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Chapter 16 : Transfer of Energy and Information across the Periplasm in Iron Transport and Regulation
Authors:
Volkmar Braun1,
Susanne Mahren2
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Affiliations:
1: Mikrobiologie/Membranphysiologie, Auf der Morgenstelle 28, D-72076 Tübingen, Germany;
2: Mikrobiologie/Membranphysiologie, Auf der Morgenstelle 28, D-72076 Tübingen, Germany
Content Type: Monograph
Publication Year:
2007
Category: Bacterial Pathogenesis; Microbial Genetics and Molecular Biology
Book DOI:
10.1128/9781555815806
Chapter DOI:
10.1128/9781555815806.ch16
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Transfer of Energy and Information across the Periplasm in Iron Transport and Regulation, Page 1 of 2
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Abstract:
Two periplasmic functions are discussed in this chapter: (i) the transfer of energy from the cytoplasmic membrane across the periplasm to the outer membrane, and (ii) the transfer of information from the outer membrane across the periplasm through the cytoplasmic membrane into the cytoplasm. To enter gram-negative bacteria, substrates must cross three compartments: the outer membrane, the periplasm, and the cytoplasmic membrane. Most substrates diffuse through outer membrane porins into the periplasm and then are actively transported, i.e., with energy coupling, across the cytoplasmic membrane. Early studies have demonstrated that TonB is involved in iron transport and that the proton motive force serves as energy source for TonB-dependent processes. It is currently impossible to decide whether the various results reflect different TonB states during the reaction cycle—energization, deenergization, interaction with ExbB and ExbD within the cytoplasmic membrane and the periplasm, and binding to and release from transporters—or whether some results are experimental artifacts caused in vitro by the use of truncated forms that lack the N-terminal membrane anchor, which is essential for TonB activity. The periplasm—once considered not more than a space between the outer membrane and the cytoplasmic membrane—is now known to be a compartment through which energy and information flow. Understanding of the underlying mechanisms will require much sophisticated work since the three compartments cannot be taken apart without loss of essential aspects of periplasmic functions.
Citation:
Braun V, Mahren S.
2007.
Transfer of Energy and Information across the Periplasm in Iron Transport and Regulation,
p 276-286.
In
Ehrmann M (ed),
The Periplasm.
ASM Press, Washington, DC.
doi: 10.1128/9781555815806.ch16
Key Concept Ranking
- Outer Membrane Proteins
- 0.625673
- Aromatic Amino Acids
- 0.46041155
- Transcription Initiation
- 0.41764078
0.625673
References
/content/book/10.1128/9781555815806.ch16
1.
Angerer, A., and, V. Braun. 1998. Iron regulates transcription of the Escherichia coli ferric citrate transport genes directly and through the transcription initiation proteins. Arch. Microbiol. 169: 483– 490.
2.
Angerer, A.,, S. Enz,, M. Ochs, and, V. Braun. 1995. Transcriptional regulation of ferric citrate transport in Escherichia coli K-12. FecI belongs to a new subfamily of a 70-type factors that respond to extracytoplasmic stimuli. Mol. Microbiol. 18: 163– 174.
3.
Braun, V., 1997. Surface signaling: novel transcription initiation mechanism string from the cell surface. Arch. Microbiol. 167: 325– 331.
4.
Braun, V., and, C. Herrmann. 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.
5.
Braun, V., and, S. Mahren. 2005. Transmembrane transcriptional control (surface signalling) of the Escherichia coli Fec type. FEMS Microbiol. Rev. 29: 673– 684.
6.
Braun, V.,, S. Mahren, and, M. Ogierman. 2003. Regulation of the FecI-type ECF sigma factor by transmembrane signalling. Curr. Opin. Microbiol. 6: 173– 180.
7.
Bradbeer, C., 1993. The proton motive force drives the outer membrane transport of cobalamin in Escherichia coli.J. Bacteriol. 175: 3146– 3150.
8.
Brito B.,, D. Aldon,, P. Barberis,, C. Boucher, and, S. Genin. 2002. A signal transfer system through three compartments transduces the plant cell contact–dependent signal controlling Ralstonia solanacearum hrp genes .Mol. Plant. Microb. Interact. 15: 109– 119
9.
Buchanan, S. K.,, B. S. Smith,, L. Venkatramani,, D. Xia,, L. Esser,, M. Palnitkar,, R. Chakraborty,, D. van der Helm, and, J. Deisenhofer. 1999. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nature Struct. Biol. 6: 56– 63.
10.
Cadieux, N., and, R. J. Kadner. 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.
11.
Campbell, E. A.,, J. L. Tupy,, T. M. Gruber,, S. Wang,, M. M. Shatrp,, C. A. Gross, and, S. A. Darst. 2003. Crystal structure of Escherichia coli σ E with the cytoplasmic domain of its anti-σ RseA. Mol. Cell 11: 1067– 1078.
12.
Cao, Z.,, P. Warfel,, S. M. C. Newton, and, P. E. Klebba. 2003. Spectroscopic observations of ferric enterobactin transport. J. Biol. Chem. 278: 1022– 1028.
13.
Chimento, D. P.,, R. J. Kadner, and, M. C. Wiener. 2005. Comparative structural analysis of TonBdependent outer membrane transporters: implications for the transport cycle .Proteins 59: 240– 251.
14.
Chimento, D. P.,, A. K. Mohanty,, R. J. Kadner, and, M. C. Wiener. 2003. Substrate–induced trans-membrane signaling in the cobalamin transporter BtuB .Nature Struct. Biol. 10: 394– 401.
15.
Cobessi, D.,, H. Celia,, N. Folschweiller,, I. Schalk,, M. Abdallah, and, F. Pattus. 2005a. The crystal structure of the pyoverdine outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 A resolution. J. Mol. Biol. 347: 121– 134.
16.
Cobessi, D.,, H. Celia, and, F. Pattus. 2005b. Crystal structure at high resolution of ferric-pyochelin and its membrane receptor FptA from Pseudomonas aeruginosa.J. Mol. Biol. 347: 121– 134.
17.
Crosa, J. H.,, A. R. Mey, and, S. M. Payne (ed.)., 2004. Iron Transport in Bacteria. ASM Press, Washington, D.C.
18.
Eisenhauer, H. A.,, S. Shames,, P. D. Pawelek, and, J. W. Coulton. 2005. Siderophore transport through Escherichia coli outer membrane receptor FhuA with disulfide-tethered cork and barrel domains. J. Biol. Chem. 280: 30574– 30580.
19.
Endrip, F.,, M. Braun,, H. Killmann, and, V. Braun. 2003. Mutant analysis of the Escherichia coli FhuA protein reveals sites of FhuA activity. J. Bacteriol. 185: 4683– 4692.
20.
Enz, S.,, H. Brand,, C. Orellana,, S. Mahren, and, V. Braun. 2003. Sites of interaction between the FecA and FecR signal transduction proteins of ferric citrate transport in Escherichia coli K-12. J. Bacteriol. 185: 3745– 3752.
21.
Enz, S.,, V. Braun, and, J. H. Crosa. 1995. Transcription of the region encoding the ferric dicitratetransport system in Escherichia coli: similarity between promoters for fecA and for extracytoplasmic function sigma factors. Gene 163: 13– 18.
22.
Enz, S.,, S. Mahren,, U. H. Stroeher, and, V. Braun. 2000. Surface signaling in ferric citrate transport gene induction: interaction of the FecA, FecR, and FecI regulatory proteins. J. Bacteriol. 182: 637– 646.
23.
Faraldo-Gomez, J. D.,, G. R. Smith, and, M. S. P. Sansom. 2003. Molecular dynamics simulations of the bacterial outer membrane protein FhuA: a comparative study of the ferrichrome-free and bound states. Biophys.J. 85: 1406– 1420.
24.
Ferguson, A. D.,, E. Hofmann,, J. W. Coulton,, K. Diederichs, and, W. Welte. 1998. Siderophoremediated iron transport: crystal structure of FhuA with bound lipopolysaccharide .Science 282: 2215– 2220.
25.
Ferguson, A. D.,, R. Chakraborty,, B. S. Smith,, L. Esser,, D. van der Helm, and, J. Deisenhofer. 2002. Structural basis of gating by the outer membrane transporter FecA. Science 295: 1715– 1719.
26.
Garcia-Herrero, A., and, H. J. Vogel. 2005. NMR solution structure of the periplasmic signaling domain of the TonB-dependent outer membrane transporter FecA .Mol. Microbiol. 58: 1226– 1237.
27.
Ghosh, J., and, K. Postle. 2005. Disulphide trapping of an in vivo energy-dependent conformation of Escherichia coli TonB protein .Mol. Microbiol. 55: 276– 288.
28.
Harle, C.,, K. Insook,, A. Angerer, and, V. Braun. 1995. Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface. EMBO J. 14: 1430– 1438.
29.
Hancock, R. E. W., and, V. Braun. 1976. Nature of the energy requirement for the irreversible adsorption of bacteriophages T1 and <J> 80 to Escherichia coli. J. Bacteriol. 125: 409– 415.
30.
Helmann, J. D., 2002. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46: 47– 110.
31.
James, E. H.,, P. A. Beare,, L. W. Martin, and, I. L. Lamont. 2005. Mutational anlysisis of a bifunctional ferrisiderophore receptor and signal-transducing protein from Pseudomonas aeruginosa. J. Bac-teriol .187: 4514– 4520.
32.
Khursigara, C. M.,, G. De Grescenco,, P. D. Pawelek, and, J. W. Coulton. 2005a. Kinetic analyses reveal multiple steps in forming TonBFhuA complexes from Escherichia coli. Biochemistry 44: 3441– 3453.
33.
Khursigara, C. M.,, G. De Grescenco,, P. D. Pawelek, and, J. W. Coulton. 2005b. Deletion of 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.
34.
Kim, I.,, A. Stiefel,, S. Plantor,, A. Angerer, and, V. Braun. 1997. Transcription induction of the ferric citrate transport genes via the N-terminus of the FecA outer membrane protein, the Ton system and the electrochemical potential of the cytoplasmic membrane. Mol. Microbiol. 23: 333– 344.
35.
Kirby A. E.,, N. D. King, and, T. D. Connell. 2004. RhuR, an extracytoplasmic function sigma factor activator, is essential for heme-dependent expression of the outer membrane heme and hemoprotein receptor of Bordetella avium. Infect. Immun. 72: 896– 907.
36.
Koebnik, R., 2005. TonB-dependent trans-envelope signalling: the exception or the rule? Trends Microbiol. 13: 343– 347.
37.
Koedding, J.,, P. Howard,, L. Kaufmann,, P. Polzer,, A. Lustig, and, W. Welte. 2004. Dimerization of TonB is not essential for its binding the outer membrane siderophore receptor FhuA of Escherichia coli. J. Biol. Chem. 279: 9978– 9986.
38.
Koster, M.,, W. van Klompenburg,, W. Bitter,, J. Leong, and, P. Weisbeek. 1994. Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope. EMBO J. 13: 2805– 2813.
39.
Larsen, R. A.,, T. E. Letain, and, K. Postle. 2003. In vivo evidence of TonB shuttling between the cytoplasmic and outer membrane in Escherichia coli. Mol. Microbiol. 49: 211– 218.
40.
Letain T. E., and, K. Postle. 1997. TonB protein appears to transducer energy by shuttling between the cytoplasmic membrane and the outer membrane in Escherichia coli. Mol. Microbiol. 24: 271– 283.
41.
Letoffe S.,, K. Wecker,, M. Delepelaire,, P. Delepelaire, and, C. Wandersman. 1999. Interactions of HasA, a bacterial hemophore, with hemoglobin and with its outer membrane receptor HasR. Mol. Microbiol. 33: 564– 555.
42.
Locher, K. P.,, B. Rees,, R. Koebnik,, A. Mitschler,, L. Moulinier,, J. P. Rosenbusch, and, D. Moras. 1998. Transmembrane signaling across the ligandgated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95: 771– 778.
43.
Luck S.,, S. A. Turner,, K. Rajakumar,, H. Sakellaris, and, B. Adler. 2001. Ferric dicitrate transport system (Fec) of Shigella flexneri 2a YSH6000 is encoded on a novel pathogenicity island carrying multiple antibiotic resistance genes. Infect. Immun. 69: 6012– 6021.
44.
Mahren, S. , and, V. Braun. 2003. The FecI extracytoplasmic–function sigma factor of Escherichia coli interacts with the β’ subunit of RNA polymerase. J. Bacteriol .185: 1796– 1802.
45.
Mahren, S.,, H. Schnell, and, V. Braun. 2005. Occurrence and regulation of the ferric citrate transport system in Escherichia coli B, Klebsiella pneumoniae, Enterobacter aerogenes and Photorhabdus luminescens. Arch. Microbiol. 184: 175– 186.
46.
Martinez-Bueno, M. A.,, R. Tobes,, M. Rey, and, J. l. Ramos. 2002. Detection of multiple extracytoplasmic function (ECF) sigma factors in the genome of Pseudomonas putida KT2440 and their counterparts in Pseudomonas aeruginosa.PAO1 .Envi-ron. Microbiol. 4: 842– 855.
47.
Neugebauer, H.,, C. Herrmann,, W. Kammer,, G. Schwarz,, A. Nordheim, and, V. Braun. 2005. ExbBD-dependent transport of maltodextrins through the novel MalA protein across the outer membrane of Caulobacter crescentus. J. Bacteriol. 187: 8300– 8311.
48.
Ochs, M.,, A. Angerer,, S. Enz, and, V. Braun. 1996. Surface signaling in transcriptional regulation of the ferric citrate transport system of Escherichia coli:mu-tational analysis of the alternative sigma factor FecI supports its essential role in fec transport gene transcription .Mol. Gen. Genet. 250: 455– 456.
49.
Ogierman, M., and, V. Braun. 2003. Interactions between the outer membrane ferric citrate transporter FecA and TonB: Studies of the FecA TonB box .J. Bacteriol .185: 1870– 1885.
50.
Peacock, P. S.,, A. M. Weljie,, S. P. Howard,, F. D. Price, and, H. J. Vogel. 2004. The solution structure of the C-terminal domain of TonB and interaction studies with TonB box peptides. J. Mol. Biol. 345: 1185– 1197.
51.
Postle, K., and, R. J. Kadner. 2003. Touch and go:tying TonB to transport. Mol. Microbiol. 49: 869– 882.
52.
Pradel, E., and, C. Locht. 2001. Expression of the putative siderophore receptor gene bfrZ is controlled by the extracytoplasmic-function sigma factor BupI in Bordetella bronchiseptica. J. Bacteriol. 183: 2910– 2917.
53.
Redly, G. A., and, K. Poole. 2005. FpvIR control of fpvA pyoverdine receptor gene expression in Pseudomonas aeruginosa: demonstration of an interaction between FpvI and FpvR and identification of mutations in each compromising this interaction. J. Bacteriol. 187: 5648– 5657.
54.
Rossi, M. S.,, A. Paquelin,, J. M. Ghigo, and, C. Wandersman. 2003. Haemophore-mediated signal transduction across the bacterial cell envelope in Serratia marcescens: the inducer and the transported substrate are different molecules. Mol. Microbiol. 48: 1467– 1480.
55.
Sauter, A.,, S. P. Howard, and, V. Braun. 2003. In vivo evidence for TonB dimerization. J. Bacteriol. 185: 5747– 5754.
56.
Scott, D. C.,, Z. Cao,, Z. Qi,, M. Bauler,, J. D. Igo,, S. M. C. Salete, and, P. E. Klebba. 2001. Exchangeability of N-termini in the ligand-gated porins of Escherichia coli.J. Biol. Chem. 276: 13025– 13033.
57.
Shen, J.,, A. Meldrum, and, K. Poole. 2002. FpvA receptor involvement in pyoverdine biosynthesis in Pseudomonas aeruginosa. J. Bacteriol. 184:3268–3275.
58.
Wandersman, C., and, P. Delepelaire. 2004. Bacterial iron sources:from siderophores to hemophores. Annu. Rev. Microbiol. 58: 611– 647.
59.
Wang, C. C., and, A. Newton. 1971. An additional step in the transport of iron defined by the tonB locus of Escherichia coli.J. Biol. Chem. 246: 2147– 2151.
60.
Yue, W. W.,, S. Grizot, and, S. K. Buchanan. 2003. Structural evidence for iron-free citrate and ferric citrate binding to the TonB-dependent outer membrane transporter FecA .J. Mol. Biol. 332: 353– 368.
61.
Xu, J.,, M. K. Bjursell,, J. Himrod,, S. Deng,, L. K. Carmichael,, H. C. Chiang,, L. V. Hooper, and, J. I. Gordon. 2003. A genomic view of the human Bacteroides thetaiotaomicron symbiosis. Science 299: 2074– 2076.