The ferrichrome uptake pathway in Pseudomonas aeruginosa involves an iron release mechanism with acylation of the siderophore and recycling of the modified desferrichrome

Journal of Bacteriology

Volumn 192, Issue 5, 2010, Pages 1212-1220

  Hannauer, Mélissa ^a   Barda, Yaniv ^b   Mislin, Gaëtan L A ^a   Shanzer, Abraham ^b   Schalk, Isabelle J ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; DESFERRICHROME; FERRICHROME; FERRIPYOCHELIN; FERRIPYOVERDINE; FIUB PROTEIN; FIUC PROTEIN; MEMBRANE PROTEIN; PERMEASE; SIDEROPHORE; TONB1 PROTEIN; UNCLASSIFIED DRUG;

ACYLATION; ARTICLE; BIOMIMETICS; IN VIVO STUDY; IRON KINETICS; IRON TRANSPORT; OUTER MEMBRANE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA;

ACYLATION; BACTERIAL PROTEINS; FERRICHROME; IRON; MEMBRANE TRANSPORT PROTEINS; METABOLIC NETWORKS AND PATHWAYS; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA;

EID: 77749270483     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01539-09     Document Type: Article

References (67)

1. Albrecht-Gary, A. M., S. Blanc, N. Rochel, A. Z. Ocacktan, and M. A. Abdallah. 1994. Bacterial iron transport: coordination properties of pyoverdin PaA, a peptidic siderophore of Pseudomonas aeruginosa. Inorg. Chem. 33:6391-6402.
2. Baba, T., T. Ara, M. Hasegawa, Y. Takai, Y. Okumura, M. Baba, K. A. Datsenko, M. Tomita, B. L. Wanner, and H. Mori. 2006. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2:2006.0008.
3. Boukhalfa, H., and A. L. Crumbliss. 2002. Chemical aspects of siderophore mediated iron transport. Biometals 15:325-339.
4. Braun, V. 2003. Iron uptake by Escherichia coli. Front. Biosci. 8:1409-1421.
5. Braun, V., and F. Endriss. 2007. Energy-coupled outer membrane transport proteins and regulatory proteins. Biometals 20:219-231.
6. Braun, V., and C. Herrmann. 2007. Docking of the periplasmic FecB binding protein to the FecCD transmembrane proteins in the ferric citrate transport system of Escherichia coli. J. Bacteriol. 189:6913-6918.
7. Brickman, T. J., and M. A. McIntosh. 1992. Overexpression and purification of ferric enterobactin esterase from Escherichia coli. Demonstration of enzymatic hydrolysis of enterobactin and its iron complex. J. Biol. Chem. 267:12350-12355.
8. Brillet, K., L. Journet, H. Celia, L. Paulus, A. Stahl, F. Pattus, and D. Cobessi. 2007. A β-strand lock-exchange for signal transduction in TonB-dependent transducers on the basis of a common structural motif. Structure 15:1383-1391.
9. Chenault, S. S., and C. F. Earhart. 1991. Organization of genes encoding membrane proteins of the Escherichia coli ferrienterobactin permease. Mol. Microbiol. 5:1405-1413.
10. Clément, E., P. J. Mesini, F. Pattus, M. A. Abdallah, and I. J. Schalk. 2004. The binding mechanism of pyoverdin with the outer membrane receptor FpvA in Pseudomonas aeruginosa is dependent on its iron-loaded status. Biochemistry 43:7954-7965.
11. Cobessi, D., H. Célia, N. Folschweiller, I. J. Schalk, M. A. Abdallah, and F. Pattus. 2005. The crystal structure of the pyoverdin outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 Å resolution. J. Mol. Biol. 347:121-134.
12. Cobessi, D., H. Celia, and F. Pattus. 2004. Crystallization and X-ray diffraction analyses of the outer membrane pyochelin receptor FptA from Pseudomonas aeruginosa. Acta Crystallogr. D Biol. Crystallogr. 60:1919-1921.
13. Cornelis, P., and S. Matthijs. 2002. Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ. Microbiol. 4:787-798.
14. Cox, C. D. 1980. Iron uptake with ferripyochelin and ferriccitrate by Pseudomonas aeruginosa. J. Bacteriol. 142:581-587.
15. Cox, C. D., K. L. Rinehart, Jr., M. L. Moore, and J. C. Cook, Jr. 1981. Pyochelin: novel structure of an iron-chelating growth promoter for Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 78:4256-4260.
16. Cuiv, P. O., P. Clarke, D. Lynch, and M. O'Connell. 2004. Identification of rhtX and fptX, novel genes encoding proteins that show homology and function in the utilization of the siderophores rhizobactin 1021 by Sinorhizobium meliloti and pyochelin by Pseudomonas aeruginosa, respectively. J. Bacteriol. 186:2996-3005.
17. Cuiv, P. O., D. Keogh, P. Clarke, and M. O'Connell. 2007. FoxB of Pseudomonas aeruginosa functions in the utilization of the xenosiderophores ferrichrome, ferrioxamine B, and schizokinen: evidence for transport redundancy at the inner membrane. J. Bacteriol. 189:284-287.
18. Dayan, I., J. Libman, Y. Agi, and A. Shanzer. 1993. Chiral siderophore analogs - ferrichrome. Inorg. Chem. 32:1467-1475.
19. Ghysels, B., B. T. Dieu, S. A. Beatson, J. P. Pirnay, U. A. Ochsner, M. L. Vasil, and P. Cornelis. 2004. FpvB, an alternative type I ferripyoverdine receptor of Pseudomonas aeruginosa. Microbiology 150:1671-1680.
20. Greenwald, J., F. Hoegy, M. Nader, L. Journet, G. L. A. Mislin, P. L. Graumann, and I. J. Schalk. 2007. Real-time FRET visualization of ferricpyoverdine uptake in Pseudomonas aeruginosa: a role for ferrous iron. J. Biol. Chem. 282:2987-2995.
21. Gumbart, J., M. C. Wiener, and E. Tajkhorshid. 2007. Mechanics of force propagation in TonB-dependent outer membrane transport. Biophys. J. 93: 496-504.
22. Hantke, K. 1983. Identification of an iron uptake system specific for coprogen and rhodotorulic acid in Escherichia coli K12. Mol. Gen. Genet 191: 301-306.
23. Harding, R. A., and P. W. Royt. 1990. Acquisition of iron from citrate by Pseudomonas aeruginosa. J. Gen. Microbiol. 136:1859-1867.
24. Hartman, A., and V. Braun. 1980. Iron transport in Escherichia coli: uptake and modification of ferrichrome. J. Bacteriol. 143:246-255.
25. Heinrichs, D. E., L. Young, and K. Poole. 1991. Pyochelin-mediated iron transport in Pseudomonas aeruginosa: involvement of a high-molecular-mass outer membrane protein. Infect. Immun. 59:3680-3684.
26. Hoegy, F., H. Celia, G. L. Mislin, M. Vincent, J. Gallay, and I. J. Schalk. 2005. Binding of iron-free siderophore, a common feature of siderophore outer membrane transporters of Escherichia coli and Pseudomonas aeruginosa. J. Biol. Chem. 280:20222-20230.
27. Hoegy, F., X. Lee, S. Noël, G. L. Mislin, D. Rognan, C. Reimmann, and I. J. Schalk. 2009. Stereospecificity of the siderophore pyochelin outer membrane transporters in fluorescent Pseudomonads. J. Biol. Chem. 284:14949-14957.
28. Huang, B., K. Ru, Z. Yuan, C. B. Whitchurch, and J. S. Mattick. 2004. tonB3 is required for normal twitching motility and extracellular assembly of type IV pili. J. Bacteriol. 186:4387-4389.
29. Jacobs, M. A., A. Alwood, I. Thaipisuttikul, D. Spencer, E. Haugen, S. Ernst, O. Will, R. Kaul, C. Raymond, R. Levy, L. Chun-Rong, D. Guenthner, D. Bovee, M. V. Olson, and C. Manoil. 2003. Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. U. S. A. 100:14339-14344.
30. Kadner, R. J., and K. J. Heller. 1995. Mutual inhibition of cobalamin and siderophore uptake systems suggests their competition for TonB function. J. Bacteriol. 177:4829-4835.
31. Kall, L., A. Krogh, and E. L. Sonnhammer. 2007. Advantages of combined transmembrane topology and signal peptide prediction - the Phobius web server. Nucleic Acids Res. 35:W429-W432.
32. Killmann, H., and V. Braun. 1998. Conversion of the coprogen transport protein FhuE and the ferrioxamine B transport protein FoxA into ferrichrome transport proteins. FEMS Microbiol. Lett. 161:59-67.
33. Koster, W. 2001. ABC transporter-mediated uptake of iron, siderophores, heme and vitamin B12. Res. Microbiol. 152:291-301.
34. Koster, W. 1991. Iron(III) hydroxamate transport across the cytoplasmic membrane of Escherichia coli. Biol. Met. 4:23-32.
35. Koster, W., and V. Braun. 1986. Iron hydroxamate transport of Escherichia coli: nucleotide sequence of the fhuB gene and identification of the protein. Mol. Gen. Genet 204:435-442.
36. Koster, W., and V. Braun. 1989. Iron-hydroxamate transport into Escherichia coli K12: localization of FhuD in the periplasm and of FhuB in the cytoplasmic membrane. Mol. Gen. Genet 217:233-239.
37. Koster, W., A. Gudmundsdottir, M. D. Lundrigan, A. Seiffert, and R. J. Kadner. 1991. Deletions or duplications in the BtuB protein affect its level in the outer membrane of Escherichia coli. J. Bacteriol. 173:5639-5647.
38. Llamas, M. A., M. J. Mooij, M. Sparrius, C. M. Vandenbroucke-Grauls, C. Ratledge, and W. Bitter. 2008. Characterization of five novel Pseudomonas aeruginosa cell-surface signalling systems. Mol. Microbiol. 67:458-472.
39. Llamas, M. A., M. Sparrius, R. Kloet, C. R. Jimenez, C. Vandenbroucke-Grauls, and W. Bitter. 2006. The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J. Bacteriol. 188:1882-1891.
40. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:1051-1060.
41. Matzanke, B. F., S. Anemuller, V. Schunemann, A. X. Trautwein, and K. Hantke. 2004. FhuF, part of a siderophore-reductase system. Biochemistry 43:1386-1392.
42. Meijler, M. M., R. Arad-Yellin, Z. I. Cabantchik, and A. Shanzer. 2002. Synthesis and evaluation of iron chelators with masked hydrophilic moieties. J. Am. Chem. Soc. 124:12666-12667.
43. Mettrick, K. A., and I. L. Lamont. 2009. Different roles for anti-sigma factors in siderophore signalling pathways of Pseudomonas aeruginosa. Mol. Microbiol. 74:1257-1271.
44. Meyer, J. M. 1992. Exogenous siderophore-mediated iron uptake in Pseudomonas aeruginosa: possible involvement of porin OprF in iron translocation. J. Gen. Microbiol. 138:951-958.
45. Mislin, G. L. A., F. Hoegy, D. Cobessi, K. Poole, D. Rognan, and I. J. Schalk. 2006. Binding properties of pyochelin and structurally related molecules to FptA of Pseudomonas aeruginosa. J. Mol. Biol. 357:1437-1448.
46. Ochsner, U. A., P. J. Wilderman, A. I. Vasil, and M. L. Vasil. 2002. Gene-Chip expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol. Microbiol. 45:1277-1287.
47. Poole, K., and G. A. McKay. 2003. Iron acquisition and its control in Pseudomonas aeruginosa: many roads lead to Rome. Front. Biosci. 8:d661-d686.
48. Poole, K., S. Neshat, K. Krebes, and D. E. Heinrichs. 1993. Cloning and nucleotide sequence analysis of the ferripyoverdine receptor gene fpvA of Pseudomonas aeruginosa. J. Bacteriol. 175:4597- 4604.
49. Poole, K., L. Young, and S. Neshat. 1990. Enterobactin-mediated iron transport in Pseudomonas aeruginosa. J. Bacteriol. 172:6991-6996.
50. Poole, K., Q. Zhao, S. Neshat, D. E. Heinrichs, and C. R. Dean. 1996. The Pseudomonas aeruginosa tonB gene encodes a novel TonB protein. Microbiology 142:1449-1458.
51. Postle, K., and R. J. Kadner. 2003. Touch and go: tying TonB to transport. Mol. Microbiol. 49:869-882.
52. Royle, P. L., H. Matsumoto, and B. W. Holloway. 1981. Genetic circularity of the Pseudomonas aeruginosa PAO chromosome. J. Bacteriol. 145:145-155.
53. Schalk, I. J. 2008. Metal trafficking via siderophores in Gram-negative bacteria: specificities and characteristics of the pyoverdine pathway. J. Inorg. Biochem. 102:1159-1169.
54. Schalk, I. J., M. A. Abdallah, and F. Pattus. 2002. Recycling of pyoverdin on the FpvA receptor after ferric pyoverdin uptake and dissociation in Pseudomonas aeruginosa. Biochemistry 41:1663-1671.
55. Schalk, I. J., C. Hennard, C. Dugave, K. Poole, M. A. Abdallah, and F. Pattus. 2001. Iron-free pyoverdin binds to its outer membrane receptor FpvA in Pseudomonas aeruginosa: a new mechanism for membrane iron transport. Mol. Microbiol. 39:351-360.
56. Staudenmaier, H., B. Van Hove, Z. Yaraghi, and V. Braun. 1989. 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. 171:2626-2633.
57. Takase, H., H. Nitanai, K. Hoshino, and T. Otani. 2000. Impact of siderophore production on Pseudomonas aeruginosa infections in immunosuppressed mice. Infect. Immun. 68:1834-1839.
58. Takase, H., H. Nitanai, K. Hoshino, and T. Otani. 2000. Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect. Immun. 68:4498-4504.
59. Van Delden, C., and B. H. Iglewski. 1998. Cell-to-cell signaling and Pseudomonas aeruginosa infections. Emerg. Infect. Dis. 4:551-560.
60. Vasil, M. L., and U. A. Ochsner. 1999. The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol. Microbiol. 34:399-413.
61. Visca, P., L. Leoni, M. J. Wilson, and I. L. Lamont. 2002. Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol. Microbiol. 45:1177-1190.
62. Wendenbaum, S., P. Demange, A. Dell, J. M. Meyer, and M. A. Abdallah. 1983. The structure of pyoverdin Pa, the siderophore of Pseudomonas aeruginosa. Tetrahedron Lett. 24:4877-4880.
63. Wiener, M. C. 2005. TonB-dependent outer membrane transport: going for Baroque? Curr. Opin. Struct. Biol. 15:394-400.
64. Winkelmann, G. 2002. Microbial siderophore-mediated transport. Biochem. Soc. Trans. 30:691-696.
65. Wirth, C., W. Meyer-Klaucke, F. Pattus, and D. Cobessi. 2007. From the periplasmic signaling domain to the extracellular face of an outer membrane signal transducer of Pseudomonas aeruginosa: crystal structure of the ferric pyoverdine outer membrane receptor. J. Mol. Biol. 68:398-406.
66. Yeterian, E., L. W. Martin, I. L. Lamont, and I. J. Schalk. A resistance-division-nodulation (RND) efflux pump is required for siderophore recycling by Pseudomonas aeruginosa. Environ. Microbiol. Rep., in press.
67. Zhao, Q., and K. Poole. 2000. A second tonB gene in Pseudomonas aeruginosa is linked to the exbB and exbD genes. FEMS Microbiol. Lett. 184:127-132.