High cellular organization of pyoverdine biosynthesis in Pseudomonas aeruginosa: Clustering of PvdA at the old cell pole

Environmental Microbiology

Volumn 14, Issue 8, 2012, Pages 1982-1994

  Guillon, Laurent ^a   El Mecherki, Maher ^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 UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; IRON; MIXED FUNCTION OXIDASE; OLIGOPEPTIDE; ORNITHINE HYDROXYLASE, PSEUDOMONAS AERUGINOSA; PYOVERDINE; SIDEROPHORE;

ARTICLE; BIOSYNTHESIS; CELL MEMBRANE; CYTOLOGY; CYTOPLASM; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN STABILITY; PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; CELL MEMBRANE; CYTOPLASM; IRON; MIXED FUNCTION OXYGENASES; OLIGOPEPTIDES; PERIPLASM; PROTEIN STABILITY; PSEUDOMONAS AERUGINOSA; SIDEROPHORES;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 84864390775     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02741.x     Document Type: Article

References (53)

1. Abramoff, M.D., Magalhaes, P.J., and Ram, S.J. (2004) Image processing with Image J. Biophotonics Int 11: 36-42.
2. Ackerley, D.F., Caradoc-Davies, T.T., and Lamont, I.L. (2003) Substrate specificity of the nonribosomal peptide synthetase PvdD from Pseudomonas aeruginosa. J Bacteriol 185: 2848-2855.
3. Bokhove, M., Jimenez, P.N., Quax, W.J., and Dijkstra, B.W. (2010) The quorum-quenching N-acyl homoserine lactone acylase PvdQ is an Ntn-hydrolase with an unusual substrate-binding pocket. Proc Natl Acad Sci USA 107: 686-691.
4. Boukhalfa, H., and Crumbliss, A.L. (2002) Chemical aspects od siderophore mediated iron transport. Biometals 15: 325-339.
5. Braun, V., and Hantke, K. (2011) Recent insights into iron import by bacteria. Curr Opin Chem Biol 15: 328-334.
6. Briegel, A., Ortega, D.R., Tocheva, E.I., Wuichet, K., Li, Z., Chen, S., etal. (2009) Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci USA 106: 17181-17186.
7. Cantwell, B.J., Draheim, R.R., Weart, R.B., Nguyen, C., Stewart, R.C., and Manson, M.D. (2003) CheZ phosphatase localizes to chemoreceptor patches via CheA-short. J Bacteriol 185: 2354-2361.
8. Clément, E., Mesini, P.J., Pattus, F., Abdallah, M.A., and Schalk, I.J. (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.
9. Demange, P., Wendenbaum, S., Linget, C., Mertz, C., Cung, M.T., Dell, A., and Abdallah, M.A. (1990) Bacterial siderophores: structure and NMR assigment of pyoverdins PaA, siderophores of Pseudomonas aeruginosa ATCC 15692. Biol Met 3: 155-170.
10. Dworkin, J. (2009) Cellular polarity in Prokaryotic organisms. Cold Spring Harb Perspect Biol 1: a003368.
11. Goldberg, M.B., Barzu, O., Parsot, C., and Sansonetti, P.J. (1993) Unipolar localization and ATPase activity of IcsA, a Shigella flexneri protein involved in intracellular movement. J Bacteriol 175: 2189-2196.
12. Greenwald, J., Hoegy, F., Nader, M., Journet, L., Mislin, G.L.A., Graumann, P.L., and Schalk, I.J. (2007) Real-time FRET visualization of ferric-pyoverdine uptake in Pseudomonas aeruginosa: a role for ferrous iron. J Biol Chem 282: 2987-2995.
13. Gulick, A.M., and Drake, E.J. (2011) Structural characterization and high-throughput screening of inhibitors of PvdQ, an NTN Hydrolase involved in pyoverdine synthesis. ACS Chem Biol 6: 1277-1286.
14. Guvener, Z.T., Tifrea, D.F., and Harwood, C.S. (2006) Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase. Mol Microbiol 61: 106-118.
15. Hannauer, M., Yeterian, E., Martin, L.W., Lamont, I.L., and Schalk, I.J. (2010) Secretion of newly synthesized pyoverdine by Pseudomonas aeruginosa involves an efflux pump. FEBS Lett 584: 4751-4755.
16. Hannauer, M., Schäfer, M., Hoegy, F., Gizzi, P., Wehrung, P., Mislin, G.L.A., etal. (2012) Biosynthesis of the pyoverdine siderophore of Pseudomonas aeruginosa involves precursors with a myristic or a myristoleic acid chain. FEBS Lett 586: 96-101.
17. Harrison, D.M., Skidmore, J., Armitage, J.P., and Maddock, J.R. (1999) Localization and environmental regulation of MCP-like proteins in Rhodobacter sphaeroides. Mol Microbiol 31: 885-892.
18. Hider, R.C., and Kong, X. (2011) Chemistry and biology of siderophores. Nat Prod Rep 27: 637-657.
19. Imperi, F., Putignani, L., Tiburzi, F., Ambrosi, C., Cipollone, R., Ascenzi, P., and Visca, P. (2008) Membrane-association determinants of the omega-amino acid monooxygenase PvdA, a pyoverdine biosynthetic enzyme from Pseudomonas aeruginosa. Microbiology 154: 2804-2813.
20. Lamont, I.L., and Martin, L.W. (2003) Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa. Microbiology 149: 833-842.
21. Lewenza, S., Gardy, J.L., Brinkman, F.S., and Hancock, R.E. (2005) Genome-wide identification of Pseudomonas aeruginosa exported proteins using a consensus computational strategy combined with a laboratory-based PhoA fusion screen. Genome Res 15: 321-329.
22. Lindner, A.B., Madden, R., Demarez, A., Stewart, E.J., and Taddei, F. (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci USA 105: 3076-3081.
23. McMorran, B.J., Kumara, H.M., Sullivan, K., and Lamont, I.L. (2001) Involvement of a transformylase enzyme in siderophore synthesis in Pseudomonas aeruginosa. Microbiology 147: 1517-1524.
24. Martin, A.C., Wadhams, G.H., and Armitage, J.P. (2001) The roles of the multiple CheW and CheA homologues in chemotaxis and in chemoreceptor localization in Rhodobacter sphaeroides. Mol Microbiol 40: 1261-1272.
25. Meneely, K.M., Barr, E.W., Bollinger, J.M., Jr, and Lamb, A.L. (2009) Kinetic mechanism of ornithine hydroxylase (PvdA) from Pseudomonas aeruginosa: substrate triggering of O2 addition but not flavin reduction. Biochemistry 48: 4371-4376.
26. Meyer, J.M., and Abdallah, M.A. (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. J Gen Microbiol 107: 319-328.
27. Mossialos, D., Ochsner, U., Baysse, C., Chablain, P., Pirnay, J.P., Koedam, N., etal. (2002) Identification of new, conserved, non-ribosomal peptide synthetases from fluorescent pseudomonads involved in the biosynthesis of the siderophore pyoverdine. Mol Microbiol 45: 1673-1685.
28. Nadal Jimenez, P., Koch, G., Papaioannou, E., Wahjudi, M., Krzeslak, J., Coenye, T., etal. (2010) Role of PvdQ in Pseudomonas aeruginosa virulence under iron-limiting conditions. Microbiology 156: 49-59.
29. Nader, M., Journet, L., Meksem, A., Guillon, L., and Schalk, I.J. (2011) Mechanism of ferrisiderophore uptake by Pseudomonas aeruginosa outer membrane transporter FpvA: no diffusion channel formed at any time during ferrisiderophore uptake. Biochemistry 50: 2530-2540.
30. Ochsner, U.A., Wilderman, P.J., Vasil, A.I., and 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.
31. Oinonen, C., and Rouvinen, J. (2000) Structural comparison of Ntn-hydrolases. Protein Sci 9: 2329-2337.
32. Putignani, L., Ambrosi, C., Ascenzi, P., and Visca, P. (2004) Expression of L-ornithine Ndelta-oxygenase (PvdA) in fluorescent Pseudomonas species: an immunochemical and in silico study. Biochem Biophys Res Commun 313: 245-257.
33. Ravel, J., and Cornelis, P. (2003) Genomics of pyoverdine-mediated iron uptake in pseudomonads. Trends Microbiol 11: 195-200.
34. Rudner, D.Z., and Losick, R. (2010) Protein subcellular localization in bacteria. Cold Spring Harb Perspect Biol 2: a000307.
35. 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.
36. Schalk, I.J., Hennard, C., Dugave, C., Poole, K., Abdallah, M.A., and Pattus, F. (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.
37. Shapiro, L., McAdams, H.H., and Losick, R. (2002) Generating and exploiting polarity in bacteria. Science 298: 1942-1946.
38. Shapiro, L., McAdams, H.H., and Losick, R. (2009) Why and how bacteria localize proteins. Science 326: 1225-1228.
39. Simon, R., Priefer, U., and Puhler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram Negative bacteria. Nat Biotechnol 1: 784-791.
40. Sio, C.F., Otten, L.G., Cool, R.H., Diggle, S.P., Braun, P.G., Bos, R., etal. (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 74: 1673-1682.
41. Siroy, A., Cosette, P., Seyer, D., Lemaitre-Guillier, C., Vallenet, D., Van Dorsselaer, A., etal. (2006) Global comparison of the membrane subproteomes between a multidrug-resistant Acinetobacter baumannii strain and a reference strain. J Proteome Res 5: 3385-3398.
42. Smith, G.A., Portnoy, D.A., and Theriot, J.A. (1995) Asymmetric distribution of the Listeria monocytogenes ActA protein is required and sufficient to direct actin-based motility. Mol Microbiol 17: 945-951.
43. Sourjik, V. (2004) Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol 12: 569-576.
44. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., etal. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
45. Vandenende, C.S., Vlasschaert, M., and Seah, S.Y. (2004) Functional characterization of an aminotransferase required for pyoverdine siderophore biosynthesis in Pseudomonas aeruginosa PAO1. J Bacteriol 186: 5596-5602.
46. Visca, P., Ciervo, A., and Orsi, N. (1994) Cloning and nucleotide sequence of the pvdA gene encoding the pyoverdin biosynthetic enzyme L-ornithine N5-oxygenase in Pseudomonas aeruginosa. J Bacteriol 176: 1128-1140.
47. Visca, P., Imperi, F., and Lamont, I.L. (2007) Pyoverdine siderophores: from biogenesis to biosignificance. Trends Microbiol 15: 22-30.
48. Voisard, C., Bull, C., Keel, C., Laville, J., Maurhofer, M., Schnider, U., etal. (1994) Biocontrol of root diseases by Pseudomonas fluorescens CHAO: current concepts and experimental approaches. In Molecular Ecology of Rhizosphere Microorganisms. O'Gara, F., Dowling, D.N., and Boesten, B. (eds). Weinheim, Germany: VCH, pp. 67-89.
49. Voulhoux, R., Filloux, A., and Schalk, I.J. (2006) Role of the TAT System in the pyoverdine-mediated iron acquisition in Pseudomonas aeruginosa. J Bacteriol 188: 3317-3323.
50. Wang, L., Zhang, C., Gong, F., Li, H., Xie, X., Xia, C., etal. (2011) Influence of Pseudomonas aeruginosa pvdQ gene on altering antibiotic susceptibility under swarming conditions. Curr Microbiol 63: 377-386.
51. Ye, R.W., Haas, D., Ka, J.O., Krishnapillai, V., Zimmermann, A., Baird, C., and Tiedje, J.M. (1995) Anaerobic activation of the entire denitrification pathway in Pseudomonas aeruginosa requires Anr, an analog of Fnr. J Bacteriol 177: 3606-3609.
52. Yeterian, E., Martin, L.W., Guillon, L., Journet, L., Lamont, I.L., and Schalk, I.J. (2010a) Synthesis of the siderophore pyoverdine in Pseudomonas aeruginosa involves a periplasmic maturation. Amino Acids 38: 1447-1459.
53. Yeterian, E., Martin, L.W., Lamont, I.L., and Schalk, I.J. (2010b) An efflux pump is required for siderophore recycling by Pseudomonas aeruginosa. Environ Microbiol Rep 2: 412-418.