Deciphering protein dynamics of the siderophore pyoverdine pathway in Pseudomonas aeruginosa

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Guillon, Laurent ^a   Altenburger, Stephan ^b   Graumann, Peter L ^b   Schalk, Isabelle J ^a  

^a Institut de Recherche de l'Ecole de Biotechnologie de Strasbourg   (France)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PERIPLASMIC BINDING PROTEIN; PROTEIN FPVC; PROTEIN FPVF; PROTEIN TONB; PYOVERDINE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; IRON; OLIGOPEPTIDE;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BIOSYNTHESIS; CELL COMPARTMENTALIZATION; CELL MOTILITY; CONTROLLED STUDY; DIFFUSION; DIFFUSION COEFFICIENT; ESCHERICHIA COLI; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; CELL POLARITY; METABOLISM;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; CELL POLARITY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IRON; METABOLIC NETWORKS AND PATHWAYS; OLIGOPEPTIDES; PSEUDOMONAS AERUGINOSA;

EID: 84921867808     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079111     Document Type: Article

References (66)

1. Hider RC, Kong X (2011) Chemistry and biology of siderophores. Nat Prod Rep 27: 637-657.
2. Schalk IJ (2008) Metal trafficking via siderophores in Gram-negative bacteria: specificities and characteristics of the pyoverdine pathway. J Inorg Biochemi 102: 1159-1169.
3. Schalk IJ, Guillon L (2013) Pyoverdine biosynthesis and secretion in Pseudomonas aeruginosa: implications for metal homeostasis. Environ Microbiol in press.
4. Visca P, Imperi F, Lamont IL (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15: 22-30.
5. Hannauer M, Schäfer M, Hoegy F, Gizzi P, Wehrung P, et al. (2012) Biosynthesis of the pyoverdine siderophore of Pseudomonas aeruginosa involves precursors with a myristic or a myristoleic acid chain. FEBS Lett 586: 96-101.
6. Guillon L, El Mecherki M, Altenburger S, Graumann PL, Schalk IJ (2012) High cellular organisation of pyoverdine biosynthesis in Pseudomonas aeruginosa: localization of PvdA at the old cell pole. Environ Microbiol 14: 1982-1994.
7. Yeterian E, Martin LW, Guillon L, Journet L, Lamont IL, et al. (2010) Synthesis of the siderophore pyoverdine in Pseudomonas aeruginosa involves a periplasmic maturation. Amino Acids 38: 1447-1459.
8. Lamont IL, Martin LW (2003) Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa. Microbiology 149: 833-842.
9. Ochsner U, Snyder A, Vasil AI, Vasil ML (2002) Effects of the twin-arginine translocase on secretion of virulence factors, stress response, and pathogenesis. Proc Natl Acad Sci U S A 99: 8312-8317.
10. Voulhoux R, Filloux A, Schalk IJ (2006) Role of the TAT System in the pyoverdine-mediated iron acquisition in Pseudomonas aeruginosa. J Bacteriol 188: 3317-3323.
11. Gulick AM, Drake EJ (2011) Structural characterization and high-throughput screening of inhibitors of PvdQ, an NTN hydrolase involved in pyoverdine synthesis. ACS Chem Biol 6: 1277-1286.
12. Hannauer M, Yeterian E, Martin LW, Lamont IL, Schalk IJ (2010) Secretion of newly synthesized pyoverdine by Pseudomonas aeruginosa involves an efflux pump. FEBS Lett 584: 4751-4755.
13. Schalk IJ, Kyslik P, Prome D, van Dorsselaer A, Poole K, et al. (1999) Copurification of the FpvA ferric pyoverdin receptor of Pseudomonas aeruginosa with its iron-free ligand: implications for siderophore-mediated iron transport. Biochemistry 38: 9357-9365.
14. Brillet K, Journet L, Celia H, Paulus L, Stahl A, et al. (2007) A b-strand lockexchange for signal transduction in TonB-dependent transducers on the basis of a common structural motif. Structure 15: 1383-1391.
15. Wirth C, Meyer-Klaucke W, Pattus F, Cobessi D (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.
16. Nader M, Dobbelaere W, Vincent M, Journet L, Adams H, et al. (2007) Identification of residues of FpvA involved in the different steps of Pvd-Fe uptake in Pseudomonas aeruginosa. Biochemistry 46: 11707-11717.
17. Gresock MG, Savenkova MI, Larsen RA, Ollis AA, Postle K (2011) Death of the TonB shuttle hypothesis. Front Microbiol 2: 206.
18. Adams H, Zeder-Lutz G, Greenwald J, Schalk IJ, Célia H, et al. (2006) Interaction of TonB with outer membrane receptor FpvA of Pseudomonas aeruginosa. J Bacteriol 188: 5752-5761.
19. Pawelek PD, Croteau N, Ng-Thow-Hing C, Khursigara CM, Moiseeva N, et al. (2006) Structure of TonB in complex with FhuA, E. coli outer membrane receptor. Science 312: 1399-1402.
20. Shultis DD, Purdy MD, Banchs CN, Wiener MC (2006) Outer membrane active transport: structure of the BtuB:TonB complex. Science 312: 1396-1399.
21. Gumbart J, Wiener MC, Tajkhorshid E (2007) Mechanics of force propagation in TonB-dependent outer membrane transport. Biophys J 93: 496-504.
22. Shirley M, Lamont IL (2009) Role of TonB1 in pyoverdine-mediated signaling in Pseudomonas aeruginosa. J Bacteriol 191: 5634-5640.
23. Greenwald J, Hoegy F, Nader M, Journet L, Mislin GLA, et al. (2007) Real-time FRET visualization of ferric-pyoverdine uptake in Pseudomonas aeruginosa: a role for ferrous iron. J Biol Chem 282: 2987-2995.
24. Brillet K, Ruffenach F, Adams H, Journet L, Gasser V, et al. (2012) An ABC transporter with two periplasmic binding proteins involved in iron acquisition in Pseudomonas aeruginosa. ACS Chem Biol 7: 2036-2045.
25. Imperi F, Tiburzi F, Visca P (2009) Molecular basis of pyoverdine siderophore recycling in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 106: 20440-20445.
26. Schalk IJ, Abdallah MA, Pattus F (2002) Recycling of pyoverdin on the FpvA receptor after ferric pyoverdin uptake and dissociation in Pseudomonas aeruginosa. Biochemistry 41: 1663-1671.
27. Yeterian E, Martin LW, Lamont IL, Schalk IJ (2010) An efflux pump is required for siderophore recycling by Pseudomonas aeruginosa. Environ Microbiol Report 2: 412-418.
28. Cornelis P, Matthijs S, Van Oeffelen L (2009) Iron uptake regulation in Pseudomonas aeruginosa. Biometals 22: 15-22.
29. Visca P, Leoni L, Wilson MJ, Lamont IL (2002) Iron transport and regulation, cell signalling and genomics: lessons from Escherichia coli and Pseudomonas. Mol Microbiol 45: 1177-1190.
30. Beare PA, For RJ, Martin LW, Lamont IL (2003) Siderophore-mediated cell signalling in Pseudomonas aeruginosa: divergent pathways regulate virulence factor production and siderophore receptor synthesis. Mol Microbiol 47: 195-207.
31. Redly GA, Poole K (2005) FpvIR control of fpvA ferric pyoverdine receptor gene expression in Pseudomonas aeruginosa: demonstration of an interaction between FpvI and FpvR and identification of mutations in each compromising this interaction. J Bacteriol 187: 5648-5657.
32. James HE, Beare PA, Martin LW, Lamont IL (2005) Mutational analysis of a bifunctional ferrisiderophore receptor and signal-transducing protein from Pseudomonas aeruginosa. J Bacteriol 187: 4514-4520.
33. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 99: 7072-7077.
34. Shen J, Meldrum A, Poole K (2002) FpvA receptor involvement in pyoverdine biosynthesis in Pseudomonas aeruginosa. J Bacteriol 184: 3268-3275.
35. Schalk IJ, Lamont IL, Cobessi D (2009) Structure-function relationships in the bifunctional ferrisiderophore FpvA receptor from Pseudomonas aeruginosa. Biometals 22: 671-678.
36. Lenn T, Leake MC, Mullineaux CW (2008) Clustering and dynamics of cytochrome bd-I complexes in the Escherichia coli plasma membrane in vivo. Mol Microbiol 70: 1397-1407.
37. Gibbs KA, Isaac DD, Xu J, Hendrix RW, Silhavy TJ, et al. (2004) Complex spatial distribution and dynamics of an abundant Escherichia coli outer membrane protein, LamB. Mol Microbiol 53: 1771-1783.
38. Oddershede L, Dreyer JK, Grego S, Brown S, Berg-Sorensen K (2002) The motion of a single molecule, the lambda-receptor, in the bacterial outer membrane. Biophys J 83: 3152-3161.
39. Spector J, Zakharov S, Lill Y, Sharma O, Cramer WA, et al. (2010) Mobility of BtuB and OmpF in the Escherichia coli outer membrane: implications for dynamic formation of a translocon complex. Biophys J 99: 3880-3886.
40. Schulmeister S, Grosse K, Sourjik V (2011) Effects of receptor modification and temperature on dynamics of sensory complexes in Escherichia coli chemotaxis. BMC Microbiol 11: 222.
41. Schulmeister S, Ruttorf M, Thiem S, Kentner D, Lebiedz D, et al. (2008) Protein exchange dynamics at chemoreceptor clusters in Escherichia coli. Proc Natl Acad Sci U S A 105: 6403-6408.
42. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image processing with Image J. Biophotonics International 11: 36-42.
43. Elowitz MB, Surette MG, Wolf PE, Stock JB, Leibler S (1999) Protein mobility in the cytoplasm of Escherichia coli. J Bacteriol 181: 197-203.
44. R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0.
45. Kaserer WA, Jiang X, Xiao Q, Scott DC, Bauler M, et al. (2008) Insight from TonB hybrid proteins into the mechanism of iron transport through the outer membrane. J Bacteriol 190: 4001-4016.
46. Hannauer M, Yeterian E, Martin LW, Lamont IL, Schalk IJ (2010) An efflux pump is involved in secretion of newly synthesized siderophore by Pseudomonas aeruginosa. FEBS Lett 584: 4751-4755.
47. Kumar M, Mommer MS, Sourjik V (2010) Mobility of cytoplasmic, membrane, and DNA-binding proteins in Escherichia coli. Biophys J 98: 552-559.
48. Nenninger A, Mastroianni G, Mullineaux CW (2010) Size dependence of protein diffusion in the cytoplasm of Escherichia coli. J Bacteriol 192: 4535-4540.
49. Takase H, Nitanai H, Hoshino K, Otani T (2000) Requirement of the Pseudomonas aeruginosa tonB gene for high-affinity iron acquisition and infection. Infect Immun 68: 4498-4504.
50. Krewulak KD, Vogel HJ (2008) Structural biology of bacterial iron uptake. Biochim Biophys Acta 1778: 1781-1804.
51. Mullineaux CW, Nenninger A, Ray N, Robinson C (2006) Diffusion of green fluorescent protein in three cell environments in Escherichia coli. J Bacteriol 188: 3442-3448.
52. Sochacki KA, Shkel IA, Record MT, Weisshaar JC (2011) Protein diffusion in the periplasm of E. coli under osmotic stress. Biophys J 100: 22-31.
53. Tiburzi F, Imperi F, Visca P (2008) Intracellular levels and activity of PvdS, the major iron starvation sigma factor of Pseudomonas aeruginosa. Mol Microbiol 67: 213-227.
54. Bratton BP, Mooney RA, Weisshaar JC (2011) Spatial distribution and diffusive motion of RNA polymerase in live Escherichia coli. J Bacteriol 193: 5138-5146.
55. Carter DM, Miousse IR, Gagnon JN, Martinez E, Clements A, et al. (2006) Interactions between TonB from Escherichia coli and the periplasmic protein FhuD. J Biol Chem 281: 35413-35424.
56. James KJ, Hancock MA, Gagnon JN, Coulton JW (2009) TonB interacts with BtuF, the Escherichia coli periplasmic binding protein for cyanocobalamin. Biochemistry 48: 9212-9220.
57. Krewulak KD, Vogel HJ (2011) TonB or not TonB: is that the question? Biochem Cell Biol 89: 87-97.
58. Schalk IJ, Mislin GL, Brillet K (2012) Structure, function and binding selectivity and stereoselectivity of siderophore-iron outer membrane transporters. Curr Top Membr 69: 37-66.
59. Higgs PI, Larsen RA, Postle K (2002) Quantification of known components of the Escherichia coli TonB energy transduction system: TonB, ExbB, ExbD and FepA. Mol Microbiol 44: 271-281.
60. Higgs PI, Myers PS, Postle K (1998) Interactions in the TonB-dependent energy transduction complex: ExbB and ExbD form homomultimers. J Bacteriol 180: 6031-6038.
61. Jana B, Manning M, Postle K (2011) Mutations in the ExbB cytoplasmic carboxy terminus prevent energy-dependent interaction between the TonB and ExbD periplasmic domains. J Bacteriol 193: 5649-5657.
62. Ollis AA, Manning M, Held KG, Postle K (2009) Cytoplasmic membrane protonmotive force energizes periplasmic interactions between ExbD and TonB. Mol Microbiol 73: 466-481.
63. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
64. Simon R, Priefer U, Puhler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram Negative bacteria. Nat Biotech 1: 784-791.
65. Tukey JW (1951) Components in regression. Biometrics 7: 33-69.
66. Abramoff MD, Magalhaes PJ, Ram SJ (2004) Image Processing with ImageJ. Biophotonics International 11: 36-42.