The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa

Journal of Bacteriology

Volumn 188, Issue 5, 2006, Pages 1882-1891

  Llamas, María A ^a   Sparrius, Marion ^a   Kloet, Roy ^a   Jiménez, Connie R ^a   Vandenbroucke Grauls, Christina ^a   Bitter, Wilbert ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

EXTRACYTOPLASMIC FUNCTION SIGMA FACTOR; FERRICHROME; FERRIOXAMINE; HYDROXAMIC ACID; IRON; MEMBRANE RECEPTOR; PYOCHELIN; PYOVERDINE; SIDEROPHORE; SIGMA FACTOR; TONB DEPENDENT RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BIOSYNTHESIS; CELL SURFACE; CONTROLLED STUDY; GENE INDUCTION; GENE LOCUS; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEOMICS; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; SENSOR; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; DEFEROXAMINE; FERRIC COMPOUNDS; FERRICHROME; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PSEUDOMONAS AERUGINOSA; RECEPTORS, CELL SURFACE; SEQUENCE ALIGNMENT; SIDEROPHORES; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 33644777983     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.5.1882-1891.2006     Document Type: Article

References (57)

1. Alexeyev, M. F., I. N. Shokolenko, and T. P. Croughan. 1995. Improved antibiotic-resistance gene cassettes and omega elements for Escherichia coli vector construction and in vitro deletion/insertion mutagenesis. Gene 160:63-67.
2. Ankenbauer, R. G. 1992. Cloning of the outer membrane high-affinity Fe(III)-pyochelin receptor of Pseudomonas aeruginosa. J. Bacteriol. 174:4401-4409.
3. Aso, H., S. Miyoshi, H. Nakao, K. Okamoto, and S. Yamamoto. 2002. Induction of an outer membrane protein of 78 kDa in Vibrio vulnificus cultured in the presence of desferrioxamine B under iron-limiting conditions. FEMS Microbiol. Lett. 212:65-70.
4. Banin, E., M. L. Vasil, and E. P. Greenberg. 2005. Iron and Pseudomonas aeruginosa biofilm formation. Proc. Natl. Acad. Sci. USA 102:11076-11081.
5. Bäumler, A. J., and K. Hantke. 1992. Ferrioxamine uptake in Yersinia enterocolitica: characterization of the receptor protein FoxA. Mol. Microbiol. 6:1309-1321.
6. Beare, P. A., R. J. For, L. W. Martin, and I. L. Lamont. 2003. Siderophore-mediated cell signalling in Pseudomonas aeruginosa: divergent pathways regulate virulence factor production and siderophore receptor synthesis. Mol. Microbiol. 47:195-207.
7. Bendtsen, J., H. Nielsen, G. Von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
8. Bitter, W., J. D. Marugg, L. A. de Weger, J. Tommassen, and P. J. Weisbeek. 1991. The ferric-pseudobactin receptor PupA of Pseudomonas putida WCS358: homology to TonB-dependent Escherichia coli receptors and specificity of the protein. Mol. Microbiol. 5:647-655.
9. Boyer, H. W., and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
10. Braun, V. 1997. Surface signaling: novel transcription initiation mechanism starting from the cell surface. Arch. Microbiol. 167:325-331.
11. Cornelis, P., and S. Matthijs. 2002. Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ. Microbiol. 4:787-798.
12. Crosa, J. H. 1997. Signal transduction and transcriptional and posttranscriptional control of iron-regulated genes in bacteria. Microbiol. Mol. Biol. Rev. 61:319-336.
13. Dean, C. R., S. Neshat, and K. Poole. 1996. PfeR, an enterobactin- responsive activator of ferric enterobactin receptor gene expression in Pseudomonas aeruginosa. J. Bacteriol. 178:5361-5369.
14. Dean, C. R., and K. Poole. 1993. Cloning and characterization of the ferric enterobactin receptor gene (pfeA) of Pseudomonas aeruginosa. J. Bacteriol. 175:317-324.
15. Dellagi, A., D. Reis, B. Vian, and D. Expert. 1999. Expression of the ferrioxamine receptor gene of Erwinia amylovora CFBP 1430 during pathogenesis. Mol. Plant-Microbe Interact. 12:463-466.
16. de Lorenzo, V., and K. N. Timmis. 1994. Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol. 235:386-405.
17. de Weger, L. A., R. van Boxtel, B. van der Burg, R. A. Gruters, F. P. Geels, B. Schippers, and B. Lugtenberg. 1986. Siderophores and outer membrane proteins of antagonistic, plant-growth-stimulating, root-colonizing Pseudomonas spp. J. Bacteriol. 165:585-594.
18. Escolar, L., J. Perez-Martin, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229.
19. Fecker, L., and V. Braun. 1983. Cloning and expression of the fhu genes involved in iron(III)-hydroxamate uptake by Escherichia coli. J. Bacteriol. 156:1301-1314.
20. Fürste, J. P., W. Pansegrau, R. Frank, H. Blocker, P. Scholz, M. Bagdasarian, and E. Lanka. 1986. Molecular cloning of the plasmid RP4 primase region in a multi-host-range tacP expression vector. Gene 48:119-131.
21. 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.
22. Ghysels, B., U. Ochsner, U. Mollman, L. Heinisch, M. Vasil, P. Cornells, and S. Matthijs. 2005. The Pseudomonas aeruginosa pirA gene encodes a second receptor for ferrienterobactin and synthetic catecholate analogues. FEMS Microbiol. Lett. 246:167-174.
23. Guerinot, M. L. 1994. Microbial iron transport. Annu. Rev. Microbiol. 48:743-772.
24. Haas, D., and B. W. Holloway. 1976. R factor variants with enhanced sex factor activity in Pseudomonas aeruginosa. Mol. Gen. Genet. 144:243-251.
25. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
26. Heim, S., M. Ferrer, H. Heuer, D. Regenhardt, M. Nimtz, and K. N. Timmis. 2003. Proteome reference map of Pseudomonas putida strain KT2440 for genome expression profiling: distinct responses of KT2440 and Pseudomonas aeruginosa strain PAO1 to iron deprivation and a new form of superoxide dismutase. Environ. Microbiol. 5:1257-1269.
27. 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.
28. 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. USA 100:14339-14344.
29. Kingsley, R. A., R. Reissbrodt, W. Rabsch, J. M. Ketley, R. M. Tsolis, P. Everest, G. Dougan, A. J. Baumler, M. Roberts, and P. H. Williams. 1999. Ferrioxamine-mediated iron(III) utilization by Salmonella enterica. Appl. Environ. Microbiol. 65:1610-1618.
30. Koebnik, R. 2005. TonB-dependent trans-envelope signalling: the exception or the rule? Trends Microbiol. 13:343-347.
31. Koster, M., J. van de Vossenberg, J. Leong, and P. J. Weisbeek. 1993. Identification and characterization of the pupB gene encoding an inducible ferric-pseudobactin receptor of Pseudomonas putida WCS358. Mol. Microbiol. 8:591-601.
32. 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.
33. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
34. Lament, I. L., P. A. Beare, U. Ochsner, A. I. Vasil, and M. L. Vasil. 2002. Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 99:7072-7077.
35. Leoni, L., N. Orsi, V. de Lorenzo, and P. Visca. 2000. Functional analysis of PvdS, an iron starvation sigma factor of Pseudomonas aeruginosa. J. Bacteriol. 182:1481-1491.
36. Mahren, S., S. Enz, and V. Braun. 2002. Functional interaction of region 4 of the extracytoplasmic function sigma factor Feel with the cytoplasmic portion of the FecR transmembrane protein of the Escherichia coli ferric citrate transport system. J. Bacteriol. 184:3704-3711.
37. 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 PA01. Environ. Microbiol. 4:842-855.
38. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
39. Missiakas, D., and S. Raina. 1998. The extracytoplasmic function sigma factors: role and regulation. Mol. Microbiol. 28:1059-1066.
40. Nelson, M., C. J. Carrano, and P. J. Szaniszlo. 1992. Identification of the ferrioxamine B receptor, FoxB, in Escherichia coli K12. Biometals 5:37-46.
41. Nelson, M., and P. J. Szaniszlo. 1992. TonB-independent ferrioxamine B-mediated iron transport in Escherichia coli K12. FEMS Microbiol. Lett. 79:191-196.
42. Norrander, J., T. Kempe, and J. Messing. 1983. Construction of improved M13 vectors using oligodeoxynucleotide-directed mutagenesis. Gene 26:101-106.
43. Ochs, M., S. Veitinger, I. Kim, D. Welz, A. Angerer, and V. Braun. 1995. Regulation of citrate-dependent iron transport of Escherichia coli: fecR is required for transcription activation by Feel. Mol. Microbiol. 15:119-132.
44. Ochsner, U. A., Z. Johnson, and M. L. Vasil. 2000. Genetics and regulation of two distinct haem-uptake systems, phu and has, in Pseudomonas aeruginosa. Microbiology 146:185-198.
45. Ochsner, U. A., and M. L. Vasil. 1996. Gene repression by the ferric uptake regulator in Pseudomonas aeruginosa: cycle selection of iron-regulated genes. Proc. Natl. Acad. Sci. USA 93:4409-4414.
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. Palma, M., S. Worgall, and L. E. Quadri. 2003. Transcriptome analysis of the Pseudomonas aeruginosa response to iron. Arch. Microbiol. 180:374-379.
48. Postle, K. 1999. Active transport by customized beta-barrels. Nat. Struct. Biol. 6:3-6.
49. Ratledge, C., and L. G. Dover. 2000. Iron metabolism in pathogenic bacteria. Annu. Rev. Microbiol. 54:881-941.
50. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
51. Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-terminating inhibitors. Proc. Natl. Acad. Sci. USA 74:5463-5467.
52. Sauer, M., K. Hantke, and V. Braun. 1990. Sequence of the fhuE outer-membrane receptor gene of Escherichia coli K12 and properties of mutants. Mol. Microbiol. 4:427-437.
53. Spaink, H. P., R. J. H. Okker, C. A. Wijffelman, E. Pees, and B. J. J. Lugtenberg. 1987. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol. Biol. 9:27-39.
54. Tanabe, T., N. Takata, A. Naka, Y. H. Moon, H. Nakao, Y. Inoue, S. Narimatsu, and S. Yamamoto. 2005. Identification of an AraC-like regulator gene required for induction of the 78-kDa ferrioxamine B receptor in Vibrio vulnificus. FEMS Microbiol. Lett. 249:309-314.
55. Vasil, M. L., and U. A. Ochsner. 1999. The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol. Microbiol. 34:399-413.
56. Visca, P., L. Leoni, M. J. Wilson, and I. L. Lament. 2002. Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol. Microbiol. 45:1177-1190.
57. Yorgey, P., L. G. Rahme, M. W. Tan, and F. M. Ausubel. 2001. The roles of mucD and alginate in the virulence of Pseudomonas aeruginosa in plants, nematodes and mice. Mol. Microbiol. 41:1063-1076.