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. 1995 Apr 3;14(7):1430–1438. doi: 10.1002/j.1460-2075.1995.tb07129.x

Signal transfer through three compartments: transcription initiation of the Escherichia coli ferric citrate transport system from the cell surface.

C Härle 1, I Kim 1, A Angerer 1, V Braun 1
PMCID: PMC398229  PMID: 7729419

Abstract

Transport of ferric citrate into cells of Escherichia coli K-12 involves two energy-coupled transport systems, one across the outer membrane and one across the cytoplasmic membrane. Previously, we have shown that ferric citrate does not have to enter the cytoplasm of E. coli K-12 to induce transcription of the fec ferric citrate transport genes. Here we demonstrate that ferric citrate uptake into the periplasmic space between the outer and the cytoplasmic membranes is not required for fec gene induction. Rather, FecA and the TonB, ExbB and ExbD proteins are involved in induction of the fec transport genes independent of their role in ferric citrate transport across the outer membrane. The uptake of ferric citrate into the periplasmic space of fecA and tonB mutants via diffusion through the porin channels did not induce transcription of fec transport genes. Point mutants in FecA displayed the constitutive expression of fec transport genes in the absence of ferric citrate but still required TonB, with the exception of one FecA mutant which showed a TonB-independent induction. The phenotype of the FecA mutants suggests a signal transduction mechanism across three compartments: the outer membrane, the periplasmic space and the cytoplasmic membrane. The signal is triggered upon the interaction of ferric citrate with FecA protein. It is postulated that FecA, TonB, ExbB and ExbD transfer the signal across the outer membrane, while the regulatory protein FecR transmits the signal across the cytoplasmic membrane to FecI in the cytoplasm. FecI serves as a sigma factor which facilitates binding of the RNA polymerase to the fec transport gene promoter upstream of fecA.(ABSTRACT TRUNCATED AT 250 WORDS)

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Selected References

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  1. Bradbeer C. The proton motive force drives the outer membrane transport of cobalamin in Escherichia coli. J Bacteriol. 1993 May;175(10):3146–3150. doi: 10.1128/jb.175.10.3146-3150.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Braun V., Herrmann C. 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. 1993 Apr;8(2):261–268. doi: 10.1111/j.1365-2958.1993.tb01570.x. [DOI] [PubMed] [Google Scholar]
  3. Chang A. C., Cohen S. N. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978 Jun;134(3):1141–1156. doi: 10.1128/jb.134.3.1141-1156.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Frost G. E., Rosenberg H. The inducible citrate-dependent iron transport system in Escherichia coli K12. Biochim Biophys Acta. 1973 Nov 30;330(1):90–101. doi: 10.1016/0005-2736(73)90287-3. [DOI] [PubMed] [Google Scholar]
  5. Giacomini A., Corich V., Ollero F. J., Squartini A., Nuti M. P. Experimental conditions may affect reproducibility of the beta-galactosidase assay. FEMS Microbiol Lett. 1992 Dec 15;100(1-3):87–90. doi: 10.1111/j.1574-6968.1992.tb14024.x. [DOI] [PubMed] [Google Scholar]
  6. Günter K., Braun V. In vivo evidence for FhuA outer membrane receptor interaction with the TonB inner membrane protein of Escherichia coli. FEBS Lett. 1990 Nov 12;274(1-2):85–88. doi: 10.1016/0014-5793(90)81335-l. [DOI] [PubMed] [Google Scholar]
  7. Güssow D., Clackson T. Direct clone characterization from plaques and colonies by the polymerase chain reaction. Nucleic Acids Res. 1989 May 25;17(10):4000–4000. doi: 10.1093/nar/17.10.4000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hantke K. Regulation of ferric iron transport in Escherichia coli K12: isolation of a constitutive mutant. Mol Gen Genet. 1981;182(2):288–292. doi: 10.1007/BF00269672. [DOI] [PubMed] [Google Scholar]
  9. Heller K. J., Kadner R. J., Günther K. 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. 1988 Apr 15;64(1):147–153. doi: 10.1016/0378-1119(88)90488-x. [DOI] [PubMed] [Google Scholar]
  10. Hussein S., Hantke K., Braun V. Citrate-dependent iron transport system in Escherichia coli K-12. Eur J Biochem. 1981 Jul;117(2):431–437. doi: 10.1111/j.1432-1033.1981.tb06357.x. [DOI] [PubMed] [Google Scholar]
  11. Kampfenkel K., Braun V. Membrane topology of the Escherichia coli ExbD protein. J Bacteriol. 1992 Aug;174(16):5485–5487. doi: 10.1128/jb.174.16.5485-5487.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kampfenkel K., Braun V. Topology of the ExbB protein in the cytoplasmic membrane of Escherichia coli. J Biol Chem. 1993 Mar 15;268(8):6050–6057. [PubMed] [Google Scholar]
  13. Killmann H., Benz R., Braun V. Conversion of the FhuA transport protein into a diffusion channel through the outer membrane of Escherichia coli. EMBO J. 1993 Aug;12(8):3007–3016. doi: 10.1002/j.1460-2075.1993.tb05969.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kohara Y., Akiyama K., Isono K. The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  15. Koster M., van Klompenburg W., Bitter W., Leong J., Weisbeek P. Role for the outer membrane ferric siderophore receptor PupB in signal transduction across the bacterial cell envelope. EMBO J. 1994 Jun 15;13(12):2805–2813. doi: 10.1002/j.1460-2075.1994.tb06574.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lugtenberg B., Meijers J., Peters R., van der Hoek P., van Alphen L. Electrophoretic resolution of the "major outer membrane protein" of Escherichia coli K12 into four bands. FEBS Lett. 1975 Oct 15;58(1):254–258. doi: 10.1016/0014-5793(75)80272-9. [DOI] [PubMed] [Google Scholar]
  17. Martinez E., Bartolomé B., de la Cruz F. pACYC184-derived cloning vectors containing the multiple cloning site and lacZ alpha reporter gene of pUC8/9 and pUC18/19 plasmids. Gene. 1988 Aug 15;68(1):159–162. doi: 10.1016/0378-1119(88)90608-7. [DOI] [PubMed] [Google Scholar]
  18. Ochs M., Veitinger S., Kim I., Welz D., Angerer A., Braun V. Regulation of citrate-dependent iron transport of Escherichia coli: fecR is required for transcription activation by FecI. Mol Microbiol. 1995 Jan;15(1):119–132. doi: 10.1111/j.1365-2958.1995.tb02226.x. [DOI] [PubMed] [Google Scholar]
  19. Postle K., Skare J. T. Escherichia coli TonB protein is exported from the cytoplasm without proteolytic cleavage of its amino terminus. J Biol Chem. 1988 Aug 5;263(22):11000–11007. [PubMed] [Google Scholar]
  20. Pressler U., Staudenmaier H., Zimmermann L., Braun V. Genetics of the iron dicitrate transport system of Escherichia coli. J Bacteriol. 1988 Jun;170(6):2716–2724. doi: 10.1128/jb.170.6.2716-2724.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rutz J. M., Liu J., Lyons J. A., Goranson J., Armstrong S. K., McIntosh M. A., Feix J. B., Klebba P. E. Formation of a gated channel by a ligand-specific transport protein in the bacterial outer membrane. Science. 1992 Oct 16;258(5081):471–475. doi: 10.1126/science.1411544. [DOI] [PubMed] [Google Scholar]
  22. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schöffler H., Braun V. Transport across the outer membrane of Escherichia coli K12 via the FhuA receptor is regulated by the TonB protein of the cytoplasmic membrane. Mol Gen Genet. 1989 Jun;217(2-3):378–383. doi: 10.1007/BF02464907. [DOI] [PubMed] [Google Scholar]
  24. Skare J. T., Ahmer B. M., Seachord C. L., Darveau R. P., Postle K. Energy transduction between membranes. TonB, a cytoplasmic membrane protein, can be chemically cross-linked in vivo to the outer membrane receptor FepA. J Biol Chem. 1993 Aug 5;268(22):16302–16308. [PubMed] [Google Scholar]
  25. Soberon X., Covarrubias L., Bolivar F. Construction and characterization of new cloning vehicles. IV. Deletion derivatives of pBR322 and pBR325. Gene. 1980 May;9(3-4):287–305. doi: 10.1016/0378-1119(90)90328-o. [DOI] [PubMed] [Google Scholar]
  26. Staudenmaier H., Van Hove B., Yaraghi Z., Braun V. Nucleotide sequences of the fecBCDE genes and locations of the proteins suggest a periplasmic-binding-protein-dependent transport mechanism for iron(III) dicitrate in Escherichia coli. J Bacteriol. 1989 May;171(5):2626–2633. doi: 10.1128/jb.171.5.2626-2633.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stock J. B., Ninfa A. J., Stock A. M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol Rev. 1989 Dec;53(4):450–490. doi: 10.1128/mr.53.4.450-490.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Takeshita S., Sato M., Toba M., Masahashi W., Hashimoto-Gotoh T. High-copy-number and low-copy-number plasmid vectors for lacZ alpha-complementation and chloramphenicol- or kanamycin-resistance selection. Gene. 1987;61(1):63–74. doi: 10.1016/0378-1119(87)90365-9. [DOI] [PubMed] [Google Scholar]
  29. Van Hove B., Staudenmaier H., Braun V. Novel two-component transmembrane transcription control: regulation of iron dicitrate transport in Escherichia coli K-12. J Bacteriol. 1990 Dec;172(12):6749–6758. doi: 10.1128/jb.172.12.6749-6758.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wagegg W., Braun V. Ferric citrate transport in Escherichia coli requires outer membrane receptor protein fecA. J Bacteriol. 1981 Jan;145(1):156–163. doi: 10.1128/jb.145.1.156-163.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Zimmermann L., Hantke K., Braun V. Exogenous induction of the iron dicitrate transport system of Escherichia coli K-12. J Bacteriol. 1984 Jul;159(1):271–277. doi: 10.1128/jb.159.1.271-277.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]

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