, C.N. Banchs, and M.C. Wiener. (2006). Outer membrane active transport: structure of the BtuB:TonB complex. Science 312: 1396-1399.

Smajs, D. and G.M. Weinstock. (2001). The iron- and temperature-regulated cjrBC genes of Shigella and enteroinvasive Escherichia coli strains code for colicin Js uptake. J. Bacteriol. 183: 3958-3966.

Stolz, J., H.J. Wöhrmann, and C. Vogl. (2005). Amiloride uptake and toxicity in fission yeast are caused by the pyridoxine transporter encoded by bsu1+ (car1+). Eukaryot. Cell. 4: 319-326.

Swayne, C. and K. Postle. (2011). Taking the Escherichia coli TonB transmembrane domain "offline"? Nonprotonatable Asn substitutes fully for TonB His20. J. Bacteriol. 193: 3693-3701.

Vianney, A., T.M. Lewin, W.F. Beyer, Jr., J.C. Lazzaroni, R. Portalier, and R.E. Webster. (1994). Membrane topology and mutational analysis of the TolQ protein of Escherichia coli required for the uptake of macromolecules and cell envelope integrity. J. Bacteriol. 176: 822-829.

Vogl, C., C.M. Klein, A.F. Batke, M.E. Schweingruber, and J. Stolz. (2008). Characterization of Thi9, a novel thiamine (Vitamin B1) transporter from Schizosaccharomyces pombe. J. Biol. Chem. 283: 7379-7389.

Zhai, Y.F., W. Heijne, and M.H. Saier, Jr. (2003). Molecular modeling of the bacterial outer membrane receptor energizer, ExbBD/TonB, based on homology with the flagellar motor, MotAB. Biochim. Biophys. Acta 1614: 201-210.

Zhang, H.H., D.R. Blanco, M.M. Exner, E.S. Shang, C.I. Champion, M.L. Phillips, J.N. Miller, and M.A. Lovett. (1999). Renaturation of recombinant Treponema pallidum rare outer membrane protein 1 into a trimeric, hydrophobic, and porin-active conformation. J. Bacteriol. 181: 7168-7175.

Zhang, X.Y., E.L. Goemaere, N. Seddiki, H. Célia, M. Gavioli, E. Cascales, and R. Lloubes. (2011). Mapping the interactions between Escherichia coli TolQ transmembrane segments. J. Biol. Chem. 286: 11756-11764.

Zhang, X.Y., E.L. Goemaere, R. Thomé, M. Gavioli, E. Cascales, and R. Lloubès. (2009). Mapping the interactions between escherichia coli tol subunits: rotation of the TolR transmembrane helix. J. Biol. Chem. 284: 4275-4282.

Examples:

TC#NameOrganismal TypeExample
2.C.1.1.1

The TonB energy-transducing system. ExbB/D are listed under TC# 1.A.30.2.1. The rotational surveillance and energy transfer (ROSET) model of TonB action postulates a mechanism for the transfer of energy from the Inner Membrane to the Outer Membrane, triggering iron uptake and concentration in the periplasm (Klebba 2016).

Gram-negative bacteria

The TonB/ExbBD system of E. coli

 
2.C.1.1.10

TonB family protein of 272 aas and 1 N-terminal TMS.

TonB of Coraliomargarita sp. CAG:312

 
2.C.1.1.11

Gram-negative bacterial TonB protein of 260 aas and 1 N-terminal TM

TonB of Candidatus Scalindua brodae

 
2.C.1.1.2HasB (a distant TonB homologue that is specific for HasR (1.B.14.5.1)) (Benevides-Matos et al., 2008).BacteriaHasB of Serratia marcescens (Q79AD1)
 
2.C.1.1.3

The CjrB TonB homologue of 258 aas;  involved in colicin J uptake together with CjrC, an outer membrane receptor (Smajs and Weinstock 2001).  CjrC has TC# 1.B.14.7.5.  They function together and are regulated by iron and temperature.

Proteobacteria

CjrB of E. coli

 
2.C.1.1.4

TonB homologue of 244 aas and 1 TMS

TonB of Bdellovibrio bacteriovorus

 
2.C.1.1.5

TonB-like protein of 195 aas

TonB-like protein of Bdellovibrio bacteriovorus

 
2.C.1.1.6

TonB of 230 aas and 1 TMS

TonB of Acidobacterium capsulatum

 
2.C.1.1.7

TonB of 248 aas and 1 TMS

TonB of Granulicella tundricola

 
2.C.1.1.8

TonB of 359 aas and 1 N-terminal TMS

TonB of Acidobacterium capsulatum

 
2.C.1.1.9

TonB of 250 aas and 1 TMS

TonB of Chlamydia psittaci

 
Examples:

TC#NameOrganismal TypeExample
2.C.1.2.1

The TolA energy-transducing system. The H+-channel-forming TolQ/R proteins are listed under TC# 1.A.30.2.2.  Proteins of the complex listed here are TolA, TolB, YbgF and Pal.  They play a role in outer membrane stabilization and uptake of colicins, but not energizaton of outer membrane receptors (OMRs: TC# 1.B.14).  May function in phospholipid transport (SS Chng, personal communication).  Cells lacking the Tol-Pal complex exhibit defects in lipid asymmetry and accumulate excess phospholipids (PLs) in the OM. This imbalance in OM lipids is due to defective retrograde PL transport in the absence of a functional Tol-Pal complex. Thus, cells ensure the assembly of a stable OM by maintaining an excess flux of PLs to the OM only to return the surplus to the inner membrane via transport mediated by the Tol-Pal complex (Shrivastava et al. 2017).  The specific function of the Tol-Pal complex may be to transport lipids from the outer leaflet of the outer membrane to the inner leaflet of the outer member. The Tol-Pal complex is essential to maintain polar localization of the MCP chemotaxis receptor complex (Santos et al. 2014). The Tol-Pal complex, energized by TolQRA, and using the outer membrane proteins, BtuB and OmpF as receptors, is responsible for the uptake of colicin ColE9 and other bacteriocins; in this process, the complex in the outer membrane bridges and immobilizes the complex components in the inner membrane (Rassam et al. 2018).

Gram-negative bacteria

The TolA/TolQR/Pal system of E. coli
TolB (P0A855)
TolA (P19934)
YbgF (P45955)
Pal (C6EJJ6)

 
2.C.1.2.2

Cell envelope energy-transducing integrity protein, TolA, of 421 aas. 

TolA of Pasteurella multocida

 
2.C.1.2.3

TolA of 356 aas and 1 N-terminal TMS

TolA of Vibrio cholerae

 
2.C.1.2.4

TolA of 371 aas

TolA of Gilliamella apicola

 
Examples:

TC#NameOrganismal TypeExample
2.C.1.3.1

TonB family protein, Slr1484, of 532 aas and 1 N-terminal TMS. Slr1484 had positive interactions with the three known ExbD proteins (Sll1405, Sll0479, and Slr0678) (Qiu et al. 2018).

Slr1484 of Synechocystis 6803

 
2.C.1.3.2

TonB family protein of 563 aas and 1 N-terminal TMS.

TonB of Phormidium ambiguum

 
2.C.1.3.3

TonB sfamily protein of 413 aas and 1 N-terminal TMS.

Ton B of Aphanothece hegewaldii

 
2.C.1.3.4

TonB family protein of 509 aas and 1 N-terminal TMS.

TonB of Leptolyngbya foveolarum

 
2.C.1.3.5

TonB of 410 aas and 1 N-terminal TMS.

TonB of Rubidibacter lacunae

 
2.C.1.3.6

TonB family protein of 512 aas and 1 N-terminla TMS. An uncharacterized constituent of a ferric siderophore transport system.

TonB of Chrysosporum ovalisporum

 
2.C.1.3.7

TonB energy transducer of 377 aas and 1 N-terminal TMS.

TonB of Acetobacter tropicalis

 
2.C.1.3.8

TonB family protein of 372 aas and 1 TM

TonB of Pirellula staleyi

 
Examples:

TC#NameOrganismal TypeExample
2.C.1.4.1

TonB-like protein of 280 aas and 1 N-terminal TMS. It interacts with outer membrane receptor proteins that carry out high-affinity binding and energy-dependent uptake into the periplasmic space of specific substrates. It could act to transduce energy from the cytoplasmic membrane to specific energy-requiring processes in the outer membrane, resulting in the release into the periplasm of ligands bound by these outer membrane proteins.

TonB of Bacteroides helcogenes

 
2.C.1.4.2

TonB protein of 271 aas and 1 N-terminal TMS

TonB of Bacteroides cellulosilyticus

 
2.C.1.4.3

TonB protein of 320 aas and 1 TMS

TonB of Bacteroides ovatus

 
2.C.1.4.4

TonB of 272 aas and 1 TMS

TonB of Flavobacterium psychrophilum