The Gac-Rsm and SadB signal transduction pathways converge on Algu to downregulate motility in Pseudomonas fluorescens

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Martínez Granero, Francisco ^a   Navazo, Ana ^a   Barahona, Emma ^a   Redondo Nieto, Miguel ^a   Rivilla, Rafael ^a   Martín, Marta ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; PROTEIN ALGU; PROTEIN FLEQ; PROTEIN MUCA; PROTEIN MUCB; PROTEIN MUCD; PROTEIN RSMA; PROTEIN RSME; PROTEIN SADB; REPRESSOR PROTEIN; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN;

ALGU GENE; AMRZ GENE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; DOWN REGULATION; FLAGELLUM; FLEQ GENE; GENE EXPRESSION; IMMUNOPRECIPITATION; MUCA GENE; MUCB GENE; MUCD GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PROTEIN BINDING; PSEUDOMONAS FLUORESCENS; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSMISSION ELECTRON MICROSCOPY; BIOLOGICAL MODEL; CYTOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MOVEMENT (PHYSIOLOGY); ULTRASTRUCTURE;

BACTERIAL PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; MODELS, BIOLOGICAL; MOVEMENT; PROTEIN BINDING; PSEUDOMONAS FLUORESCENS; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84857385762     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031765     Document Type: Article

References (73)

1. de Souza JT, Mazzola M, Raaijmakers JM, (2003) Conservation of the response regulator gene gacA in Pseudomonas species. Environ Microbiol 5: 1328-1340.
2. Heeb S, Haas D, (2001) Regulatory roles of the GacS/GacA two-component system in plant-associated and other Gram-negative bacteria. Mol Plant Microbe Interact 14: 1351-1363.
3. Hassan KA, Johnson A, Shaffer BT, Ren Q, Kidarsa TA, et al. (2010) Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. Environ Microbiol 12: 899-915.
4. Haas D, Défago G, (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nature Reviews Microbiology 3: 307-319.
5. Lapouge K, Schubert M, Allain FH, Haas D, (2008) Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 67: 241-253.
6. Sonnleitner E, Haas D, (2011) Small RNAs as regulators of primary and secondary metabolism in Pseudomonas species. Appl Microbiol Biotechnol 91: 63-79.
7. Reimmann C, Beyeler M, Latifi A, Winteler H, Foglino M, et al. (1997) The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol Microbiol 24: 309-319.
8. Burrowes E, Abbas A, O'Neill A, Adams C, O'Gara F, (2005) Characterisation of the regulatory RNA rsmB from Pseudomonas aeruginosa PAO1. Res Microbiol 156: 7-16.
9. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, et al. (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
10. Vodovar N, Vallenet D, Cruveiller S, Rouy Z, Barbe V, et al. (2006) Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Nat Biotechnol 24: 673-679.
11. Rich JJ, Kinscherf TG, Kitten T, Willis DK, (1994) Genetic evidence that the gacA gene encodes the cognate response regulator for the lemA sensor in Pseudomonas syringae. J Bacteriol 176: 7468-7475.
12. Kinscherf TG, Willis DK, (1999) Swarming by Pseudomonas syringae B728a requires gacS (lemA) and gacA but not the acyl-homoserine lactone biosynthetic gene ahlI. J Bacteriol 181: 4133-4136.
13. Willis DK, Holmstadt JJ, Kinscherf TG, (2001) Genetic evidence that loss of virulence associated with gacS or gacA mutations in Pseudomonas syringae B728a does not result from effects on alginate production. Appl Environ Microbiol 67: 1400-1403.
14. Chatterjee A, Cui YY, Yang HL, Collmer A, Alfano JR, et al. (2003) GacA, the response regulator of a two-component system, acts as a master regulator in Pseudomonas syringae pv. tomato DC3000 by controlling regulatory RNA, transcriptional activators, and alternate sigma factors. Mol Plant Microbe Interact 16: 1106-1117.
15. Aarons S, Abbas A, Adams C, Fenton A, O'Gara F, (2000) A regulatory RNA (PrrB RNA) modulates expression of secondary metabolite genes in Pseudomonas fluorescens F113. J Bacteriol 182: 3913-3919.
16. Kang BR, Yang KY, Cho BH, Han TH, Kim IS, et al. (2006) Production of indole-3-acetic acid in the plant-beneficial strain Pseudomonas chlororaphis O6 is negatively regulated by the global sensor kinase GacS. Curr Microbiol 52: 473-476.
17. Laville J, Voisard C, Keel C, Maurhofer M, Defago G, et al. (1992) Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root-rot of tobacco. Proc Natl Acad Sci U S A 89: 1562-1566.
18. Zhang ZG, Pierson LS, (2001) A second quorum-sensing system regulates cell surface properties but not phenazine antibiotic production in Pseudomonas aureofaciens. Appl Environ Microbiol 67: 4305-4315.
19. Liao CH, McCallus DE, Wells JM, Tzean SS, Kang GY, (1996) The repB gene required for production of extracellular enzymes and fluorescent siderophores in Pseudomonas viridiflava is an analog of the gacA gene of Pseudomonas syringae. Can J Microbiol 42: 177-182.
20. Sacherer P, Defago G, Haas D, (1994) Extracellular protease and phospholipase-C are controlled by the global regulatory gene gacA in the biocontrol strain Pseudomonas fluorescens CHA0. FEMS Microbiol Lett 116: 155-160.
21. Koch B, Nielsen TH, Sorensen D, Andersen JB, Christophersen C, et al. (2002) Lipopeptide production in Pseudomonas sp. strain DSS73 is regulated by components of sugar beet seed exudate via the Gac two-component regulatory system. Appl Environ Microbiol 68: 4509-4516.
22. Dubern JF, Lagendijk EL, Lugtenberg BJJ, Bloemberg GV, (2005) The heat shock genes dnaK, dnaJ, and grpE are involved in regulation of putisolvin biosynthesis in Pseudomonas putida PCL1445. J Bacteriol 187: 5967-5976.
23. Barahona E, Navazo A, Martinez-Granero F, Zea-Bonilla T, Perez-Jimenez RM, et al. (2011) A Pseudomonas fluorescens F113 mutant with enhanced competitive colonization ability shows improved biocontrol activity against fungal root pathogens. Appl Environ Microbiol 77: 5412-5419.
24. Zuber S, Carruthers F, Keel C, Mattart A, Blumer C, et al. (2003) GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHA0. Mol Plant Microbe Interact 16: 634-644.
25. Kay E, Dubuis C, Haas D, (2005) Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci U S A 102: 17136-17141.
26. Valverde C, Heeb S, Keel C, Haas D, (2003) RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0. Mol Microbiol 50: 1361-1379.
27. Kay E, Humair B, Dénervaud V, Riedel K, Spahr S, et al. (2006) Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 188: 6026-6033.
28. Lapouge K, Sineva E, Lindell M, Starke K, Baker CS, et al. (2007) Mechanism of hcnA mRNA recognition in the Gac/Rsm signal transduction pathway of Pseudomonas fluorescens. Mol Microbiol 66: 341-356.
29. Schubert M, Lapouge K, Duss O, Oberstrass FC, Jelesarov I, et al. (2007) Molecular basis of messenger RNA recognition by the specific bacterial repressing clamp RsmA/CsrA. Nature Structural & Molecular Biology 14: 807-813.
30. Heurlier K, Williams F, Heeb S, Dormond C, Pessi G, et al. (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/rsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186: 2936-2945.
31. Martínez-Granero F, Capdevila S, Sánchez-Contreras M, Martín M, Rivilla R, (2005) Two site-specific recombinases are implicated in phenotypic variation and competitive rhizosphere colonization in Pseudomonas fluorescens. Microbiology 151: 975-983.
32. Martínez-Granero F, Rivilla R, Martin M, (2006) Rhizosphere selection of highly motile phenotypic variants of Pseudomonas fluorescens with enhanced competitive colonization ability. Appl Environ Microbiol 72: 3429-3434.
33. Navazo A, Barahona E, Redondo-Nieto M, Martinez-Granero F, Rivilla R, et al. (2009) Three independent signalling pathways repress motility in Pseudomonas fluorescens F113. Microb Biotechnol 2: 489-498.
34. Caiazza NC, O'Toole GA, (2004) SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J Bacteriol 186: 4476-4485.
35. Caiazza NC, Shanks RM, O'Toole GA, (2005) Rhamnolipids modulate swarming motility patterns of Pseudomonas aeruginosa. J Bacteriol 187: 7351-7361.
36. Redondo-Nieto M, Barret M, Morrisey J, Germaine K, Martínez-Granero F, et al. Genome sequence of the biocontrol strain Pseudomonas fluorescens F113. J Bacteriol In press. doi: 10.1128/JB.06601-11.
37. Capdevila S, Martínez-Granero FM, Sánchez-Contreras M, Rivilla R, Martín M, (2004) Analysis of Pseudomonas fluorescens F113 genes implicated in flagellar filament synthesis and their role in competitive root colonization. Microbiology 150: 3889-3897.
38. Dasgupta N, Wolfgang MC, Goodman AL, Arora SK, Jyot J, et al. (2003) A four-tiered transcriptional regulatory circuit controls flagellar biogenesis in Pseudomonas aeruginosa. Mol Microbiol 50: 809-824.
39. Sánchez-Contreras M, Martín M, Villacieros M, O'Gara F, Bonilla I, et al. (2002) Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. J Bacteriol 184: 1587-1596.
40. de Weger LA, van der vlugt CIM, Wijfjes AHM, Bakker PAHM, Schippers B, et al. (1987) Flagella of a plant-growth-stimulating Pseudomonas fluorescens strain are required for colonization of potato roots. J Bacteriol 169: 2769-2773.
41. Blumer C, Heeb S, Pessi G, Haas D, (1999) Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc Natl Acad Sci U S A 96: 14073-14078.
42. Reimmann C, Valverde C, Kay E, Haas D, (2005) Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in biocontrol strain Pseudomonas fluorescens CHA0. J Bacteriol 187: 276-285.
43. Choy WK, Zhou L, Syn CKC, Zhang LH, Swarup S, (2004) MorA defines a new class of regulators affecting flagellar development and biofilm formation in diverse Pseudomonas species. J Bacteriol 186: 7221-7228.
44. Dasgupta N, Ramphal R, (2001) Interaction of the antiactivator FleN with the transcriptional activator FleQ regulates flagellar number in Pseudomonas aeruginosa. J Bacteriol 183: 6636-6644.
45. Tart AH, Wolfgang MC, Wozniak DJ, (2005) The Alternative Sigma Factor AlgT Represses Pseudomonas aeruginosa Flagellum Biosynthesis by Inhibiting Expression of fleQ. J Bacteriol 187: 7955-7962.
46. Dasgupta N, Ferrell EP, Kanack KJ, West SEH, Ramphal R, (2002) fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is s70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein. J Bacteriol 184: 5240-5250.
47. Tart AH, Blanks MJ, Wozniak DJ, (2006) The AlgT-dependent transcriptional regulator AmrZ (AlgZ) inhibits flagellum biosynthesis in mucoid, nonmotile Pseudomonas aeruginosa cystic fibrosis isolates. J Bacteriol 188: 6483-6489.
48. Beatson SA, Whitchurch CB, Sargent JL, Levesque RC, Mattick JS, (2002) Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa. J Bacteriol 184: 3605-3613.
49. Goodman AL, Merighi M, Hyodo M, Ventre I, Filloux A, et al. (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23: 249-259.
50. Valverde C, Lindell M, Wagner EGH, Haas D, (2004) A repeated GGA motif is critical for the activity and stability of the riboregulator rsmY of Pseudomonas fluorescens. J Biol Chem 279: 25066-25074.
51. Brencic A, Lory S, (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 72: 612-632.
52. Petrova OE, Sauer K, (2010) The novel two-component regulatory system BfiSR regulates biofilm development by controlling the small RNA rsmZ through CafA. J Bacteriol 192: 5275-5288.
53. Pessi G, Williams F, Hindle Z, Heurlier K, Holden MTG, et al. (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183: 6676-6683.
54. Wei BDL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, et al. (2001) Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40: 245-256.
55. Kuchma SL, Brothers KM, Merritt JH, Liberati NT, Ausubel FM, et al. (2007) BifA, a cyclic-di-GMP phosphodiesterase, inversely regulates biofilm formation and swarming motility by Pseudomonas aeruginosa PA14. J Bacteriol 189: 8165-8178.
56. Damron FH, Qiu D, Yu HD, (2009) The Pseudomonas aeruginosa sensor kinase KinB negatively controls alginate production through AlgW-dependent MucA proteolysis. J Bacteriol 191: 2285-2295.
57. Wozniak DJ, Ohman DE, (1994) Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB, and algD reveals a hierarchy of alginate gene expression which is modulated by algT. J Bacteriol 176: 6007-6014.
58. Ma S, Wozniak DJ, Ohman DE, (1997) Identification of the histidine protein kinase KinB in Pseudomonas aeruginosa and its phosphorylation of the alginate regulator AlgB. J Biol Chem 272: 17952-17960.
59. Schreiber KJ, Desveaux D, (2011) AlgW regulates multiple Pseudomonas syringae virulence strategies. Mol Microbiol 80: 364-377.
60. Heeb S, Valverde C, Gigot-Bonnefoy C, Haas D, (2005) Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. FEMS Microbiol Lett 243: 251-258.
61. Whistler CA, Corbell NA, Sarniguet A, Ream W, Loper JE, (1998) The two-component regulators GacS and GacA influence accumulation of the stationary-phase sigma factor ss and the stress response in Pseudomonas fluorescens Pf-5. J Bacteriol 180: 6635-6641.
62. Dubern JF, Bloemberg GV, (2006) Influence of environmental conditions on putisolvins I and II production in Pseudomonas putida strain PCL1445. FEMS Microbiol Lett 263: 169-175.
63. Shanahan P, O'Sullivan DJ, Simpson P, Glennon JD, O'Gara F, (1992) Isolation of 2,4-diacetylphloroglucinol from a fluorescent pseudomonad and investigation of physiological parameters influencing its production. Appl Environ Microbiol 58: 353-358.
64. Kalogeraki VS, Winans SC, (1997) Suicide plasmids containing promoterless reporter genes can simultaneously disrupt and create fusions to target genes of diverse bacteria. Gene 188: 69-75.
65. Schäfer A, Tauch A, Jager W, Kalinowski J, Thierbach G, et al. (1994) Small mobilizable multipurpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: Selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145: 69-73.
66. Kirchner O, Tauch A, (2003) Tools for genetic engineering in the amino acid-producing bacterium Corynebacterium glutamicum. J Biotechnol 104: 287-299.
67. de Lorenzo V, Eltis L, Kessler B, Timmis KN, (1993) Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes. Gene 123: 17-24.
68. Finan TM, Kunkel B, De Vos GF, Signer ER, (1986) Second symbiotic megaplasmid in Rhizobium meliloti carrying exopolysaccharide and thiamine synthesis genes. J Bacteriol 167: 66-72.
69. Scher FM, Baker R, (1982) Effects of Pseudomonas putida and a synthetic iron chelator on induction of soil suppressiveness to Fusarium wilt pathogens. Phytopathology 72: 1567-1573.
70. Bertani G, (1951) Studies on Lysogenesis. 1. The Mode of Phage Liberation by Lysogenic Escherichia coli. J Bacteriol 62: 293-300.
71. Sambrook J, Fritsch EF, Maniatics T, (1989) Molecular cloning: a laboratory manual. 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
72. Laemmli UK, (1970) Cleavage of structural proteins during assembly of head of bacteriophage T4. Nature 227: 680-685.
73. Lin C, Yang L, Yang JJ, Huang Y, Liu ZR, (2005) ATPase/helicase activities of p68 RNA helicase are required for pre-mRNA splicing but not for assembly of the spliceosome. Mol Cell Biol 25: 7484-7493.