The pathogenicity island encoded PvrSR/RcsCB regulatory network controls biofilm formation and dispersal in Pseudomonas aeruginosa PA14

Molecular Microbiology

Volumn 89, Issue 3, 2013, Pages 450-463

  Mikkelsen, Helga ^a   Hui, Kailyn ^a   Barraud, Nicolas ^b   Filloux, Alain ^a  

^a MEDICAL RESEARCH COUNCIL   (United Kingdom)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATASE; PHOSPHODIESTERASE; PHOSPHOTRANSFERASE; PROTEIN PVRS; PROTEIN PVRSR; PROTEIN RCSB; PROTEIN RCSC; PROTEIN RCSCB; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; CUPD GENE; ENZYME ACTIVITY; GENE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; MICROARRAY ANALYSIS; NONHUMAN; PATHOGENICITY ISLAND; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PVRR GENE;

BACTERIAL PROTEINS; BIOFILMS; GENE EXPRESSION REGULATION, BACTERIAL; GENE REGULATORY NETWORKS; GENOMIC ISLANDS; MULTIGENE FAMILY; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHOTRANSFERASES; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION MAPPING; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

EID: 84880822645     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12287     Document Type: Article

References (54)

1. Bourret, R.B. (2010) Receiver domain structure and function in response regulator proteins. Curr Opin Microbiol 13: 142-149.
2. Breidenstein, E.B., de la Fuente-Nunez, C., and Hancock, R.E. (2011) Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol 19: 419-426.
3. Carter, M.Q., Chen, J., and Lory, S. (2010) The Pseudomonas aeruginosa pathogenicity island PAPI-1 is transferred via a novel type IV pilus. J Bacteriol 192: 3249-3258.
4. Cho, H.S., Lee, S.Y., Yan, D., Pan, X., Parkinson, J.S., Kustu, S., etal. (2000) NMR structure of activated CheY. J Mol Biol 297: 543-551.
5. Chung, I.Y., Choi, K.B., Heo, Y.J., and Cho, Y.H. (2008) Effect of PEL exopolysaccharide on the wspF mutant phenotypes in Pseudomonas aeruginosa PA14. J Microbiol Biotechnol 18: 1227-1234.
6. Clarke, D.J. (2010) The Rcs phosphorelay: more than just a two-component pathway. Future Microbiol 5: 1173-1184.
7. Drenkard, E., and Ausubel, F.M. (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740-743.
8. Filloux, A. (2010) A variety of bacterial pili involved in horizontal gene transfer. J Bacteriol 192: 3243-3245.
9. Galperin, M.Y. (2010) Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 13: 150-159.
10. Giraud, C., and de Bentzmann, S. (2012) Inside the complex regulation of Pseudomonas aeruginosa chaperone usher systems. Environ Microbiol 14: 1805-1816.
11. Giraud, C., Bernard, C.S., Calderon, V., Yang, L., Filloux, A., Molin, S., etal. (2011) The PprA-PprB two-component system activates CupE, the first non-archetypal Pseudomonas aeruginosa chaperone-usher pathway system assembling fimbriae. Environ Microbiol 13: 666-683.
12. Goodman, A.L., Kulasekara, B., Rietsch, A., Boyd, D., Smith, R.S., and Lory, S. (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7: 745-754.
13. Goodman, A.L., Merighi, M., Hyodo, M., Ventre, I., Filloux, A., and Lory, S. (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23: 249-259.
14. Harmsen, M., Yang, L., Pamp, S.J., and Tolker-Nielsen, T. (2010) An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59: 253-268.
15. He, J., Baldini, R.L., Deziel, E., Saucier, M., Zhang, Q., Liberati, N.T., etal. (2004) The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc Natl Acad Sci USA 101: 2530-2535.
16. Hoang, T.T., Kutchma, A.J., Becher, A., and Schweizer, H. (2000) Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43: 59-72.
17. Huynh, T.N., and Stewart, V. (2011) Negative control in two-component signal transduction by transmitter phosphatase activity. Mol Microbiol 82: 275-286.
18. Huynh, T.N., Noriega, C.E., and Stewart, V. (2010) Conserved mechanism for sensor phosphatase control of two-component signaling revealed in the nitrate sensor NarX. Proc Natl Acad Sci USA 107: 21140-21145.
19. Jenal, U., and Galperin, M.Y. (2009) Single domain response regulators: molecular switches with emerging roles in cell organization and dynamics. Curr Opin Microbiol 12: 152-160.
20. Karimova, G., Pidoux, J., Ullmann, A., and Ladant, D. (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756.
21. Kelley, L.A., and Sternberg, M.J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
22. Kovach, M.E., Elzer, P.H., Hill, D.S., Robertson, G.T., Farris, M.A., Roop, R.M., 2nd, and Peterson, K.M. (1995) Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166: 175-176.
23. Krasteva, P.V., Fong, J.C., Shikuma, N.J., Beyhan, S., Navarro, M.V., Yildiz, F.H., and Sondermann, H. (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327: 866-868.
24. Kulasakara, H., Lee, V., Brencic, A., Liberati, N., Urbach, J., Miyata, S., etal. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103: 2839-2844.
25. Kulasekara, B., and Lory, S. (2004) The genome of Pseudomonas aeruginosa. In Pseudomonas, Vol. 1. Ramos, J.L. (ed.). New York: Kluwer Academic/Plenum Publishers, pp. 47-75.
26. Kulasekara, H.D., Ventre, I., Kulasekara, B.R., Lazdunski, A., Filloux, A., and Lory, S. (2005) A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 55: 368-380.
27. Liberati, N.T., Urbach, J.M., Miyata, S., Lee, D.G., Drenkard, E., Wu, G., etal. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci USA 103: 2833-2838.
28. Majdalani, N., and Gottesman, S. (2005) The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol 59: 379-405.
29. Mao, F., Dam, P., Chou, J., Olman, V., and Xu, Y. (2009) DOOR: a database for prokaryotic operons. Nucleic Acids Res 37: D459-D463.
30. Meissner, A., Wild, V., Simm, R., Rohde, M., Erck, C., Bredenbruch, F., etal. (2007) Pseudomonas aeruginosa cupA-encoded fimbriae expression is regulated by a GGDEF and EAL domain-dependent modulation of the intracellular level of cyclic diguanylate. Environ Microbiol 9: 2475-2485.
31. Mikkelsen, H., Ball, G., Giraud, C., and Filloux, A. (2009) Expression of Pseudomonas aeruginosa cupD fimbrial genes is antagonistically controlled by RcsB and the EAL-containing PvrR response regulators. PLoS ONE 4: e6018.
32. Mikkelsen, H., Sivaneson, M., and Filloux, A. (2011) Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ Microbiol 13: 1666-1681.
33. Miller, J.H. (1992) A Short Course in Bacterial Genetics: A Laboratory Manual and Handbook for Escherichia coli and Related Bacteria. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
34. Moscoso, J.A., Mikkelsen, H., Heeb, S., Williams, P., and Filloux, A. (2011) The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ Microbiol 13: 3128-3138.
35. Newman, J.R., and Fuqua, C. (1999) Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227: 197-203.
36. Nicastro, G.G., Boechat, A.L., Abe, C.M., Kaihami, G.H., and Baldini, R.L. (2009) Pseudomonas aeruginosa PA14 cupD transcription is activated by the RcsB response regulator, but repressed by its putative cognate sensor RcsC. FEMS Microbiol Lett 301: 115-123.
37. Paul, K., Brunstetter, D., Titen, S., and Blair, D.F. (2011) A molecular mechanism of direction switching in the flagellar motor of Escherichia coli. Proc Natl Acad Sci USA 108: 17171-17176.
38. Qaisar, U., Luo, L., Haley, C.L., Brady, S.F., Carty, N.L., Colmer-Hamood, J.A., and Hamood, A.N. (2013) The pvc operon regulates the expression of the Pseudomonas aeruginosa fimbrial chaperone/usher pathway (Cup) genes. PLoS ONE 8: e62735.
39. Rampioni, G., Pustelny, C., Fletcher, M.P., Wright, V.J., Bruce, M., Rumbaugh, K.P., etal. (2010) Transcriptomic analysis reveals a global alkyl-quinolone-independent regulatory role for PqsE in facilitating the environmental adaptation of Pseudomonas aeruginosa to plant and animal hosts. Environ Microbiol 12: 1659-1673.
40. Rodrigue, A., Quentin, Y., Lazdunski, A., Mejean, V., and Foglino, M. (2000) Two-component systems in Pseudomonas aeruginosa: why so many? Trends Microbiol 8: 498-504.
41. Ruer, S., Stender, S., Filloux, A., and de Bentzmann, S. (2007) Assembly of fimbrial structures in Pseudomonas aeruginosa: functionality and specificity of chaperone-usher machineries. J Bacteriol 189: 3547-3555.
42. Ruer, S., Ball, G., Filloux, A., and de Bentzmann, S. (2008) The 'P-usher', a novel protein transporter involved in fimbrial assembly and TpsA secretion. EMBO J 27: 2669-2680.
43. Sivaneson, M., Mikkelsen, H., Ventre, I., Bordi, C., and Filloux, A. (2011) Two-component regulatory systems in Pseudomonas aeruginosa: an intricate network mediating fimbrial and efflux pump gene expression. Mol Microbiol 79: 1353-1366.
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. Tomich, M., and Mohr, C.D. (2004a) Genetic characterization of a multicomponent signal transduction system controlling the expression of cable pili in Burkholderia cenocepacia. J Bacteriol 186: 3826-3836.
46. Tomich, M., and Mohr, C.D. (2004b) Transcriptional and posttranscriptional control of cable pilus gene expression in Burkholderia cenocepacia. J Bacteriol 186: 1009-1020.
47. Valle, J., Da Re, S., Henry, N., Fontaine, T., Balestrino, D., Latour-Lambert, P., and Ghigo, J.M. (2006) Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci USA 103: 12558-12563.
48. Vallet, I., Olson, J.W., Lory, S., Lazdunski, A., and Filloux, A. (2001) The chaperone/usher pathways of Pseudomonas aeruginosa: identification of fimbrial gene clusters (cup) and their involvement in biofilm formation. Proc Natl Acad Sci USA 98: 6911-6916.
49. Vallet, I., Diggle, S.P., Stacey, R.E., Camara, M., Ventre, I., Lory, S., etal. (2004) Biofilm formation in Pseudomonas aeruginosa: fimbrial cup gene clusters are controlled by the transcriptional regulator MvaT. J Bacteriol 186: 2880-2890.
50. Ventre, I., Goodman, A.L., Vallet-Gely, I., Vasseur, P., Soscia, C., Molin, S., etal. (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA 103: 171-176.
51. Waksman, G., and Hultgren, S.J. (2009) Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Microbiol 7: 765-774.
52. Waters, C.M., and Bassler, B.L. (2006) The Vibrio harveyi quorum-sensing system uses shared regulatory components to discriminate between multiple autoinducers. Genes Dev 20: 2754-2767.
53. Wehland, M., and Bernhard, F. (2000) The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J Biol Chem 275: 7013-7020.
54. Whitworth, D.E. (2012) Two-component regulatory systems in prokaryotes. In Bacterial Regulatory Networks. Filloux, A.M. (ed.). Norfolk, UK: Caister Academic Press, pp. 191-222.