AlgW regulates multiple Pseudomonas syringae virulence strategies

Molecular Microbiology

Volumn 80, Issue 2, 2011, Pages 364-377

  Schreiber, Karl J ^a   Desveaux, Darrell ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID; FLAGELLIN; PROTEIN ALGW; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOSYNTHESIS; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; MICROBIAL ACTIVITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS SYRINGAE; REGULATORY MECHANISM; TYPE III SECRETION SYSTEM;

ALGINATES; BACTERIAL PROTEINS; FLAGELLIN; GENE EXPRESSION REGULATION, BACTERIAL; GLUCURONIC ACID; HEXURONIC ACIDS; IMMUNE EVASION; LOCOMOTION; PLANT DISEASES; PLANTS; PSEUDOMONAS SYRINGAE; REPRESSOR PROTEINS; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS SYRINGAE;

EID: 79954421075     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07571.x     Document Type: Article

References (76)

1. Akerley, B.J., Cotter, P.A., and Miller, J.F. (1995) Ectopic expression of the flagellar regulon alters development of the Bordetella-host interaction. Cell 80: 611-620.
2. Alexeyev, M.F., Shokolenko, I.N., and Croughan, T.P. (1995) New mini-Tn5 derivatives for insertion mutagenesis and genetic engineering in Gram-negative bacteria. Can J Microbiol 41: 1053-1055.
3. Arnold, C., and Hodgson, I.J. (1991) Vectorette PCR: a novel approach to genomic walking. PCR Methods Appl 1: 39-42.
4. Aslam, S.N., Newman, M.A., Erbs, G., Morrissey, K.L., Chinchilla, D., Boller, T., etal. (2008) Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr Biol 18: 1078-1083.
5. Boch, J., Joardar, V., Gao, L., Robertson, T.L., Lim, M., and Kunkel, B.N. (2002) Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol 44: 73-88.
6. Boller, T., and He, S.Y. (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742-744.
7. Boucher, J.C., Martinez-Salazar, J., Schurr, M.J., Mudd, M.H., Yu, H., and Deretic, V. (1996) Two distinct loci affecting conversion to mucoidy in Pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease HtrA. J Bacteriol 178: 511-523.
8. S form part of a cascade that controls alginate production in Azotobacter vinelandii. J Bacteriol 183: 6787-6793.
9. Cesbron, S., Paulin, J.P., Tharaud, M., Barny, M.A., and Brisset, M.N. (2006) The alternative sigma factor HrpL negatively modulates the flagellar system in the phytopathogenic bacterium Erwinia amylovora under hrp-inducing conditions. FEMS Microbiol Lett 257: 221-227.
10. Cezairliyan, B.O., and Sauer, R.T. (2009) Control of Pseudomonas aeruginosa AlgW protease cleavage of MucA by peptide signals and MucB. Mol Microbiol 72: 368-379.
11. Cobb, L.M., Mychaleckyj, J.C., Wozniak, D.J., and López-Boado, Y.S. (2004) Pseudomonas aeruginosa flagellin and alginate elicit very distinct gene expression patterns in airway epithelial cells: implications for cystic fibrosis disease. J Immunol 173: 5659-5670.
12. Coburn, J., and Frank, D.W. (1999) Macrophages and epithelial cells respond differently to the Pseudomonas aeruginosa type III secretion system. Infect Immun 67: 3151-3154.
13. Damron, F.H., Qiu, D., and Yu, H.W.D. (2009) The Pseudomonas aeruginosa sensor kinase KinB negatively controls alginate production through AlgW-dependent MucA proteolysis. J Bacteriol 191: 2285-2295.
14. DeVault, J.D., Kimbara, K., and Chakrabarty, A.M. (1990) Pulmonary dehydration and infection in cystic fibrosis: evidence that ethanol activates alginate gene expression and induction of mucoidy in Pseudomonas aeruginosa. Mol Microbiol 4: 737-745.
15. Ellermeier, C.D., and Slauch, J.M. (2003) RtsA and RtsB coordinately regulate expression of the invasion and flagellar genes in Salmonella enterica serovar Typhimurium. J Bacteriol 185: 5096-5108.
16. Felix, G., Duran, J.D., Volko, S., and Boller, T. (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265-276.
17. Galan, J.E., and Collmer, A. (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284: 1322-1328.
18. Garrett, E.S., Perlegas, D., and Wozniak, D.J. (1999) Negative control of flagellum synthesis in Pseudomonas aeruginosa is modulated by the alternative sigma factor AlgT (AlgU). J Bacteriol 181: 7401-7404.
19. Godfrey, S., Mansfield, J.W., Corry, D., Lovell, H., Jackson, R., and Arnold, D. (2010) Confocal imaging of Pseudomonas syringae pv. phaseolicola colony development in bean reveals reduced multiplication of strains containing the genomic island PPHGI-1. Mol Plant Microbe Interact 23: 1294-1302.
20. Gómez-Gómez, L., Felix, G., and Boller, T. (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284.
21. Guenin-Macé, L., Siméone, R., and Demangel, C. (2009) Lipids of pathogenic Mycobacteria: contributions to virulence and host immune suppression. Transbound Emerg Dis 56: 255-268.
22. Guo, M., Tian, F., Wamboldt, Y., and Alfano, J.R. (2009) The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Mol Plant Microbe Interact 22: 1069-1080.
23. Hauser, A.R. (2009) The type III secretion system of Pseudomonas aeruginosa: infection by injection. Nat Rev Microbiol 7: 654-665.
24. Hauser, A.R., and Engel, J.N. (1999) Pseudomonas aeruginosa induces type-III-secretion-mediated apoptosis of macrophages and epithelial cells. Infect Immun 67: 5530-5537.
25. Hickman, J.W., and Harwood, C.S. (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69: 376-389.
26. Huynh, T.V., Dahlbeck, D., and Staskawicz, B.J. (1989) Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245: 1374-1377.
27. Ichinose, Y., Shimizu, R., Ikeda, Y., Taguchi, F., Marutani, M., Mukaihara, T., etal. (2003) Need for flagella for complete virulence of Pseudomonas syringae pv. tabaci: genetic analysis with flagella-defective mutants ΔfliC and ΔfliD in host tobacco plants. J Gen Plant Pathol 69: 244-249.
28. Jones, J.D.G., and Dangl, J.L. (2006) The plant immune system. Nature 444: 323-329.
29. Katagiri, F., Thilmony, R., and He, S.Y. (2002) The Arabidopsis thaliana-Pseudomonas syringae interaction. The Arabidopsis Book 1: e0039. doi:10.1199/tab.0039.
30. 22) controls alginate production and tolerance to environmental stress in Pseudomonas syringae. J Bacteriol 181: 7176-7184.
31. Keith, R.C., Keith, L.M.W., Hernández-Guzmán, G., Uppalapati, S.R., and Bender, C.L. (2003) Alginate gene expression by Pseudomonas syringae pv. tomato DC3000 in host and non-host plants. Microbiology 149: 1127-1138.
32. King, E.O., Ward, M.K., and Raney, D.E. (1954) Two simple media for the demonstration of pyocyanin and fluorescin. J Lab Clin Med 44: 301-307.
33. Kvitko, B.H., Park, D.H., Velásquez, A.C., Wei, C.F., Russell, A.B., Martin, G.B., etal. (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog 5: e1000388.
34. Lan, L.F., Deng, X., Zhou, J.M., and Tang, X.Y. (2006) Genome-wide gene expression analysis of Pseudomonas syringae pv. tomato DC3000 reveals overlapping and distinct pathways regulated by hrpL and hrpRS. Mol Plant Microbe Interact 19: 976-987.
35. Leid, J.G., Willson, C.J., Shirtliff, M.E., Hassett, D.J., Parsek, M.R., and Jeffers, A.K. (2005) The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-γ-mediated macrophage killing. J Immunol 175: 7512-7518.
36. Lewis, J.D., Guttman, D.S., and Desveaux, D. (2009) The targeting of plant cellular systems by injected type III effector proteins. Semin Cell Dev Biol 20: 1055-1063.
37. Li, X.Y., Lin, H.Q., Zhang, W.G., Zou, Y., Zhang, J., Tang, X.Y., etal. (2005) Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Nat Acad Sci USA 102: 12990-12995.
38. -ΔΔCT method. Methods 25: 402-408.
39. Marlovits, T.C., and Stebbins, C.E. (2010) Type III secretion systems shape up as they ship out. Curr Opin Microbiol 13: 47-52.
40. E and stress response. J Bacteriol 176: 6688-6696.
41. May, T.B., and Chakrabarty, A.M. (1994) Isolation and assay of Pseudomonas aeruginosa alginate. Methods Enzymol 235: 295-304.
42. Naito, K., Taguchi, F., Suzuki, T., Inagaki, Y., Toyoda, K., Shiraishi, T., etal. (2008) Amino acid sequence of bacterial microbe-associated molecular pattern flg22 is required for virulence. Mol Plant Microbe Interact 21: 1165-1174.
43. Nguyen, L.C., Yamamoto, M., Ohnishi-Kameyama, M., Andi, S., Taguchi, F., Iwaki, M., etal. (2009) Genetic analysis of genes involved in synthesis of modified 4-amino-4, 6-dideoxyglucose in flagellin of Pseudomonas syringae pv. tabaci. Mol Genet Genomics 282: 595-605.
44. Ormonde, P., Hörstedt, P., O'Toole, R., and Milton, D.L. (2000) Role of motility in adherence to and invasion of a fish cell line by Vibrio anguillarum. J Bacteriol 182: 2326-2328.
45. Ortiz-Martín, I., Thwaites, R., Macho, A.P., Mansfield, J.W., and Beuzón, C.R. (2010) Positive regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. Mol Plant Microbe Interact 23: 665-681.
46. Pier, G.B. (2007) Pseudomonas aeruginosa lipopolysaccharide: a major virulence factor, initiator of inflammation and target for effective immunity. Int J Med Microbiol 297: 277-295.
47. Pier, G.B., Coleman, F., Grout, M., Franklin, M., and Ohman, D.E. (2001) Role of alginate O acetylation in resistance of mucoid Pseudomonas aeruginosa to opsonic phagocytosis. Infect Immun 69: 1895-1901.
48. Pitzschke, A., Schikora, A., and Hirt, H. (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12: 421-426.
49. Qiu, D.R., Eisinger, V.M., Rowen, D.W., and Yu, H.W.D. (2007) Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa. Proc Nat Acad Sci USA 104: 8107-8112.
50. Rainey, P.B., Heithoff, D.M., and Mahan, M.J. (1997) Single-step conjugative cloning of bacterial gene fusions involved in microbe-host interactions. Mol Gen Genet 256: 84-87.
51. Rico, A., and Preston, G.M. (2008) Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol Plant Microbe Interact 21: 269-282.
52. Schenk, A., Berger, M., Keith, L.M., Bender, C.L., Muskhelishvili, G., and Ullrich, M.S. (2006) The algT gene of Pseudomonas syringae pv. glycinea and new insights into the transcriptional organization of the algT-muc gene cluster. J Bacteriol 188: 8013-8021.
53. Schnider-Keel, U., Lejbølle, K.B., Baehler, E., Haas, D., and Keel, C. (2001) The sigma factor AlgU (AlgT) controls exopolysaccharide production and tolerance towards desiccation and osmotic stress in the biocontrol agent Pseudomonas fluorescens CHA0. Appl Environ Microbiol 67: 5683-5693.
54. E) which controls mucoidy in cystic fibrosis isolates of Pseudomonas aeruginosa. J Bacteriol 177: 5670-5679.
55. Schwessinger, B., and Zipfel, C. (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11: 389-395.
56. Shimizu, R., Taguchi, F., Marutani, M., Mukaihara, T., Inagaki, Y., Toyoda, K., etal. (2003) The ΔfliD mutant of Pseudomonas syringae pv. tabaci, which secretes flagellin monomers, induces a strong hypersensitive reaction (HR) in non-host tomato cells. Mol Genet Genomics 269: 21-30.
57. Silipo, A., Erbs, G., Shinya, T., Dow, J.M., Parrilli, M., Lanzetta, R., etal. (2010) Glyco-conjugates as elicitors or suppressors of plant innate immunity. Glycobiology 20: 406-419.
58. Simpson, J.A., Smith, S.E., and Dean, R.T. (1988) Alginate inhibition of the uptake of Pseudomonas aeruginosa by macrophages. J Gen Microbiol 134: 29-36.
59. Simpson, J.A., Smith, S.E., and Dean, R.T. (1989) Scavenging by alginate of free radicals released by macrophages. Free Radic Biol Med 6: 347-353.
60. Taguchi, F., Takeuchi, K., Katoh, E., Murata, K., Suzuki, T., Marutani, M., etal. (2006) Identification of glycosylation genes and glycosylated amino acids of flagellin in Pseudomonas syringae pv. tabaci. Cell Microbiol 8: 923-938.
61. Tang, X.Y., Xiao, Y.M., and Zhou, J.M. (2006) Regulation of the type III secretion system in phytopathogenic bacteria. Mol Plant Microbe Interact 19: 1159-1166.
62. Tans-Kersten, J., Huang, H.Y., and Allen, C. (2001) Ralstonia solanacearum needs motility for invasive virulence on tomato. J Bacteriol 183: 3597-3605.
63. Tart, A.H., Wolfgang, M.C., and Wozniak, D.J. (2005) The alternative sigma factor AlgT represses Pseudomonas aeruginosa flagellum biosynthesis by inhibiting expression of fleQ. J Bacteriol 187: 7955-7962.
64. Tart, A.H., Blanks, M.J., and Wozniak, D.J. (2006) The AlgT-dependent transcriptional regulator AmrZ (AlgZ) inhibits flagellum biosynthesis in mucoid, nonmotile Pseudomonas aeruginosa cystic fibrosis isolates. J Bacteriol 188: 6483-6489.
65. Truman, W., de Zabala, M.T., and Grant, M. (2006) Type III effectors orchestrate a complex interplay between transcriptional networks to modify basal defence responses during pathogenesis and resistance. Plant J 46: 14-33.
66. Wang, L.H., and Ligoxygakis, P. (2006) Pathogen recognition and signalling in the Drosophila innate immune response. Immunobiology 211: 251-261.
67. West, S.E.H., Schweizer, H.P., Dall, C., Sample, A.K., and Runyenjanecky, L.J. (1994) Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148: 81-86.
68. Wolfgang, M.C., Jyot, J., Goodman, A.L., Ramphal, R., and Lory, S. (2004) Pseudomonas aeruginosa regulates flagellin expression as part of a global response to airway fluid from cystic fibrosis patients. Proc Nat Acad Sci USA 101: 6664-6668.
69. 22 (AlgT/U) activation by regulated proteolysis and its regulon in Pseudomonas aeruginosa. Mol Microbiol 72: 183-201.
70. 22 (AlgT) and the AlgW and Prc proteases. Mol Microbiol 62: 412-426.
71. Wu, W.H., Badrane, H., Arora, S., Baker, H.V., and Jin, S.G. (2004) MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J Bacteriol 186: 7575-7585.
72. Xiao, Y.X., Lu, Y., Heu, S.G., and Hutcheson, S.W. (1992) Organization and environmental regulation of the Pseudomonas syringae pv. syringae 61 hrp cluster. J Bacteriol 174: 1734-1741.
73. E). Infect Immun 64: 2774-2781.
74. Yu, J., Peñaloza-Vázquez, A., Chakrabarty, A.M., and Bender, C.L. (1999) Involvement of the exopolysaccharide alginate in the virulence and epiphytic fitness of Pseudomonas syringae pv. syringae. Mol Microbiol 33: 712-720.
75. Zhang, M.Y., Lovgren, A., Low, M.G., and Landen, R. (1993) Characterization of an avirulent pleiotropic mutant of the insect pathogen Bacillus thuringiensis: reduced expression of flagellin and phospholipases. Infect Immun 61: 4947-4954.
76. Zielinski, N.A., Maharaj, R., Roychoudhury, S., Danganan, C.E., Hendrickson, W., and Chakrabarty, A.M. (1992) Alginate synthesis in Pseudomonas aeruginosa: environmental regulation of the algC promoter. J Bacteriol 174: 7680-7688.