Citrate-mediated iron uptake in Pseudomonas aeruginosa: Involvement of the citrate-inducible FecA receptor and the FeoB ferrous iron transporter

Microbiology

Volumn 155, Issue 1, 2009, Pages 305-315

  Marshall, Bryan ^a   Stintzi, Alain ^b   Gilmour, Christie ^a   Meyer, Jean Marie ^c   Poole, Keith ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CERULOPLASMIN; FERRIC CITRATE; FERRIC CITRATE RECEPTOR; FERRIC UPTAKE REGULATOR; SIDEROPHORE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CATION TRANSPORT PROTEIN; CELL SURFACE RECEPTOR; CITRIC ACID; IRON;

ARTICLE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM CULTURE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; IRON DEFICIENCY; IRON TRANSPORT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SENSITIVITY ANALYSIS; CULTURE MEDIUM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL; TRANSPOSON;

ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA;

BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CATION TRANSPORT PROTEINS; CITRIC ACID; CULTURE MEDIA; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION REGULATION, BACTERIAL; IRON; MUTAGENESIS, INSERTIONAL; PSEUDOMONAS AERUGINOSA; RECEPTORS, CELL SURFACE;

EID: 61449206201     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.023531-0     Document Type: Article

References (67)

1. Adhikari, P., Berish, S. A., Nowalk, A. J., Veraldi, K. L., Morse, S. A. & Mietzner, T. A. (1996). The fbpABC locus of Neisseria gonorrhoeae functions in the periplasm-to-cytosol transport of iron. J Bacteriol 178, 2145-2149.
2. Angerer, A., Klupp, B. & Braun, V. (1992). Iron transport systems of Serratia marcescens. J Bacteriol 174, 1378-1387.
3. Ankenbauer, R. G. & Cox, C. D. (1988). Isolation and characterization of Pseudomonas aeruginosa mutants requiring salicylic acid for pyochelin biosynthesis. J Bacteriol 170, 5364-5367.
4. Ankenbauer, R. G., Toyokuni, T., Staley, A., Rinehart, K. L., Jr & Cox, C. D. (1988). Synthesis and biological activity of pyochelin, a siderophore of Pseudomonas aeruginosa. J Bacteriol 170, 5344-5351.
5. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A. & Struhl, K. (1992). Short Protocols in Molecular Biology, 2nd edn. New York: Wiley.
6. Banin, E., Vasil, M. L. & Greenberg, E. P. (2005). Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102, 11076-11081.
7. Barcak, G. J., Chandler, M. S., Redfield, R. J. & Tomb, J. F. (1991). Genetic systems in Haemophilus influenzae. Methods Enzymol 204, 321-342.
8. Braun, V. (2003). Iron uptake by Escherichia coli. Front Biosci 8, s1409-s1421.
9. Braun, V. & Mahren, S. (2005). Transmembrane transcriptional control (surface signalling) of the Escherichia coli Fec type. FEMS Microbiol Rev 29, 673-684.
10. Braun, V., Mahren, S. & Sauter, A. (2006). Gene regulation by transmembrane signaling. Biometals 19, 103-113.
11. Cao, L., Srikumar, R. & Poole, K. (2004). MexAB-OprM hyperexpression in NalC type multidrug resistant Pseudomonas aeruginosa: identification and characterization of the nalC gene encoding a repressor of PA3720-PA3719. Mol Microbiol 53, 1423-1436.
12. 2+ homeostasis and avoidance of metal toxicity. Mol Microbiol 44, 561-571.
13. Choi, K. H., Kumar, A. & Schweizer, H. P. (2005). A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64, 391-397.
14. Cornelis, P., Moguilevsky, N., Jacques, J. F. & Masson, P. L. (1987). Study of the siderophores and receptors in different clinical isolates of Pseudomonas aeruginosa. Antibiot Chemother 39, 290-306.
15. Cox, C. D. (1980a). Iron reductases from Pseudomonas aeruginosa. J Bacteriol 141, 199-204.
16. Cox, C. D. (1980b). Iron uptake with ferripyochelin and ferric citrate by Pseudomonas aeruginosa. J Bacteriol 142, 581-587.
17. Cuiv, P. O., Clarke, P. & O'Connell, M. (2006). Identification and characterization of an iron-regulated gene, chtA, required for the utilization of the xenosiderophores aerobactin, rhizobactin 1021 and schizokinen by Pseudomonas aeruginosa. Microbiology 152, 945-954.
18. Cuiv, P. O., Keogh, D., Clarke, P. & O'Connell, M. (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.
19. de Lorenzo, V., Herrero, M., Jakubzik, U. & Timmis, K. N. (1990). Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol 172, 6568-6572.
20. Faguy, D. M., Bayley, D. P., Kostyukova, A. S., Thomas, N. A. & Jarrell, K. F. (1996). Isolation and characterization of flagella and flagellin proteins from the thermoacidophilic archaea Thermoplasma volcanium and Sulfolobus shibatae. J Bacteriol 178, 902-905.
21. Ghysels, B., Ochsner, U., Mollman, U., Heinisch, L., Vasil, M., Cornelis, P. & Matthijs, S. (2005). The Pseudomonas aeruginosa pirA gene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues. FEMS Microbiol Lett 246, 167-174.
22. Greenwald, J., Hoegy, F., Nader, M., Journet, L., Mislin, G. L., Graumann, P. L. & Schalk, I. J. (2007). Real time fluorescent resonance energy transfer visualization of ferric pyoverdine uptake in Pseudomonas aeruginosa. A role for ferrous iron. J Biol Chem 282, 2987-2995.
23. Hantke, K. (1987). Ferrous iron transport mutants in Escherichia coli K-12. FEMS Microbiol Lett 44, 53-58.
24. Harding, R. A. & Royt, P. W. (1990). Acquisition of iron from citrate by Pseudomonas aeruginosa. J Gen Microbiol 136, 1859-1867.
25. Heinrichs, D. E., Young, L. & Poole, K. (1991). Pyochelin-mediated iron transport in Pseudomonas aeruginosa: involvement of a high-molecular- mass outer membrane protein. Infect Immun 59, 3680-3684.
26. Hoang, T. T., Karkhoff-Schweizer, R. R., Kutchma, A. J. & Schweizer, H. P. (1998). A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212, 77-86.
27. Huston, W. M., Jennings, M. P. & McEwan, A. G. (2002). The multicopper oxidase of Pseudomonas aeruginosa is a ferroxidase with a central role in iron acquisition. Mol Microbiol 45, 1741-1750.
28. Inoue, H., Nojima, H. & Okayama, H. (1990). High efficiency transformation of Escherichia coli with plasmids. Gene 96, 23-28.
29. Kammler, M., Schon, C. & Hantke, K. (1993). Characterization of the ferrous iron uptake system of Escherichia coli. J Bacteriol 175, 6212-6219.
30. Katoh, H., Hagino, N., Grossman, A. R. & Ogawa, T. (2001). Genes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 183, 2779-2784.
31. Keen, N. T., Tamaki, S., Kobayashi, D. & Trollinger, D. (1988). Improved broad-host-range plasmids for DNA cloning in Gram-negative bacteria. Gene 70, 191-197.
32. Llamas, M. A., Sparrius, M., Kloet, R., Jimenez, C. R., Vandenbroucke-Grauls, C. & Bitter, W. (2006). The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J Bacteriol 188, 1882-1891.
33. Llamas, M. A., Mooij, M. J., Sparrius, M., Vandenbroucke-Grauls, C. M., Ratledge, C. & Bitter, W. (2008). Characterization of five novel Pseudomonas aeruginosa cell-surface signalling systems. Mol Microbiol 67, 458-472.
34. Louvel, H., Saint, G. I. & Picardeau, M. (2005). Isolation and characterization of FecA- and FeoB-mediated iron acquisition systems of the spirochete Leptospira biflexa by random insertional mutagenesis. J Bacteriol 187, 3249-3254.
35. Mazoy, R., Lopez, E. M., Fouz, B., Amaro, C. & Lemos, M. L. (1999). Ferric-reductase activities in Vibrio vulnificus biotypes 1 and 2. FEMS Microbiol Lett 172, 205-211.
36. 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.
37. Meyer, J.-M. & Abdallah, M. A. (1978). The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physio-chemical properties. J Gen Microbiol 107, 319-328.
38. Pf, the iron-binding fluorescent pigment of Pseudomonas fluorescens, in iron transport. J Gen Microbiol 107, 329-331.
39. Meyer, J. M., Stintzi, A., Coulanges, V., Shivaji, S., Voss, J. A., Taraz, K. & Budzikiewicz, H. (1998). Siderotyping of fluorescent pseudomonads: characterization of pyoverdines of Pseudomonas fluorescens and Pseudomonas putida strains from Antarctica. Microbiology 144, 3119-3126.
40. Meyer, J. M., Stintzi, A. & Poole, K. (1999). The ferripyoverdine receptor FpvA of Pseudomonas aeruginosa PAO1 recognizes the ferripyoverdines of Pseudomonas aeruginosa PAO1 and Pseudomonas fluorescens ATCC 13525. FEMS Microbiol Lett 170, 145-150.
41. Michel, L., Bachelard, A. & Reimmann, C. (2007). Ferripyochelin uptake genes are involved in pyochelin-mediated signalling in Pseudomonas aeruginosa. Microbiology 153, 1508-1518.
42. Mielczarek, E. V., Royt, P. W. & Toth-Allen, J. (1990). A Mossbauer spectroscopy study of cellular acquisition of iron from pyoverdine by Pseudomonas aeruginosa. Biol Met 3, 34-38.
43. Miller, V. L. & Mekalanos, J. J. (1988). A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170, 2575-2583.
44. Naikare, H., Palyada, K., Panciera, R., Marlow, D. & Stintzi, A. (2006). Major role for FeoB in Campylobacter jejuni ferrous iron acquisition, gut colonization, and intracellular survival. Infect Immun 74, 5433-5444.
45. Nehme, D., Li, X. Z., Elliot, R. & Poole, K. (2004). Assembly of the MexAB-OprM multidrug efflux system of Pseudomonas aeruginosa: identification and characterization of mutations in mexA compromising MexA multimerization and interaction with MexB. J Bacteriol 186, 2973-2983.
46. Ochsner, U. A., Wilderman, P. J., Vasil, A. I. & Vasil, M. L. (2002). GeneChip® expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol Microbiol 45, 1277-1287.
47. Poch, M. T. & Johnson, W. (1993). Ferric reductases of Legionella pneumophila. Biometals 6, 107-114.
48. Poole, K. & McKay, G. A. (2003). Iron acquisition and its control in Pseudomonas aeruginosa: many roads lead to Rome. Front Biosci 8, d661-d686.
49. Poole, K., Young, L. & Neshat, S. (1990). Enterobactin-mediated iron transport in Pseudomonas aeruginosa. J Bacteriol 172, 6991-6996.
50. Poole, K., Neshat, S. & Heinrichs, D. (1991). Pyoverdine-mediated iron transport in Pseudomonas aeruginosa: involvement of a high-molecular molecular-mass outer membrane protein. FEMS Microbiol Lett 62, 1-5.
51. Ravel, J. & Cornelis, P. (2003). Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol 11, 195-200.
52. Redly, G. A. & Poole, K. (2003). Pyoverdine-mediated regulation of FpvA synthesis in Pseudomonas aeruginosa: involvement of a probable extracytoplasmic-function sigma factor, FpvI. J Bacteriol 185, 1261-1265.
53. Robey, M. & Cianciotto, N. P. (2002). Legionella pneumophila feoAB promotes ferrous iron uptake and intracellular infection. Infect Immun 70, 5659-5669.
54. Royt, P. W. (1990). Pyoverdine-mediated iron transport. Fate of iron and ligand in Pseudomonas aeruginosa. Biol Met 3, 28-33.
55. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
56. Sanders, J. D., Cope, L. D. & Hansen, E. J. (1994). Identification of a locus involved in the utilization of iron by Haemophilus influenzae. Infect Immun 62, 4515-4525.
57. Schäfer, A., Tauch, A., Jäger, W., Kalinowski, J., Thierbach, G. & Pühler, A. (1994). Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145, 69-73.
58. Schweizer, H. P. (1991). Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene 97, 109-121.
59. Simon, R., Priefer, U. & Puehler, A. (1983). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio/Technology 1, 784-791.
60. Sobel, M. L., McKay, G. A. & Poole, K. (2003). Contribution of the MexXY multidrug transporter to aminoglycoside resistance in Pseudomonas aeruginosa clinical isolates. Antimicrob Agents Chemother 47, 3202-3207.
61. Sobel, M. L., Poole, K. & Neshat, S. (2005). Mutations in PA2491 (mexS) promote MexT-dependent mexEF-oprN expression and multidrug resistance in a clinical strain of Pseudomonas aeruginosa. J Bacteriol 187, 1246-1253.
62. Srikumar, R., Kon, T., Gotoh, N. & Poole, K. (1998). Expression of Pseudomonas aeruginosa multidrug efflux pumps MexA-MexB-OprM and MexC-MexD-OprJ in a multidrug-sensitive Escherichia coli strain. Antimicrob Agents Chemother 42, 65-71.
63. Stover, C. K., Pham, X. Q., Erwin, A. L., Mizoguchi, S. D., Warrener, P., Hickey, M. J., Brinkman, F. S., Hufnagle, W. O., Kowalik, D. J. & other authors (2000). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959-964.
64. Velayudhan, J., Hughes, N. J., McColm, A. A., Bagshaw, J., Clayton, C. L., Andrews, S. C. & Kelly, D. J. (2000). Iron acquisition and virulence in Helicobacter pylori: a major role for FeoB, a high-affinity ferrous iron transporter. Mol Microbiol 37, 274-286.
65. Visca, P., Leoni, L., Wilson, M. J. & Lamont, I. L. (2002). Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45, 1177-1190.
66. Visca, P., Imperi, F. & Lamont, I. L. (2007). Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15, 22-30.
67. Wyckoff, E. E., Mey, A. R., Leimbach, A., Fisher, C. F. & Payne, S. M. (2006). Characterization of ferric and ferrous iron transport systems in Vibrio cholerae. J Bacteriol 188, 6515-6523.