Abstract
The TonB system of Escherichia coli (and most other Gram-negative bacteria) is distinguished by its importance to iron acquisition, its contribution to bacterial pathogenesis, and a unique and mysterious mechanism of action. This system somehow gathers the potential energy of the cytoplasmic membrane (CM) proton gradient and delivers it to active transporters in the outer membrane (OM). Our understanding of this system is confounded by the challenge of reconciling often contradictory in vivo and in vitro studies that are presented in this review.
Similar content being viewed by others
References
Bell PE, Nau CD, Brown JT, Konisky J, Kadner RJ (1990) Genetic suppression demonstrates direct interaction of TonB protein with outer membrane transport proteins in Escherichia coli. J Bacteriol 172:3826–3829
Blair DF (2003) Flagellar movement driven by proton translocation. FEBS Lett 545:86–95
Braun V (1989) The structurally related exbB and tolQ genes are interchangeable in conferring tonB-dependent colicin, bacteriophage, and albomycin sensitivity. J Bacteriol 171:6387–6390
Braun V, Herrmann C (1993) Evolutionary relationship of uptake systems for biopolymers in Escherichia coli: cross-complementation between the TonB-ExbB-ExbD and the TolA-TolQ-TolR proteins. Mol Microbiol 8:261–268
Braun V, Herrmann C (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, Gaisser S, Herrmann C, Kampfenkel K, Killman H, Traub I (1996) Energy-coupled transport across the outer membrane of Escherichia coli: ExbB binds ExbD and TonB in vitro, and leucine 132 in the periplasmic region and aspartate 25 in the transmembrane region are important for ExbD activity. J Bacteriol 178:2836–2845
Braun V, Patzer SI, Hantke K (2002) Ton-dependent colicins and microcins: modular design and evolution. Biochimie 84:365–380
Brewer S, Tolley M, Trayer IP, Barr GC, Dorman CJ, Hannavy K, Higgins CF, Evans JS, Levine BA, Wormald MW (1990) Structure and function of X-Pro dipeptide repeats in the TonB protein of Salmonella typhimurium and Escherichia coli. J Mol Biol 216:883–895
Cadieux N, Kadner RJ (1999) Site-directed disulfide bonding reveals an interaction site between energy-coupling protein TonB and BtuB, the outer membrane cobalamin transporter. Proc Natl Acad Sci USA 96:10673–10678
Carter DM, Gagnon JN, Damlaj M, Mandava S, Makowski L, Rodi DJ, Pawelek PD, Coulton JW (2006) Phage display reveals multiple contact sites between FhuA, an outer membrane receptor of Escherichia coli, and TonB. J Mol Biol 357:236–251
Cascales E, Lloubes R, Sturgis JN (2001) The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol 42:795–807
Chang C, Mooser A, Plückthun A, Wiodawer A (2001) Crystal structure of the dimeric carboxy-terminal domain of TonB reveals a novel fold. J Biol Chem 276:27535–27540
Chimento DP, Kadner RJ, Weiner MC (2005) Comparative structural analysis of TonB-dependent outer membrane transporters: implications for the transport cycle. Proteins 59:240–251
Evans JS, Levine BA, Trayer IP, Dorman CJ, Higgins CF (1986) Sequence-imposed structural constraints in the TonB protein of E. coli. FEBS Lett 208:211–216
Ferguson AD, Hofmann E, Coulton JW, Diederiche K, Welte W (1998) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215–2220
Ferguson AD, Chakraborty R, Smith BS, Esser L, van der Helm D, Deisenhofer J (2002) Structural basis of gating by the outer membrane transporter FecA. Science 295:1715–1719
Germon P, Ray MC, Vianney A, Lazzaroni J-C (2001) Energy-dependent conformational change in the TolA protein of Escherichia coli involves its amino-terminal domain, TolQ, and TolR. J Bacteriol 183:4110–4114
Ghosh J, Postle K (2004) Evidence for dynamic clustering of carboxy-terminal aromatic amino acids in TonB-dependent energy transduction. Mol Microbiol 51:203–213
Ghosh J, Postle K (2005) Disulphide trapping of an in vivo energy-dependent conformation of Escherichia coli TonB protein. Mol Microbiol 55:276–288
Gudmundsdottir A, Bell PE, Lundrigan MD, Bradbeer C, Kadner RJ (1989) Point mutations in a conserved region (TonB box) of Escherichia coli outer membrane protein BtuB affect vitamin B12 transport. J Bacteriol 171:6526–6533
Hannavy K, Barr GC, Dorman CJ, Adamson J, Mazengera LR, Gallagher MP, Evans JS, Levine BA, Trayer IP, Higgins CF (1990) TonB protein of Salmonella typhimurium. A model for signal transduction between membranes. J Mol Biol 216:897–910
Held KG, Postle K (2002) ExbB and ExbD do not function independently in TonB-dependent energy transduction. J Bacteriol 184:5170–5173
Heller K, Kadner RJ (1985) Nucleotide sequence of the gene for the vitamin B12 receptor protein in the outer membrane of Escherichia coli. J Bacteriol 161:904–908
Heller K, Kadner RJ, Günter K (1988) Suppression of the btuB451 mutation by mutations in the tonB gene suggests a direct interaction between TonB and TonB-dependent receptor proteins in the outer membrane of Escherichia coli. Gene 64:147–153
Heringa J (1999) Two strategies for sequence comparison: profile-preprocessed and secondary structure-induced multiple alignment. Computers Chem 23:341–364
Higgs PI, Myers PS, Postle K (1998) Interactions in the TonB-dependent energy transduction complex: ExbB and ExbD form homomultimers. J Bacteriol 180:6031–6038
Higgs PI, Larsen RA, Postle K (2002a) Quantification of known components of the Escherichia coli TonB-dependent energy transduction system: TonB, ExbB, ExbD, and FepA. Mol Microbiol 44:271–281
Howard SP, Herrmann C, Stratilo CW, Braun V (2001) In vivo synthesis of the periplasmic domain of TonB inhibits transport through the FecA and FhuA iron siderophore transporters of Escherichia coli. J Bacteriol 183:5885–5895
Jaskula JC, Letain TE, Roof SK, Skare JT, Postle K (1994) Role of the TonB amino terminus in energy transduction between membranes. J Bacteriol 176:2326–2338
Karlsson M, Hannavy K, Higgins CF (1993) A sequence-specific function for the amino-terminal signal-like sequence of the TonB protein. Mol Microbiol 8:379–388
Koebnik R (1993) The molecular interaction between components of the TonB-ExbBD-dependent and of the TolQRA-dependent bacterial uptake systems. Mol Microbiol 9:219
Ködding J, Howard SP, Kaufmann L, Potzer P, Lustig A, Welte W (2004) Dimerization of TonB is not essential for tis binding to the outer membrane siderophore receptor FhuA of Escherichia coli. J Biol Chem 279:9978–9986
Ködding J, Killig F, Polzer P, Howard SP, Diederichs K, Welte W (2005) Crystal structure of a 92-residue carboxy-terminal fragment of TonB from Escherichia coli reveals significant conformational changes compared to structures of smaller TonB fragments. J Biol Chem 280:3022–3028
Kojima S, Blair DF (2001) Conformational change in the stator of the bacterial flagellar motor. Biochemistry 40:13041–13050
Khursigara CM, De Crescenzo G, Pawelek PD, Coulton JW (2004) Enhanced binding of TonB to a ligand-loaded outer membrane receptor. Role of the oligomeric state of TonB in formation of a functional FhuA-TonB complex. J Biol Chem 279:7405–7412
Khursigara CM, De Crescenzo G, Pawelek PD, Coulton JW (2005b) Deletion of the proline-rich region of TonB disrupts formation of a 2:1 complex with FhuA, an outer membrane receptor of Escherichia coli. Protein Sci 14:1266–1273
Larsen RA, Postle K (2001) Conserved residues Ser(16) and His(20) and their relative positioning are essential for TonB activity, cross-linking of TonB with ExbB, and the ability of TonB to respond to proton motive force. J Biol Chem 276:8111–8117
Larsen RA, Wood GE, Postle K (1993) The conserved proline-rich motif is not essential for energy transduction by Escherichia coli TonB protein. Mol Microbiol 10:943–953
Larsen RA, Thomas MT, Wood GE, Postle K (1994) Partial suppression of an Escherichia coli TonB transmembrane domain mutation (δV17) by a missense mutation in ExbB. Mol Microbiol 13:627–640
Larsen RA, Foster-Hartnett D, McIntosh MA, Postle K (1997) Regions of Escherichia coli TonB and FepA proteins essential for in vivo physical interactions. J Bacteriol 179:3213–3221
Larsen RA, Thomas MG, Postle K (1999) Protonmotive force, ExbB and ligand-bound FepA drive conformational changes in TonB. Mol Microbiol 31:1809–1824
Larsen RA, Letain TE, Postle K (2003) In vivo evidence of TonB shuttling between the cytoplasmic and outer membrane in Escherichia coli. Mol Microbiol 49:211–218
Letain TE, Postle K (1997) TonB protein appears to transduce energy by shuttling between the cytoplasmic membrane and the outer membrane in Gram-negative bacteria. Mol Microbiol 24:271–283
Locher KP, Rees B, Koebnik R, Mitschler A, Moulinier l, Rosenbusch JP, Moras D (1998) Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771–778
Lubkowski J, Hennecke F, Plückthun A, Wlodawer A (1999) Filamentous phage infection: crystal structure of g3p in complex with its coreceptor, the carboxy-terminal domain of TolA. Structure 7:711–722
Mann BJ, Holroyd CD, Bradbeer C, Kadner RJ (1986) Reduced activity of TonB-dependent functions in strains of Escherichia coli. FEMS Lett 33:255–260
Mey AR, Payne SM (2003) Analysis of residues determining specificity of Vibrio cholerae TonB1 for its receptors. J Bacteriol 185:1195–1207
Neugebauer H, Herrmann C, Kammer W, Schwarz G, Nordheim A, Braun V (2005) ExbBD-dependent transport of maltodextrins through the novel MalA protein across the outer membrane of Caulobacter crescentus. J Bacteriol 187: 8300–8311
Pawelek PD, Croteau N, Ng-Thow-Hing C, Khursigara CM, Moiseeva N, Allaire M, Coulton JW (2006) Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312:1399–1402
Peacock RS, Weljie AM, Howard SP, Price FD, Vogel HJ (2005) The solution structure of the carboxy-terminal domain of TonB and interaction studies with TonB box peptides. J Mol Biol 345:1185–1197
Peacock RS, Andrushchenko VV, Demcoe AR, Gehmlich M, Lu LS, Herrero AG, Vogel HJ (2006) Characterization of TonB interactions with the FepA cork domain and FecA amino-terminal signaling domain. Biometals 19:127–142
Postle K, Good RF (1983) DNA sequence of the Escherichia coli tonB gene. Proc Natl Acad Sci USA 80:5235–5239
Postle K, Skare JT (1988) Escherichia coli TonB protein is exported from the cytoplasm without proteolytic cleavage of its amino terminus. J Biol Chem 263:11000–11007
Postle K, Kadner RJ (2003) Touch and go: tying TonB to transport. Mol Microbiol 49:869–882
Postle K, Larsen RA (2004) The TonB, ExbB, and ExbD proteins. In: Crosa JH, Mey AR, Payne SM (eds) Iron transport in bacteria. ASM Press, Washington, DC, pp 96–112
Pressler U, Staudenmaier H, Zimmermann L, Braun V (1988) Genetics of the iron dicitrate transport system of Escherichia coli. J Bacteriol 170:2716–2724
Roof SK, Allard JD, Bertrand KP, Postle K (1991) Analysis of Escherichia coli TonB membrane topology by use of PhoA fusions. J Bacteriol 173:5554–5557
Saier MH Jr (2000) A functional/phylogenetic classification system for transmembrane solute transporters. Microbiol Mol Biol Rev 64:351–411
Sauter A, Howard SP, Braun V (2003) In vivo evidence for TonB dimerization. J Bacteriol 185:5747–5754
Schöffler H, Braun V (1989) Transport across the outer membrane of Escherichia coli via the FhuA receptor is regulated by the TonB protein of the cytoplasmic membrane. Mol Gen Genet 217:378–383
Schramm E, Mende J, Braun V, Kamp RM (1987) Nucleotide sequence of the colicin B activity gene cba: consensus pentapeptide among TonB-dependent colicins and receptors. J Bacteriol 169:3350–3357
Seliger S, Mey A, Valle A, Payne S (2001) The two TonB systems of Vibrio cholerae: redundant and specific functions. Mol Microbiol 39:801–812
Shultis DD, Purdy MD, Banchs CN, Wiener MC (2006) Outer membrane active transport: structure of the BtuB:TonB complex. Science 312:1396–1399
Simossis VA, Kleinjung J, Heringa J (2005) Homology-extended sequence alignment. Nucleic Acids Res 33:816–824
Skare JT, Roof SK, Postle K (1989) A mutation in the amino terminus of a hybrid TrpC-TonB protein relieves overproduction lethality and results in cytoplasmic accumulation. J Bacteriol 171:4442–4447
Traub I, Gaisser S, Braun V (1993) Activity domains of the TonB protein. Mol Microbiol 8:409–423
Tuckman M, Osburne MS (1992) In vivo inhibition of TonB-dependent processes by a TonB box consensus pentapeptide. J Bacteriol 174:320–323
Weiner MC (2005) TonB-dependent outer membrane transport: going for Baroque? Curr Opin Struct Biol 15: 394–400
Witty M, Sanz C, Shah A, Grossmann JG, Mizuguchi K, Perham RN, Luisi B (2002) Structure of the periplasmic domain of Pseudomonas aeruginosa TolA: evidence for an evolutionary relationship with the TonB transporter protein. EMBO J 21:4207–4218
Zhai YF, Heijne W, Saier MH 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
Acknowledgments
The authors are grateful for awards from the National Institutes of General Medical Sciences (to K. P.) and the National Science Foundation (to R. L.), and thank Dick van der Helm for very helpful discussions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Postle, K., Larsen, R.A. TonB-dependent energy transduction between outer and cytoplasmic membranes. Biometals 20, 453–465 (2007). https://doi.org/10.1007/s10534-006-9071-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10534-006-9071-6