Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora

Molecular Microbiology

Volumn 60, Issue 6, 2006, Pages 1474-1489

  Sjöblom, Solveig ^a   Brader, Günter ^a   Koch, Gudrun ^a   Palva, E Tapio ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

LACTONE DERIVATIVE; PROTEIN; PROTEIN EXPR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; GENE EXPRESSION; GENE EXPRESSION REGULATION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PECTOBACTERIUM CAROTOVORUM; PRIORITY JOURNAL; QUORUM SENSING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

4-BUTYROLACTONE; AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CELL WALL; CELLULASE; GENE EXPRESSION REGULATION, BACTERIAL; HOMOSERINE; MOLECULAR SEQUENCE DATA; PECTOBACTERIUM CAROTOVORUM; PHENOTYPE; PLANT DISEASES; PLANT PROTEINS; REPRESSOR PROTEINS; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; VIRULENCE;

BACTERIA (MICROORGANISMS); PECTOBACTERIUM CAROTOVORUM;

EID: 33744502625     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2006.05210.x     Document Type: Article

References (53)

1. Andersson R.A. Eriksson A.R. Heikinheimo R. Mae A. Pirhonen M. Koiv V., et al. 2000 Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expR (Ecc). Mol Plant Microbe Interact 13: 384 393.
2. Atkinson S. Throup J.P. Stewart G.S. Williams P. 1999 A hierarchical quorum-sensing system in Yersinia pseudotuberculosis is involved in the regulation of motility and clumping. Mol Microbiol 33: 1267 1277.
3. Beck von Bodman S. Farrand S.K. 1995 Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J Bacteriol 177: 5000 5008.
4. Bell K.S. Sebaihia M. Pritchard L. Holden M.T.G. Hyman L.J. Holeva M.C., et al. 2004 Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci USA 101: 11105 11110.
5. von Bodman S.B. Majerczak D.R. Coplin D.L. 1998 A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc Natl Acad Sci USA 95: 7687 7692.
6. von Bodman S.B. Ball J.K. Faini M.A. Herrera C.M. Minogue T.D. Urbanowski M.L. Stevens A.M. 2003 The quorum sensing negative regulators EsaR and ExpR (Ecc), homologues within the LuxR family, retain the ability to function as activators of transcription. J Bacteriol 185: 7001 7007.
7. Brader G. Sjoblom S. Hyytiainen H. Sims-Huopaniemi K. Palva E.T. 2005 Altering substrate chain length specificity of an acylhomoserine lactone synthase in bacterial communication. J Biol Chem 280: 10403 10409.
8. Burr T. Barnard A.M.L. Corbett M.J. Pemberton C.L. Simpson N.J.L. Salmond G.P.C. 2006 Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Mol Microbiol 59: 113 125.
9. Chai Y. Winans C. 2004 Site-directed mutagenesis of a LuxR-type quorum sensing transcription factor: alteration of autoinducer specificity. Mol Microbiol 51: 765 776.
10. Chatterjee A. Cui Y. Liu Y. Dumenyo C.K. Chatterjee A.K. 1995 Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl Environ Microbiol 61: 1959 1967.
11. Chatterjee A. Cui Y. Hasegawa H. Leigh N. Dixit V. Chatterjee A.K. 2005 Comparative Analysis of Two Classes of Quorum-Sensing Signaling Systems That Control Production of Extracellular Proteins and Secondary Metabolites in Erwinia carotovora Subspecies. J Bacteriol 187: 8026 8038.
12. Cui Y. Chatterjee A. Hasegawa H. Dixit V. Leigh N. Chattrjee A.K. 2005 ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein. J Bacteriol 187: 4792 4803.
13. Eberhard A. Burlingame A.L. Eberhard C. Kenyon G.L. Nealson K.H. Oppenheimer N.J. 1981 Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20: 2444 2449.
14. Engebrecht J. Silverman M. 1984 Identification of genes and gene products necessary for bacterial bioluminescence. Proc Natl Acad Sci USA 81: 4154 4158.
15. Fuqua C. Greenberg E.P. 2002 Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 9: 685 695.
16. Fuqua C. Parsek M.R. Greenberg E.P. 2001 Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35: 439 468.
17. Guard-Petter J. 1998 Variants of smooth Salmonella enterica serovar enteritidis that grow to higher cell density than the wild-type are more virulent. Appl Environ Microbiol 64: 2166 2172.
18. Hanahan D. 1983 Studies on transformation of E. coli with plasmids. J Mol Biol 166: 557 580.
19. Hyytiäinen H. Sjöblom S. Palomäki T. Tuikkala A. Palva T.E. 2003 The PmrA-PmrB two-component system responding to acidic pH and iron controls virulence in the plant pathogen Erwinia carotovora ssp. carotovora. Mol Microbiol 50: 795 807.
20. Jones S. Yu B. Bainton N.J. Birdsall M. Bycroft B.W. Chhabra S.R., et al. 1993 The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12: 2477 2482.
21. Keller L. Surette M.G. 2006 Communication in bacteria: an ecological and evolutionary perspective. Nat Rev Microbiol 4: 249 258.
22. Kõiv V. Mae A. 2001 Quorum sensing controls the synthesis of virulence factors by modulating rsmA gene expression in Erwinia carotovora subsp. carotovora. Mol Genet Genomics 265: 287 292.
23. Lazdunski A.M. Ventre I. Sturgis J.N. 2004 Regulatory circuits and communication in Gram-negative bacteria. Nat Rev Microbiol 7: 581 592.
24. de Lorenzo V. Timmis K.N. 1994 Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol 235: 386 405.
25. Luo Z.Q. Smyth A.J. Gao P. Qin Y. Farrand S.K. 2003 Mutational analysis of TraR. Correlating function with molecular structure of a quorum-sensing transcriptional activator. J Biol Chem 278: 13173 13182.
26. Manefield M. Turner S.L. 2002 Quorum sensing in context: out of molecular biology and into microbial ecology. Microbiology 148: 3762 3764.
27. Marits R. Tshuikina M. Pirhonen M. Laasik E. Mäe. A. 2002 Regulation of expression of prtW::gusA fusions on Erwinia carotovora subsp. carotovora. Microbiology 148: 835 842.
28. Medina G. Juarez K. Valderrama B. Soberon-Chavez G. 2003 Mechanism of Pseudomonas aeruginosa RhlR transcriptional regulation of the rhlAB promoter. J Bacteriol 185: 5976 5983.
29. Miller J.H. 1972 Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
30. Miller V.L. Mekalanos J.J. 1988 A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio Cholerae requires toxR. J Bacteriol 170: 2575 2583.
31. Minogue T.D. Wehland-von Trebra M. Bernhard F. von Bodman S.B. 2002 The autoregulatory role of EsaR, a quorum-sensing regulator in Pantoea stewartii ssp. stewartii: evidence for a repressor function. Mol Microbiol 44: 1625 1635.
32. Minogue T.D. Carlier A.L. Koutsoudis M.D. von Bodman S.B. 2005 The cell density-dependent expression of stewartan exopolysaccharide in Pantoea stewartii ssp. stewartii is a function of EsaR-mediated repression of the rcsA gene. Mol Microbiol 56: 189 203.
33. Novel G. Didier-Fichet M.L. Stoeber F. 1974 Inducibility of β-glucuronidase in wild-type and hexuronate-negative mutants of Escherichia coli K-12. J Bacteriol 120: 89 95.
34. Pappas K.M. Weingart C.L. Winans S.C. 2004 Chemical communication in proteobacteria: biochemical and structural studies of signal synthases and receptors required for intercellular signalling. Mol Microbiol 53: 755 769.
35. Pesci E.C. Pearson J.P. Seed P.C. Iglewski B.H. 1997 Regulation of las and rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 179: 3127 3132.
36. Pirhonen M. Heino P. Helander I. Harju P. Palva E.T. 1988 Bacteriophage T4 resistant mutants of the plant pathogen Erwinia carotovora. Microb Pathog 4: 359 367.
37. Pirhonen M. Saarilahti H. Karlsoon M.-B. Palva E.T. 1991 Identification of pathogenicity determinants of Erwinia carotovora subsp. carotovora by transposon mutagenesis. Mol Plant Microbe Interact 4: 276 283.
38. Pirhonen M. Flego D. Heikinheimo R. Palva E.T. 1993 A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J 12: 2467 2476.
39. Qin Y. Luo Z.Q. Smyth A.J. Gao P. Beck von Bodman S. Farrand S.K. 2000 Quorum-sensing signal binding results in dimerization of TraR and its release from membranes into the cytoplasm. EMBO J 19: 5212 5221.
40. Redfield R. 2002 Is quorum sensing a side effect of diffusion sensing? Trends Microbiol 10: 365 370.
41. Saarilahti H.T. Palva E.T. 1986 Major outer membrane proteins in the phytopathogenic bacteria Erwinia carotovora subsp. carotovora and subsp. atroseptica. FEMS Microbiol Lett 35: 267 270.
42. Sambrook J. Russell D.W. 2001 Molecular Cloning. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
43. Sambrook J. Fritsch E.F. Maniatis T.A. 1989 Molecular Cloning. A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
44. Thompson J.D. Higgins D.G. Gibson T.J. 1994 CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673 4680.
45. Toth I.K. Birch P.R. 2005 Rotting softly and stealthily. Curr Opin Plant Biol 8: 424 429.
46. Urbanowski M.L. Lostroh C.P. Greenberg E.P. 2004 Reversible acyl-homoserine lactone binding to purified Vibrio fischeri LuxR protein. J Bacteriol 186: 631 637.
47. Vannini A. Volpari C. Gargioli C. Muraglia E. Cortese R. De Francesco R., et al. 2002 The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA. EMBO J 21: 4393 4401.
48. Waters C.M. Bassler B.L. 2005 Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21: 319 346.
49. Welch M. Todd D.E. Whitehead N.A. McGowan S.J. Bycroft B.W. Salmond G.P. 2000 N-acylhomoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia. EMBO J 19: 631 641.
50. Whitehead N.A. Barnard A.M. Slater H. Simpson N.J. Salmond G.P. 2001 Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25: 365 404.
51. Winson M.K. Camara M. Latifi A. Foglino M. Chhabra S.R. Daykin M., et al. 1995 Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 92: 9427 9431.
52. Zhang L. Murphy P.J. Kerr A. Tate M.E. 1993 Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones. Nature 362: 446 448.
53. Zhang R.G. Pappas T. Brace J.L. Miller P.C. Oulmassov T. Molyneaux J.M., et al. 2002 Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA. Nature 417: 971 974.