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. 1996 Feb;178(4):1227–1231. doi: 10.1128/jb.178.4.1227-1231.1996

Analysis of the Erwinia chrysanthemi ferrichrysobactin receptor gene: resemblance to the Escherichia coli fepA-fes bidirectional promoter region and homology with hydroxamate receptors.

C Sauvage 1, T Franza 1, D Expert 1
PMCID: PMC177792  PMID: 8576065

Abstract

The fct cbsCEBA operon from the Erwinia chrysanthemi 3937 chrysobactin-dependent iron assimilation system codes for transport and biosynthetic functions. The sequence of the fct outer membrane receptor gene was determined. The fct promoter region displays a strong resemblance to the Escherichia coli bidirectional intercistronic region controlling the expression of the fepA-entD and fes-entF operons. An apparent Fur-binding site was shown to confer iron regulation on an fct::lac fusion expressed on a low-copy-number plasmid in a Fur-proficient E. coli strain. The fct gene consists of an open reading frame encoding a 735-amino-acid polypeptide with a signal sequence of 38 residues. The Fct protein has 36% sequence homology with the E. coli ferrichrome receptor FhuA and the Yersinia enterocolitica ferrioxamine receptor FoxA. On the basis of secondary-structure predictions and these homologies, we propose a two-dimensional folding model for Fct.

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Selected References

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  1. Ankenbauer R. G., Quan H. N. FptA, the Fe(III)-pyochelin receptor of Pseudomonas aeruginosa: a phenolate siderophore receptor homologous to hydroxamate siderophore receptors. J Bacteriol. 1994 Jan;176(2):307–319. doi: 10.1128/jb.176.2.307-319.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armstrong S. K., Francis C. L., McIntosh M. A. Molecular analysis of the Escherichia coli ferric enterobactin receptor FepA. J Biol Chem. 1990 Aug 25;265(24):14536–14543. [PubMed] [Google Scholar]
  3. Bagg A., Neilands J. B. Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol Rev. 1987 Dec;51(4):509–518. doi: 10.1128/mr.51.4.509-518.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bäumler A. J., Hantke K. Ferrioxamine uptake in Yersinia enterocolitica: characterization of the receptor protein FoxA. Mol Microbiol. 1992 May;6(10):1309–1321. doi: 10.1111/j.1365-2958.1992.tb00852.x. [DOI] [PubMed] [Google Scholar]
  5. Carmel G., Coulton J. W. Internal deletions in the FhuA receptor of Escherichia coli K-12 define domains of ligand interactions. J Bacteriol. 1991 Jul;173(14):4394–4403. doi: 10.1128/jb.173.14.4394-4403.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carmel G., Hellstern D., Henning D., Coulton J. W. Insertion mutagenesis of the gene encoding the ferrichrome-iron receptor of Escherichia coli K-12. J Bacteriol. 1990 Apr;172(4):1861–1869. doi: 10.1128/jb.172.4.1861-1869.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Charbit A., Ronco J., Michel V., Werts C., Hofnung M. Permissive sites and topology of an outer membrane protein with a reporter epitope. J Bacteriol. 1991 Jan;173(1):262–275. doi: 10.1128/jb.173.1.262-275.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chou P. Y., Fasman G. D. Prediction of protein conformation. Biochemistry. 1974 Jan 15;13(2):222–245. doi: 10.1021/bi00699a002. [DOI] [PubMed] [Google Scholar]
  9. Coulton J. W., Mason P., Cameron D. R., Carmel G., Jean R., Rode H. N. Protein fusions of beta-galactosidase to the ferrichrome-iron receptor of Escherichia coli K-12. J Bacteriol. 1986 Jan;165(1):181–192. doi: 10.1128/jb.165.1.181-192.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dessen P., Fondrat C., Valencien C., Mugnier C. BISANCE: a French service for access to biomolecular sequence databases. Comput Appl Biosci. 1990 Oct;6(4):355–356. doi: 10.1093/bioinformatics/6.4.355. [DOI] [PubMed] [Google Scholar]
  11. Expert D., Sauvage C., Neilands J. B. Negative transcriptional control of iron transport in Erwinia chrysanthemi involves an iron-responsive two-factor system. Mol Microbiol. 1992 Jul;6(14):2009–2017. doi: 10.1111/j.1365-2958.1992.tb01373.x. [DOI] [PubMed] [Google Scholar]
  12. Franza T., Enard C., van Gijsegem F., Expert D. Genetic analysis of the Erwinia chrysanthemi 3937 chrysobactin iron-transport system: characterization of a gene cluster involved in uptake and biosynthetic pathways. Mol Microbiol. 1991 Jun;5(6):1319–1329. doi: 10.1111/j.1365-2958.1991.tb00778.x. [DOI] [PubMed] [Google Scholar]
  13. Franza T., Expert D. The virulence-associated chrysobactin iron uptake system of Erwinia chrysanthemi 3937 involves an operon encoding transport and biosynthetic functions. J Bacteriol. 1991 Nov;173(21):6874–6881. doi: 10.1128/jb.173.21.6874-6881.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Garnier J., Osguthorpe D. J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J Mol Biol. 1978 Mar 25;120(1):97–120. doi: 10.1016/0022-2836(78)90297-8. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Hunt M. D., Pettis G. S., McIntosh M. A. Promoter and operator determinants for fur-mediated iron regulation in the bidirectional fepA-fes control region of the Escherichia coli enterobactin gene system. J Bacteriol. 1994 Jul;176(13):3944–3955. doi: 10.1128/jb.176.13.3944-3955.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jeanteur D., Lakey J. H., Pattus F. The bacterial porin superfamily: sequence alignment and structure prediction. Mol Microbiol. 1991 Sep;5(9):2153–2164. doi: 10.1111/j.1365-2958.1991.tb02145.x. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Killmann H., Braun V. An aspartate deletion mutation defines a binding site of the multifunctional FhuA outer membrane receptor of Escherichia coli K-12. J Bacteriol. 1992 Jun;174(11):3479–3486. doi: 10.1128/jb.174.11.3479-3486.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Koebnik R., Braun V. Insertion derivatives containing segments of up to 16 amino acids identify surface- and periplasm-exposed regions of the FhuA outer membrane receptor of Escherichia coli K-12. J Bacteriol. 1993 Feb;175(3):826–839. doi: 10.1128/jb.175.3.826-839.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Koebnik R., Hantke K., Braun V. The TonB-dependent ferrichrome receptor FcuA of Yersinia enterocolitica: evidence against a strict co-evolution of receptor structure and substrate specificity. Mol Microbiol. 1993 Feb;7(3):383–393. doi: 10.1111/j.1365-2958.1993.tb01130.x. [DOI] [PubMed] [Google Scholar]
  22. Liu J., Rutz J. M., Feix J. B., Klebba P. E. Permeability properties of a large gated channel within the ferric enterobactin receptor, FepA. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10653–10657. doi: 10.1073/pnas.90.22.10653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Mahé B., Masclaux C., Rauscher L., Enard C., Expert D. Differential expression of two siderophore-dependent iron-acquisition pathways in Erwinia chrysanthemi 3937: characterization of a novel ferrisiderophore permease of the ABC transporter family. Mol Microbiol. 1995 Oct;18(1):33–43. doi: 10.1111/j.1365-2958.1995.mmi_18010033.x. [DOI] [PubMed] [Google Scholar]
  24. Moeck G. S., Bazzaz B. S., Gras M. F., Ravi T. S., Ratcliffe M. J., Coulton J. W. Genetic insertion and exposure of a reporter epitope in the ferrichrome-iron receptor of Escherichia coli K-12. J Bacteriol. 1994 Jul;176(14):4250–4259. doi: 10.1128/jb.176.14.4250-4259.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Murphy C. K., Kalve V. I., Klebba P. E. Surface topology of the Escherichia coli K-12 ferric enterobactin receptor. J Bacteriol. 1990 May;172(5):2736–2746. doi: 10.1128/jb.172.5.2736-2746.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ozenberger B. A., Brickman T. J., McIntosh M. A. Nucleotide sequence of Escherichia coli isochorismate synthetase gene entC and evolutionary relationship of isochorismate synthetase and other chorismate-utilizing enzymes. J Bacteriol. 1989 Feb;171(2):775–783. doi: 10.1128/jb.171.2.775-783.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Persmark M., Expert D., Neilands J. B. Isolation, characterization, and synthesis of chrysobactin, a compound with siderophore activity from Erwinia chrysanthemi. J Biol Chem. 1989 Feb 25;264(6):3187–3193. [PubMed] [Google Scholar]
  28. Pettis G. S., Brickman T. J., McIntosh M. A. Transcriptional mapping and nucleotide sequence of the Escherichia coli fepA-fes enterobactin region. Identification of a unique iron-regulated bidirectional promoter. J Biol Chem. 1988 Dec 15;263(35):18857–18863. [PubMed] [Google Scholar]
  29. Rose R. E. The nucleotide sequence of pACYC184. Nucleic Acids Res. 1988 Jan 11;16(1):355–355. doi: 10.1093/nar/16.1.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rutz J. M., Abdullah T., Singh S. P., Kalve V. I., Klebba P. E. Evolution of the ferric enterobactin receptor in gram-negative bacteria. J Bacteriol. 1991 Oct;173(19):5964–5974. doi: 10.1128/jb.173.19.5964-5974.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. Sauer M., Hantke K., Braun V. Sequence of the fhuE outer-membrane receptor gene of Escherichia coli K12 and properties of mutants. Mol Microbiol. 1990 Mar;4(3):427–437. doi: 10.1111/j.1365-2958.1990.tb00609.x. [DOI] [PubMed] [Google Scholar]
  33. Schiltz E., Kreusch A., Nestel U., Schulz G. E. Primary structure of porin from Rhodobacter capsulatus. Eur J Biochem. 1991 Aug 1;199(3):587–594. doi: 10.1111/j.1432-1033.1991.tb16158.x. [DOI] [PubMed] [Google Scholar]
  34. Simon R., Quandt J., Klipp W. New derivatives of transposon Tn5 suitable for mobilization of replicons, generation of operon fusions and induction of genes in gram-negative bacteria. Gene. 1989 Aug 1;80(1):161–169. doi: 10.1016/0378-1119(89)90262-x. [DOI] [PubMed] [Google Scholar]
  35. Struyvé M., Moons M., Tommassen J. Carboxy-terminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol. 1991 Mar 5;218(1):141–148. doi: 10.1016/0022-2836(91)90880-f. [DOI] [PubMed] [Google Scholar]
  36. Uzan M., Favre R., Brody E. A nuclease that cuts specifically in the ribosome binding site of some T4 mRNAs. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8895–8899. doi: 10.1073/pnas.85.23.8895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Vogel H., Jähnig F. Models for the structure of outer-membrane proteins of Escherichia coli derived from raman spectroscopy and prediction methods. J Mol Biol. 1986 Jul 20;190(2):191–199. doi: 10.1016/0022-2836(86)90292-5. [DOI] [PubMed] [Google Scholar]
  38. Weiss M. S., Abele U., Weckesser J., Welte W., Schiltz E., Schulz G. E. Molecular architecture and electrostatic properties of a bacterial porin. Science. 1991 Dec 13;254(5038):1627–1630. doi: 10.1126/science.1721242. [DOI] [PubMed] [Google Scholar]
  39. de Lorenzo V., Wee S., Herrero M., Neilands J. B. Operator sequences of the aerobactin operon of plasmid ColV-K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol. 1987 Jun;169(6):2624–2630. doi: 10.1128/jb.169.6.2624-2630.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. von Heijne G. A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 1986 Jun 11;14(11):4683–4690. doi: 10.1093/nar/14.11.4683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. von Heijne G., Manoil C. Membrane proteins: from sequence to structure. Protein Eng. 1990 Dec;4(2):109–112. doi: 10.1093/protein/4.2.109. [DOI] [PubMed] [Google Scholar]

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