The Pseudomonas aeruginosa phosphate transport protein PstS plays a phosphate-independent role in biofilm formation

FASEB Journal

Volumn 28, Issue 12, 2014, Pages 5223-5233

  Neznansky, Avi ^a   Blus Kadosh, Inna ^a   Yerushalmi, Gal ^a   Banin, Ehud ^a   Opatowsky, Yarden ^a  

^a BAR ILAN UNIVERSITY   (Israel)

Author keywords

N loop; Substrate binding protein; Swarming

Indexed keywords

PHOSPHATE TRANSPORTER; PSTS PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PHOSPHATE; PHOSPHATE BINDING PROTEIN; PRIMER DNA;

ARTICLE; BIOFILM; CONTROLLED STUDY; CRYSTAL STRUCTURE; MUTAGENESIS; MUTANT; NONHUMAN; ORTHOLOGY; PHOSPHATE TRANSPORT; POINT MUTATION; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY; CHEMISTRY; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN CONFORMATION;

PSEUDOMONAS AERUGINOSA;

BACTERIAL PROTEINS; BASE SEQUENCE; BIOFILMS; DNA PRIMERS; PHOSPHATE-BINDING PROTEINS; PHOSPHATES; PROTEIN CONFORMATION; PSEUDOMONAS AERUGINOSA;

EID: 84919784624     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-258293     Document Type: Article

References (45)

1. Gerdes, R. G., Strickland, K. P., and Rosenberg, H. (1977) Restoration of phosphate transport by the phosphate-binding protein in spheroplasts of Escherichia coli. J. Bacteriol. 131, 512-518
2. Ames, G. F. (1986) Bacterial periplasmic transport systems: structure, mechanism, and evolution. Annu. Rev. Biochem. 55, 397-425
3. Van Veen, H. W. (1997) Phosphate transport in prokaryotes: molecules, mediators and mechanisms. Antonie Van Leeuwenhoek 72, 299-315
4. Blus-Kadosh, I., Zilka, A., Yerushalmi, G., and Banin, E. The effect of pstS and phoB on quorum sensing and swarming motility in Pseudomonas aeruginosa. PLoS One 8, e74444
5. Nikata, T., Sakai, Y., Shibat, K., Kato, J., Kuroda, A., and Ohtake, H. (1996) Molecular analysis of the phosphate-specific transport (pst) operon of Pseudomonas aeruginosa. Mol. Gen. Genet. 250, 692-698
6. Neznansky, A., and Opatowsky, Y. (2014) Expression, purification and crystallization of the phosphate-binding PstS protein from Pseudomonas aeruginosa. Acta Crystallogr. F Struct. Biol. Commun. 70, 5
7. Vyas, N. K., Vyas, M. N., and Quiocho, F. A. (2003) Crystal structure of M tuberculosis ABC phosphate transport receptor: specificity and charge compensation dominated by ion-dipole interactions. Structure 11, 765-774
8. Espitia, C., and Mancilla, R. (1989) Identification, isolation and partial characterization of Mycobacterium tuberculosis glycoprotein antigens. Clin. Exp. Immunol. 77, 378-383
9. Wang, Z., Choudhary, A., Ledvina, P. S., and Quiocho, F. A. (1994) Fine tuning the specificity of the periplasmic phosphate transport receptor. Site-directed mutagenesis, ligand binding, and crystallographic studies. J. Biol. Chem. 269, 25091-25094
10. Esteban, A., Diaz, M., Yepes, A., and Santamaria, R. I. (2008) Expression of the pstS gene of Streptomyces lividans is regulated by the carbon source and is partially independent of the PhoP regulator. BMC Microbiol. 8, 201
11. Diaz, M., Esteban, A., Fernandez-Abalos, J. M., and Santamaria, R. I. (2005) The high-affinity phosphate-binding protein PstS is accumulated under high fructose concentrations and mutation of the corresponding gene affects differentiation in Streptomyces lividans. Microbiology 151, 2583-2592
12. Young, D. B., and Garbe, T. R. (1991) Lipoprotein antigens of Mycobacterium tuberculosis. Res. Microbiol. 142, 55-65
13. Zaborina, O., Holbrook, C., Chen, Y. M., Long, J., Zaborin, A., Morozova, I., Fernandez, H., Wang, Y. M., Turner, J. R., and Alverdy, J. C. (2008) Structure-function aspects of PstS in multi-drug-resistant Pseudomonas aeruginosa. PLoS Pathog. 4, e43
14. Bastonero, S., Le Priol, Y., Armand, M., Bernard, C. S., Reynaud-Gaubert, M., Olive, D., Parzy, D., de Bentzmann, S., Capo, C., and Mege, J. L. (2009) New microbicidal functions of tracheal glands: defective anti-infectious response to Pseudomonas aeruginosa in cystic fibrosis. PLoS One 4, e5357
15. Shah, M., Zaborin, A., Alverdy, J. C., Scott, K., and Zaborina, O. (2013) Localization of DING proteins on PstS-containing outer-surface appendages of Pseudomonas aeruginosa. FEMS Microbiol. Lett. 352, 54-61
16. O'May, G. A., Jacobsen, S. M., Longwell, M., Stoodley, P., Mobley, H. L., and Shirtliff, M. E. (2009) The high-affinity phosphate transporter Pst in Proteus mirabilis HI4320 and its importance in biofilm formation. Microbiology 155, 1523-1535
17. Mudrak, B., and Tamayo, R. The Vibrio cholerae Pst2 phosphate transport system is upregulated in biofilms and contributes to biofilm-induced hyperinfectivity. Infect. Immun. 80, 1794-1802
18. Monds, R. D., Silby, M. W., and Mahanty, H. K. (2001) Expression of the Pho regulon negatively regulates biofilm formation by Pseudomonas aureofaciens PA147-2. Mol. Microbiol. 42, 415-426
19. Krug, M., Weiss, M. S., Heinemann, U., and Mueller, U. (2012) XDSAPP: a graphical user interface for the convenient processing of diffraction data using XDS. J. Appl. Crystallogr. 45, 5
20. Long, F., Vagin, A. A., Young, P., and Murshudov, G. N. (2008) BALBES: a molecular-replacement pipeline. Acta Crystallogr. D Biol. Crystallogr. 64, 125-132
21. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
22. Joosten, R. P. J. K., Murshudov, G. N., and Perrakis, A. (2012) PDB-REDO: constructive validation, more than just looking for errors. Acta Crystallogr. D Biol. Crystallogr. 68, 13
23. Rybtke, M. T., Borlee, B. R., Murakami, K., Irie, Y., Hentzer, M., Nielsen, T. E., Givskov, M., Parsek, M. R., and Tolker-Nielsen, T. (2012) Fluorescence-based reporter for gauging cyclic di-GMP levels in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 78, 5060-5069
24. Choi, K. H., and Schweizer, H. P. (2005) An improved method for rapid generation of unmarked Pseudomonas aeruginosa deletion mutants. BMC Microbiol. 5, 30
25. Lewenza, S., Falsafi, R. K., Winsor, G., Gooderham, W. J., McPhee, J. B., Brinkman, F. S., and Hancock, R. E. (2005) Construction of a mini-Tn5-luxCDABE mutant library in Pseudomonas aeruginosa PAO1: a tool for identifying differentially regulated genes. Genome. Res. 15, 583-589
26. Schweizer, H. P., and Hoang, T. T. (1995) An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158, 15-22
27. Hou, C. I., Gronlund, A. F., and Campbell, J. J. (1966) Influence of phosphate starvation on cultures of Pseudomonas aeruginosa. J. Bacteriol. 92, 851-855
28. Weiss Nielsen, M., Sternberg, C., Molin, S., and Regenberg, B. (2011) Pseudomonas aeruginosa and Saccharomyces cerevisiae biofilm in flow cells. J. Vis. Exp. 47, pii2383
29. Mueller, L. N., de Brouwer, J. F., Almeida, J. S., Stal, L. J., and Xavier, J. B. (2006) Analysis of a marine phototrophic biofilm by confocal laser scanning microscopy using the new image quantification software PHLIP. BMC Ecol. 6, 1
30. Berntsson, R. P., Smits, S. H., Schmitt, L., Slotboom, D. J., and Poolman, B. A structural classification of substrate-binding proteins. FEBS Lett. 584, 2606-2617
31. Hollenstein, K., Frei, D. C., and Locher, K. P. (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446, 213-216
32. Laskowski, R. A., and Swindells, M. B. LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J. Chem. Inf. Model. 51, 2778-2786
33. Garnett, J. A., and Matthews, S. (2013) Interactions in bacterial biofilm development: a structural perspective. Curr. Protein Pept. Sci. 13, 739-755
34. Bains, M., Fernandez, L., and Hancock, R. E. Phosphate starvation promotes swarming motility and cytotoxicity of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 78, 6762-6768
35. Fischer, R. J., Oehmcke, S., Meyer, U., Mix, M., Schwarz, K., Fiedler, T., and Bahl, H. (2006) Transcription of the pst operon of Clostridium acetobutylicum is dependent on phosphate concentration and pH. J. Bacteriol. 188, 5469-5478
36. Madhusudhan, K. T., McLaughlin, R., Komori, N., and Matsumoto, H. (2003) Identification of a major protein upon phosphate starvation of Pseudomonas aeruginosa PAO1. J. Basic Microbiol. 43, 36-46
37. Duque, E., de la Torre, J., Bernal, P., Molina-Henares, M. A., Alaminos, M., Espinosa-Urgel, M., Roca, A., Fernandez, M., de Bentzmann, S., and Ramos, J. L. Identification of reciprocal adhesion genes in pathogenic and non-pathogenic Pseudomonas. Environ. Microbiol. 15, 36-48
38. Monds, R. D., Newell, P. D., Gross, R. H., and O'Toole, G. A. (2007) Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol. Microbiol. 63, 656-679
39. Paas, Y. (1998) The macro- and microarchitectures of the ligand-binding domain of glutamate receptors. Trends Neurosci. 21, 117-125
40. Borlee, B. R., Goldman, A. D., Murakami, K., Samudrala, R., Wozniak, D. J., and Parsek, M. R. Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75, 827-842
41. Romero, D., Aguilar, C., Losick, R., and Kolter, R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc. Natl. Acad. Sci. U.S.A. 107, 2230-2234
42. Holloway, B. W., Krishnapillai, V., and Morgan, A. F. (1979) Chromosomal genetics of Pseudomonas. Microbiol. Rev. 43, 73-102
43. Blus-Kadosh, I., Zilka, A., Yerushalmi, G., and Banin, E. (2013) The Effect of pstS and phoB on quorum sensing and swarming motility in Pseudomonas aeruginosa. PloS One. 8, e74444
44. Woodcock, D. M., Crowther, P. J., Doherty, J., Jefferson, S., DeCruz, E., Noyer-Weidner, M., Smith, S. S., Michael, M. Z., and Graham, M. W. (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 17, 3469-3478
45. Schweizer, H. P. (1991) Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene 97, 109-121