Chapter 12 : Quorum Sensing in the Soft-Rot Erwinias

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Quorum Sensing in the Soft-Rot Erwinias, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555815578/9781555814045_Chap12-1.gif /docserver/preview/fulltext/10.1128/9781555815578/9781555814045_Chap12-2.gif


One of the first bacterial species for which -acylhomoserine lactone (AHL) quorum sensing (QS) was described was . Since then, QS has been well studied in the soft-rot erwinias, where, as described in this chapter, QS plays a key role in the regulation of secreted plant cell wall-degrading enzymes (PCWDEs) production and hence in virulence. In certain strains, a well-defined AHL QS system also controls production of β-lactam antibiotic, carbapenem. In addition, it must be emphasized that QS is only one of many regulatory inputs into virulence factor production in . The majority of the key secreted virulence factors of and , including multiple Pels, Peh, Cel, and Svx, are secreted by a type II secretion system known as the Out system. There have been two reports describing the existence of AHL QS in . First, production of a single AHL, most likely 3-oxo-C-HSL, was described for several Italian strains of ; for one strain, production of AHL was observed in planta. Second, AHL activity was detected in the culture supernatant of a Swiss strain of . Both reports describe the detection and partial sequencing of pairs of convergent homologues, named .

Citation: Coulthurst S, Monson R, Salmond G. 2008. Quorum Sensing in the Soft-Rot Erwinias, p 185-199. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch12

Key Concept Ranking

Type II Secretion System
Type I Secretion System
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


Image of FIGURE 1

Regulation of carbapenem antibiotic (Car) production by AHL QS in subsp. ATCC 39048. The signaling molecule, 3-oxo-C-HSL, is synthesized by CarI. At low cell densities (top), 3-oxo-CHSL diffuses away from the cell and CarR is in a transcriptionally inactive state. The gene cluster is not transcribed from the QS-dependent promoter (P) upstream of hence, no antibiotic is produced, but the resistance functions, encoded by are expressed from the internal promoter (P). At high cell densities (bottom), a high concentration of 3-oxo-C-HSL is achieved and CarR binds 3-oxo-C-HSL, making it competent to activate transcription of the genes from P and also to upregulate its own transcription. As a result, Car antibiotic is produced. The regulator Hor is also required for expression and other regulatory inputs are indicated: expression is dependent on carbon source and possibly also downregulated in the presence of high 3-oxo-C-HSL levels; temperature affects transcription and probably also affects expression on a posttranscriptional level. Arrows with “+” indicate positive regulation, and flattened arrowhead indicates repression. Refer to text and references and for details.

Citation: Coulthurst S, Monson R, Salmond G. 2008. Quorum Sensing in the Soft-Rot Erwinias, p 185-199. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch12
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of FIGURE 2

Model for the regulation of virulence factor production by AHL QS in At low cell density (top), ExpI synthesizes the AHL signaling molecule, 3-oxo-C-HSL, which diffuses into the environment. VirR, the cognate LuxR homologue, is expressed constitutively and may directly repress expression of PCWDEs. RsmA is activated by VirR and itself represses expression of and PCWDEs. At high cell density, high concentrations of 3-oxo-C HSL are achieved and the signal binds to VirR. This causes derepression and allows expression of PCWDEs and . The untranslated RNA further sequesters RsmA in the cell, thus immediately affecting PCWDE expression in a cell-density-dependent manner.

Citation: Coulthurst S, Monson R, Salmond G. 2008. Quorum Sensing in the Soft-Rot Erwinias, p 185-199. In Winans S, Bassler B (ed), Chemical Communication among Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555815578.ch12
Permissions and Reprints Request Permissions
Download as Powerpoint


1. Andersson, R. A.,, A. R. Eriksson,, R. Heikinheimo,, A. Mae,, M. Pirhonen,, V. Koiv,, H. Hyytiainen,, A. Tuikkala, and, E. T. Palva. 2000. Quorum sensing in the plant pathogen Erwinia carotovora subsp. carotovora: the role of expR(Ecc). Mol. Plant-Microbe Interact 13:384393.
2. Bainton, N. J.,, P. Stead,, S. R. Chhabra,, B. W. Bycroft,, G. P. Salmond,, G. S. Stewart, and, P. Williams. 1992. N-(3-oxohexanoyl)-l-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem. J. 288:9971004.
3. Barnard, A. M.,, and G. P. Salmond. 2006. Quorum sensing in Erwinia species. Anal. Bioanal. Chem.387:415423.
4. Bell, K. S.,, M. Sebaihia,, L. Pritchard,, M. T. Holden,, L. J. Hyman,, M. C. Holeva,, N. R. Thomson,, S. D. Bentley,, L. J. Churcher,, K. Mungall,, R. Atkin,, N. Bason,, K. Brooks,, T. Chillingworth,, K. Clark,, J. Doggett,, A. Fraser,, Z. Hance,, H. Hauser,, K. Jagels,, S. Moule,, H. Norbertczak,, D. Ormond,, C. Price,, M. A. Quail,, M. Sanders,, D. Walker,, S. Whitehead,, G. P. Salmond,, P. R. Birch,, J. Parkhill, and, I. K. Toth. 2004. Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc. Natl. Acad. Sci. USA 101:1110511110.
5. Brader, G.,, S. Sjoblom,, H. Hyytiainen,, K. Sims-Huopaniemi, and, E. T. Palva. 2005. Altering substrate chain length specificity of an acylhomoserine lactone synthase in bacterial communication. J. Biol. Chem. 280:1040310409.
6. Burr, T.,, A. M. Barnard,, M. J. Corbett,, C. L. Pemberton,, N. J. Simpson, and, G. P. Salmond. 2006. Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Mol. Microbiol. 59:113125.
7. Castang, S.,, S. Reverchon,, P. Gouet, and, W. Nasser. 2006. Direct evidence for the modulation of the activity of the Erwinia chrysanthemi quorum-sensing regulator ExpR by acylho-moserine lactone pheromone. J. Biol. Chem. 281:2997229987.
8. Chapon-Herve, V.,, M. Akrim,, A. Latifi,, P. Williams,, A. Lazdunski, and, M. Bally. 1997. Regulation of the xcp secretion pathway by multiple quorum-sensing modulons in Pseudomonas aeruginosa. Mol. Microbiol. 24:11691178.
9. Chatterjee, A.,, Y. Cui, and, A. K. Chatterjee. 2002. RsmA and the quorum-sensing signal, N-[3-oxohexanoyl]-l-homoserine lactone, control the levels of rsmB RNA in Erwinia carotovora subsp. carotovora by affecting its stability. J. Bacteriol. 184:40894095.
10. Chatterjee, A.,, Y. Cui,, Y. Liu,, C. K. Dumenyo, and, A. K. Chatterjee. 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. 61:19591967.
11. Corbett, M.,, S. Virtue,, K. Bell,, P. Birch,, T. Burr,, L. Hyman,, K. Lilley,, S. Poock,, I. Toth, and, G. Salmond. 2005. Identification of a new quorum-sensing-controlled virulence factor in Erwinia carotovora subsp. atroseptica secreted via the type II targeting pathway. Mol. Plant-Microbe Interact. 18:334342.
12. Costa, J. M.,, and J. E. Loper. 1997. EcbI and EcbR: homologs of LuxI and LuxR affecting antibiotic and exoenzyme production by Erwinia carotovora subsp. betavasculorum. Can. J. Microbiol. 43:11641171.
13. Coulthurst, S. J.,, A. M. Barnard, and, G. P. Salmond. 2005. Regulation and biosynthesis of carbapenem antibiotics in bacteria. Nat. Rev. Microbiol. 3:295306.
14. Coulthurst, S. J.,, K. S. Lilley, and, G. P. Salmond. 2006. Genetic and proteomic analysis of the role of luxS in the enteric phytopathogen, Erwinia carotovora. Mol. Plant Pathol. 7:3135.
15. Coulthurst, S. J.,, N. R. Williamson,, A. K. Harris,, D. R. Spring, and, G. P. Salmond. 2006. Metabolic and regulatory engineering of Serratia marcescens: mimicking phage-mediated horizontal acquisition of antibiotic biosynthesis and quorum-sensing capacities. Microbiology 152:18991911.
16. Cui, Y.,, A. Chatterjee,, H. Hasegawa, and, A. K. Chatterjee. 2006. Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with N-acylhomoserine lactone signals. J. Bacteriol. 188:47154726.
17. Cui, Y.,, A. Chatterjee,, H. Hasegawa,, V. Dixit,, N. Leigh, and, A. K. Chatterjee. 2005. ExpR, a LuxR homolog of Erwinia carotovora subsp. carotovora, activates transcription of rsmA, which specifies a global regulatory RNA-binding protein. J. Bacteriol. 187:47924803.
18. Cui, Y.,, A. Chatterjee,, Y. Liu,, C. K. Dumenyo, and, A. K. Chatterjee. 1995. Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-l-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. J. Bacteriol. 177:51085115.
19. Cui, Y.,, A. Mukherjee,, C. K. Dumenyo,, Y. Liu, and, A. K. Chatterjee. 1999. rsmC of the softrotting bacterium Erwinia carotovora subsp. carotovora negatively controls extracellular enzyme and harpin(Ecc) production and virulence by modulating levels of regulatory RNA (rsmB) and RNA-binding protein (RsmA). J. Bacteriol. 181:60426052.
20. Filloux, A. 2004. The underlying mechanisms of type II protein secretion. Biochim. Biophys. Acta 1694:163179.
21. Fineran, P. C.,, H. Slater,, L. Everson,, K. Hughes, and, G. P. Salmond. 2005. Biosynthesis of tripyrrole and beta-lactam secondary metabolites in Serratia: integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production. Mol. Microbiol. 56:14951517.
22. Ham, J. H.,, Y. Cui,, J. R. Alfano,, P. Rodriguez-Palenzuela,, C. M. Rojas,, A. K. Chatterjee, and, A. Collmer. 2004. Analysis of Erwinia chrysanthemi EC16 pelE::uidA, pelL::uidA, and hrpN::uidA mutants reveals strain-specific atypical regulation of the Hrp type III secretion system. Mol. Plant-Microbe Interact. 17:184194.
23. He, S. Y.,, M. Lindeberg,, A. K. Chatterjee, and, A. Collmer. 1991. Cloned Erwinia chrysanthemi out genes enable Escherichia coli to selectively secrete a diverse family of heterologous proteins to its milieu. Proc. Natl. Acad. Sci. USA 88:10791083.
24. Holden, M. T.,, S. J. McGowan,, B. W. Bycroft,, G. S. Stewart,, P. Williams, and, G. P. Salmond. 1998. Cryptic carbapenem antibiotic production genes are widespread in Erwinia carotovora: facile trans activation by the carR transcriptional regulator. Microbiology 144:14951508.
25. Jones, S.,, B. Yu,, N. J. Bainton,, M. Birdsall,, B. W. Bycroft,, S. R. Chhabra,, A. J. Cox,, P. Golby,, P. J. Reeves,, S. Stephens, et al. 1993. The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 12:24772482.
26. Laasik, E.,, L. Andresen, and, A. Mae. 2006. Type II quorum sensing regulates virulence in Erwinia carotovora ssp. carotovora. FEMS Microbiol. Lett. 258:227234.
27. Lazdunski, A. M.,, I. Ventre, and, J. N. Sturgis. 2004. Regulatory circuits and communication in gram-negative bacteria. Nat. Rev. Microbiol. 2:581592.
28. Liu, M. Y.,, G. Gui,, B. Wei,, J. F. Preston III,, L. Oakford,, U. Yuksel,, D. P. Giedroc, and, T. Romeo. 1997. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J. Biol. Chem. 272:1750217510.
29. Liu, M. Y.,, and T. Romeo. 1997. The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein. J. Bacteriol. 179:46394642.
30. Liu, M. Y.,, H. Yang, and, T. Romeo. 1995. The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. J. Bacteriol. 177:26632672.
31. Liu, Y.,, Y. Cui,, A. Mukherjee, and, A. K. Chatterjee. 1998. Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Mol. Microbiol. 29:219234.
32. McGowan, S.,, M. Sebaihia,, S. Jones,, B. Yu,, N. Bainton,, P. F. Chan,, B. Bycroft,, G. S. Stewart,, P. Williams, and, G. P. Salmond. 1995. Carbapenem antibiotic production in Erwinia carotovora is regulated by CarR, a homologue of the LuxR transcriptional activator. Microbiology. 141:541550.
33. McGowan, S. J.,, A. M. Barnard,, G. Bosgelmez,, M. Sebaihia,, N. J. Simpson,, N. R. Thomson,, D. E. Todd,, M. Welch,, N. A. White-head, and, G. P. Salmond. 2005. Carbapenem antibiotic biosynthesis in Erwinia carotovora is regulated by physiological and genetic factors modulating the quorum sensing-dependent control pathway. Mol. Microbiol. 55:526545.
34. McGowan, S. J.,, M. Sebaihia,, S. O’Leary,, K. R. Hardie,, P. Williams,, G. S. Stewart,, B. W. Bycroft, and, G. P. Salmond. 1997. Analysis of the carbapenem gene cluster of Erwinia carotovora: definition of the antibiotic biosynthetic genes and evidence for a novel beta-lactam resistance mechanism. Mol. Microbiol. 26:545556.
35. McGowan, S. J.,, M. Sebaihia,, L. E. Porter,, G. S. Stewart,, P. Williams,, B. W. Bycroft, and, G. P. Salmond. 1996. Analysis of bacterial carbapenem antibiotic production genes reveals a novel beta-lactam biosynthesis pathway. Mol. Microbiol. 22:415426.
36. Molina, L.,, F. Rezzonico,, G. Defago, and, B. Duffy. 2005. Autoinduction in Erwinia amylovora: evidence of an acyl-homoserine lactone signal in the fire blight pathogen. J. Bacteriol. 187:32063213.
37. Mukherjee, A.,, Y. Cui,, Y. Liu, and, A. K. Chatterjee. 1997. Molecular characterization and expression of the Erwinia carotovora hrpNEcc gene, which encodes an elicitor of the hypersensitive reaction. Mol. Plant-Microbe Interact. 10:462471.
38. Nasser, W.,, M. L. Bouillant,, G. Salmond, and, S. Reverchon. 1998. Characterization of the Erwinia chrysanthemi expI-expR locus directing the synthesis of two N-acyl-homoserine lactone signal molecules. Mol. Microbiol. 29:13911405.
39. Pemberton, C. L.,, N. A. Whitehead,, M. Sebaihia,, K. S. Bell,, L. J. Hyman,, S. J. Harris,, A. J. Matlin,, N. D. Robson,, P. R. Birch,, J. P. Carr,, I. K. Toth, and, G. P. Salmond. 2005. Novel quorum-sensing-controlled genes in Erwinia carotovora subsp. carotovora: identification of a fungal elicitor homologue in a soft-rotting bacterium. Mol. Plant-Microbe Interact. 18:343353.
40. Perombelon, M. C. M. 2002. Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol. 51:112.
41. Pirhonen, M.,, D. Flego,, R. Heikinheimo, and, E. T. Palva. 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. 12:24672476.
42. Reeves, P. J.,, D. Whitcombe,, S. Wharam,, M. Gibson,, G. Allison,, N. Bunce,, R. Barallon,, P. Douglas,, V. Mulholland,, S. Stevens, et al. 1993. Molecular cloning and characterization of 13 out genes from Erwinia carotovora subspecies carotovora: genes encoding members of a general secretion pathway (GSP) widespread in gram-negative bacteria. Mol. Microbiol. 8:443456.
43. Reverchon, S.,, M. L. Bouillant,, G. Salmond, and, W. Nasser. 1998. Integration of the quorum-sensing system in the regulatory networks controlling virulence factor synthesis in Erwinia chrysanthemi. Mol. Microbiol. 29:14071418.
44. Riedel, K.,, T. Ohnesorg,, K. A. Krogfelt,, T. S. Hansen,, K. Omori,, M. Givskov, and, L. Eberl. 2001. N-acyl-l-homoserine lactone-mediated regulation of the lip secretion system in Serratia liquefaciens MG1. J. Bacteriol. 183:18051809.
45. Romeo, T. 1998. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol. Microbiol. 29:13211330.
46. Romeo, T.,, and M. Gong. 1993. Genetic and physical mapping of the regulatory gene csrA on the Escherichia coli K-12 chromosome. J. Bacteriol. 175:57405741.
47. Sandkvist, M. 2001. Biology of type II secretion. Mol. Microbiol. 40:271283.
48. Schuster, M.,, C. P. Lostroh,, T. Ogi, and, E. P. Greenberg. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:20662079.
49. Sjoblom, S.,, G. Brader,, G. Koch, and, E. T. Palva. 2006. Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol. Microbiol. 60:14741489.
50. Slater, H.,, M. Crow,, L. Everson, and, G. P. Salmond. 2003. Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol. Microbiol. 47:303320.
51. Smadja, B.,, X. Latour,, D. Faure,, S. Chevalier,, Y. Dessaux, and, N. Orange. 2004. Involvement of N-acylhomoserine lactones throughout plant infection by Erwinia carotovora subsp. atroseptica (Pectobacterium atrosepticum). Mol. Plant-Microbe Interact. 17:12691278.
52. Swift, S.,, M. K. Winson,, P. F. Chan,, N. J. Bainton,, M. Birdsall,, P. J. Reeves,, C. E. Rees,, S. R. Chhabra,, P. J. Hill,, J. P. Throup, et al. 1993. A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR: LuxI superfamily in enteric bacteria. Mol. Microbiol. 10:511520.
53. Thomson, N. R.,, J. D. Thomas, and, G. P. Salmond. 1999. Virulence determinants in the bacterial phytopathogen Erwinia. Methods Microbiol. 29:347426.
54. Toth, I. K.,, K. S. Bell,, M. C. Holeva, and, P. R. J. Birch. 2003. Soft rot erwiniae: from genes to genomes. Mol. Plant Pathol. 4:1730.
55. Toth, I. K.,, and P. R. Birch. 2005. Rotting softly and stealthily. Curr. Opin. Plant Biol. 8:424429.
56. Vendeville, A.,, K. Winzer,, K. Heurlier,, C. M. Tang, and, K. R. Hardie. 2005. Making ‘sense’ of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat. Rev. Microbiol. 3:383396.
57. Venturi, V.,, C. Venuti,, G. Devescovi,, C. Lucchese,, A. Friscina,, G. Degrassi,, C. Aguilar, and, U. Mazzucchi. 2004. The plant pathogen Erwinia amylovora produces acyl-homoserine lactone signal molecules in vitro and in planta. FEMS Microbiol. Lett. 241:179183.
58. Vincent-Sealy, L. V.,, J. D. Thomas,, P Commander, and, G. P. Salmond. 1999. Erwinia carotovora DsbA mutants: evidence for a periplasmic-stress signal transduction system affecting transcription of genes encoding secreted proteins. Microbiology 145:19451958.
59. von Bodman, S. B.,, J. K. Ball,, M. A. Faini,, C. M. Herrera,, T. D. Minogue,, M. L. Urbanowski, and, A. M. Stevens. 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. 185:70017007.
60. Welch, M.,, J. M. Dutton,, F. G. Glansdorp,, G. L. Thomas,, D. S. Smith,, S. J. Coulthurst,, A. M. Barnard,, G. P. Salmond, and, D. R. Spring. 2005. Structure-activity relationships of Erwinia carotovora quorum sensing signaling molecules. Bioorg. Med. Chem. Lett. 15:42354238.
61. Welch, M.,, D. E. Todd,, N. A. Whitehead,, S. J. McGowan,, B. W. Bycroft, and, G. P. Salmond. 2000. N-acyl homoserine lactone binding to the CarR receptor determines quorum-sensing specificity in Erwinia. EMBO J. 19:631641.
62. Whitehead, N. A.,, A. M. Barnard,, H. Slater,, N. J. Simpson, and, G. P. Salmond. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25:365404.
63. Whitehead, N. A.,, J. T. Byers,, P. Commander,, M. J. Corbett,, S. J. Coulthurst,, L. Everson,, A. K. Harris,, C. L. Pemberton,, N. J. Simpson,, H. Slater,, D. S. Smith,, M. Welch,, N. Williamson, and, G. P. Salmond. 2002. The regulation of virulence in phytopathogenic Erwinia species: quorum sensing, antibiotics and ecological considerations. Antonie Van Leeuwenhoek 81:223231.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error