N-acyl homoserine lactones in diverse Pectobacterium and dickeya plant pathogens: Diversity, abundance, and involvement in virulence

Sensors

Volumn 12, Issue 3, 2012, Pages 3484-3497

  Crépin, Alexandre ^a,b   Beury Cirou, Amélie ^b,c   Barbey, Corinne ^a   Farmer, Christine ^a   Hélias, Valérie ^d,e   Burini, Jean François ^a   Faure, Denis ^c   Latour, Xavier ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b SIPRE Comité Nord Station de recherche et de création variétale   (France)

^c INSTITUT DES SCIENCES DU VÉGÉTAL   (France)

^d Fédération Nationale des Producteurs de Plants de Pomme de Terre ^*  (France)

^e Universite Rennes 1   (France)

Author keywords

AttM lactonase; N Acyl homoserine lactones; Quorum quenching; Quorum sensing; Soft rot bacteria; Solanum tuberosum L.

Indexed keywords

GAMMA BUTYROLACTONE DERIVATIVE;

ARTICLE; CHEMISTRY; ENTEROBACTERIACEAE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; ISOLATION AND PURIFICATION; METABOLISM; PATHOGENICITY; PECTOBACTERIUM; QUORUM SENSING; TANDEM MASS SPECTROMETRY; VIRULENCE;

ACYL-BUTYROLACTONES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ENTEROBACTERIACEAE; PECTOBACTERIUM; QUORUM SENSING; TANDEM MASS SPECTROMETRY; VIRULENCE;

EID: 84858971457     PISSN: 14248220     EISSN: None     Source Type: Journal    
DOI: 10.3390/s120303484     Document Type: Article

References (55)

1. Ryan, R.P.; Dow, J.M. Diffusible signals and interspecies communication in bacteria. Microbiology 2008, 154, 1845-1858.
2. Fuqua, W.C.; Winans, S.C.; Greenberg, E.P. Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol. 1994, 176, 269-275.
3. von Bodman, S.B.; Bauer, W.D.; Coplin, D.L. Quorum sensing in plant-pathogenic bacteria. Annu. Rev. Phytopathol. 2003, 41, 455-482.
4. Barras, F.; van Gijsegem, F.; Chatterjee, A.K. Extracellular enzymes and pathogenesis of soft-rot Erwinia. Ann. Rev. Phytopathol. 1994, 32, 201-234.
5. Barnard, A.M.; Salmond, G.P. Quorum sensing in Erwinia species. Anal. Bioanal. Chem. 2007, 387, 415-423.
6. Nasser, W.; Bouillant, M.L.; Salmond, G.P.C.; Reverchon, S. Characterization of the Erwinia chrysanthemi expI-expR locus directing the synthesis of two N-acyl-homoserine lactone signal molecules. Mol. Microbiol. 1998, 29, 1391-1405.
7. Charkowsky, A.O. The Soft Rot Erwinia. In Plant-Associated Bacteria; Gnanamanickam, S., Ed.; Springer: Dordrecht, The Netherlands, 2006; Part 3, pp. 423-505.
8. Hussain, M.B.B.; Zhang, H.B.; Xu, J.L.; Liu, Q.; Jiang, Z.; Zhang, L.H. The acyl-homoserine lactone-type quorum sensing system modulates cell motility and virulence of Erwinia chrysanthemi pv. zeae. J. Bacteriol. 2008, 190, 1045-1053.
9. Liu, H.; Coulthurst, S.J.; Pritchard, L.; Hedley, P.E.; Ravensdale, M.; Humphris, S.; Burr, T.; Takle, G.; Brurberg, M.B.; Birch, P.R.; et al. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog. 2008, 4, e1000093.
10. Smadja, B.; Latour, X.; Faure, D.; Chevalier, S.; Dessaux, Y.; Orange, N. Involvement of N-acylhomoserine lactones throughout the plant infection by Erwinia carotovora subsp. atroseptica (Pectobacterium atrosepticum). Mol. Plant Microbe Interact. 2004, 17, 1269-1278.
11. Toth, I.K.; Newton, J.A.; Hyman, L.J.; Lees, A.K.; Daykin, M.; Ortori, C.; Williams, P.; Fray, R.G. Potato plants genetically modified to produce N-acylhomoserine lactones increases susceptibility to soft rot Erwiniae. Mol. Plant Microbe Interact. 2004, 17, 880-887.
12. Maë, A.; Montesano, M.; Koiv, V.; Palva, E.T. Transgenic plants producing the bacterial pheromone N-acylhomoserine lactone exhibit enhanced resistance to the bacterial phyto-pathogen Erwinia carotovora. Mol. Plant Microbe Interact. 2001, 14, 1035-1042.
13. Cirou, A.; Diallo, S.; Kurt, C.; Latour, X.; Faure, D. Growth promotion of quorum-quenching bacteria in the rhizosphere of Solanum tuberosum. Environ. Microbiol. 2007, 9, 1511-1522.
14. Crépin, A.; Barbey, C.; Cirou, A.; Tannières, M.; Orange, N.; Feuilloley, M.; Dessaux, Y.; Burini, J.F.; Faure, D.; Latour, X. Biological control of pathogen communication in the rhizosphere: A novel approach applied to potato soft rot due to Pectobacterium atrosepticum. Plant Soil 2011, doi:10.1007/s11104-011-1030-5.
15. Ma, B.; Hibbing, M.E.; Kim, H.S.; Reedy, R.M.; Yedidia, I.; Breuer, J.; Glasner, D.; Perna, N.T.; Kelman, A.; Charkowski, A.O. Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology 2007, 97, 1150-1163.
16. Laurila, J.; Ahola, V.; Lehtinen, A.; Joutsjoki, T.; Hannukkala, A.; Rahkohnen, A.; Pirhonen, M. Characterization of Dickeya strains isolated from potato and river water samples in Finland. Eur. J. Plant Pathol. 2008, 122, 213-225.
17. Czajkowski, R.; Grabe, G.J.; van der Wolf, J.M. Distribution of Dickeya spp. and Pectobacterium carotovorum subsp. carotovorum in naturally infected seed potatoes. Eur. J. Plant Pathol. 2009, 125, 263-275.
18. Slawiak, M.; van Beckhoven, J.R.C.M.; Specksnijder, A.G.C.L.; Czajkowski, R.; Grabe, G.; van der Wolf, J.M. Biochemical and genetical analysis reveal a new clade of biovar 3 Dickeya spp. strains isolated from potato in Europe. Eur. J. Plant Pathol. 2009, 125, 245-261.
19. Tsor (Lahkim), L.; Erlich, O.; Lebiush, S.; Hazanovsky, M.; Zig, U.; Slawiak, M.; Grabe, G.; van der Wolf, J.M.; van de Haar, J.J. Assessment of recent outbreaks of Dickeya sp. (syn. Erwinia chrysanthemi) slow wilt in potato crops in Israel. Eur. J. Plant Pathol. 2009, 123, 311-320.
20. Pitman, A.R.; Harrow, S.A.; Visnovsky, S.B. Genetic characterization of Pectobacterium wasabiae causing soft rot disease of potato in New Zealand. Eur. J. Plant Pathol. 2010, 126, 423-435.
21. Hélias V.; Hamon, P.; Huchet, E.; van der Wolf, J.; Andrivon, D. Two new effective semiselective crystal violet pectate media for isolation of Pectobacterium and Dickeya. Plant Pathol. 2011, doi:10.1111/j.1365-3059.2011.02508.x.
22. Toth, I.K.; van der Wolf, J.M.; Saddler, G.; Lojkowska, E.; Hélias, V.; Pirhonen, M.; Tsror (Lahkim), L.; Elphinstone, J.G. Dickeya species: An emerging problem for potato production in Europe. Plant Pathol. 2011, 60, 385-399.
23. Samson R.; Legendre, J.B.; Christen, R.; Fisher-Le Saux, M.; Achouak, W.; Gardan, L. Transfer of Pectobacterium chrysanthemi (Burkholder et al. 1953) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov. as Dickeya chrysanthemi comb. nov. and Dickeya paradisiaca comb. nov. and delineation of four novel species: Dickeya dadantii sp. nov., Dickeya dianthicola sp. nov., Dickeya dieffenbachiae sp. nov. and Dickeya zeae sp. nov. Int. J. Syst. Evol. Microbiol. 2005, 55, 1415-1427.
24. Diallo, S.; Latour, X.; Groboillot, A.; Copin, P.; Smadja, B.; Orange, N.; Chevalier, S. Simultaneous and selective detection of two major soft rot pathogens of potato: Pectobacterium atrosepticum (Erwinia carotovora subsp. atrosepticum) and Dickeya spp. (Erwinia chrysanthemi). Eur. J. Plant Pathol. 2009, 125, 349-354.
25. Smadja, B.; Latour, X.; Trigui, S.; Burini, J.F.; Chevalier, S.; Orange, N. Thermodependence of growth and enzymatic activities implicated in pathogenicity of two Erwinia carotovora subspecies (Pectobacterium spp.). Can. J. Microbiol. 2004, 50, 19-27.
26. Hasegawa, H.; Chatterjee, A.; Cui, Y.; Chatterjee, A.K. Elevated temperature enhances virulence of Erwinia carotovora subsp. carotovora strain EC153 to plants and stimulates production of the quorum-sensing signal, N-acyl homoserine lactone, and extracellular proteins. Appl. Environ. Microbiol. 2005, 71, 4655-4663.
27. Kotoujansky, A.; Lemattre, M.; Boistard, P. Utilization of a thermosensitive episome bearing transposon Tn10 to isolate Hfr donor strains of Erwinia carotovora subsp. chrysanthemi. J. Bacteriol. 1982, 150, 122-131.
28. Heeb, S.; Itoh, Y.; Nishijyo, T.; Schnider, U.; Keel, C.; Wade, J.; Walsh, U.; O'Gara, F.; Haas, D. Small, stable shuttle vectors based on the minimal pVS1 replicon for use in gram-negative, plant-associated bacteria. Mol. Plant Microbe Interact. 2000, 13, 232-237.
29. Carlier, A.; Uroz, S.; Smadja, B.; Latour, X.; Fray, R.; Dessaux, Y.; Faure, D. The Ti plasmid of Agrobacterium tumefaciens harbors an attM-paralogous gene, aiiB, also encoding N-acyl homoserine lactonase activity. Appl. Environ. Microbiol. 2003, 69, 4989-4993.
30. Morin, D.; Grasland, B.; Vallée-Réhel, K.; Dufau, C.; Haras, D. On-line high-performance liquid chromatography-mass spectrometric detection and quantification of N-acyl homoserine lactones, quorum-sensing signal molecules, in the presence of biological matrices. J. Chromatogr. A 2003, 1002, 79-92.
31. Latour X.; Diallo, S.; Chevalier, S.; Morin, D.; Smadja, B.; Burini, J.F.; Haras, D.; Orange, N. Thermoregulation of N-acyl homoserine lactones-based quorum sensing in the soft rot bacterium Pectobacterium atrosepticum. Appl. Environ. Microbiol. 2007, 73, 4078-4081.
32. Hugouvieux-Cotte-Pattat, N.; Condemine, G.; Nasser, W.; Reverchon, S. Regulation of pectinolysis in Erwinia chrysanthemi. Ann. Rev. Microbiol. 1996, 50, 213-257.
33. Glasner, J.D.; Yang, C.H.; Reverchon, S.; Hugouvieux-Cotte-Pattat, N.; Condemine, G.; Bohin, J.P.; van Gijsegem, F.; Yang, S.; Franza, T.; Expert, D.; et al. Genome sequence of the plant-pathogenic bacterium Dickeya dadantii 3937. J. Bacteriol. 2011, 193, 2076-2077.
34. Brader, G.; Sjöblom, S.; Hyytiäinen, H.; Sims-Huopaniemi, K.; Palva, E.T. Altering substrate chain length specificity of an acylhomoserine lactone synthase in bacterial communication. J. Biol. Chem. 2005, 280, 10403-10409.
35. Welch, M.; Dutton, J.M.; Glansdorp, F.G.; Thomas, G.L.; Smith, D.S.; Coulthurst, S.J.; Barnard, A.M.L.; Salmond, G.P.C.; Spring, D.R. Structure-activity relationships of Erwinia carotovora quorum sensing signaling molecules. Bioorg. Med. Chem. Lett. 2005, 15, 4235-4238.
36. Cha, C.; Gao, P.; Chen, Y.C.; Shaw, P.; Farrand, S.K. Production of acyl-homoserine lactone quorum-sensing signals by Gram-negative plant-associated bacteria. Mol. Plant Microbe Interact. 1998, 11, 1119-1129.
37. Ham, J.H.; Cui, Y.; Alfano, J.R.; Rodriguez-Palenzuela, P.; Rojas, C.M.; Chatterjee, A.K.; Collmer, A. Analysis of Erwinia chrysanthemi EC16 pelE::uidA, pel::uidA, and hrpN::uidA mutants reveals strain-specific atypical regulation of the Hrp type III secretion system. Mol. Plant Microbe Interact. 2004, 17, 184-194.
38. Chatterjee, A.; Cui, Y.; Hasegawa, H.; Leigh, N.; Dixit, V.; Chatterjee, A.K. 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. 2005, 187, 8026-8038.
39. Toth, I.K.; Pritchard, L.; Birch, P.R.J. Comparative genomics reveals what makes an enterobacterial plant pathogen. Annu. Rev. Phytopathol. 2006, 44, 305-336.
40. Jafra, S.; Jalink, H.; van der Schoor, R.; van der Wolf, J.M. Pectobacterium carotovorum subsp. carotovorum strains show diversity in production of response to N-acyl homoserine lactones. J. Phytopathol. 2006, 154, 729-739.
41. Gardan, L.; Gouy, C.; Christen, R.; Samson, R. Elevation of three subspecies of Pectobacterium carotovorum to species level: Pectobacterium atrosepticum sp. nov., Pectobacterium betavasculorum sp. nov. and Pectobacterium wasabiae sp. nov. Int. J. Syst. Evol. Microbiol. 2003, 53, 381-391.
42. Glasner, J.D.; Marquez-Villavicencio, M.; Kim, H.S.; Jahn, C.E.; Ma, B.; Biehl, B.S.; Rissman, A.I.; Mole, B.; Yi, X.; Yang, C.H.; et al. Niche-specificity and the variable fraction of the Pectobacterium Pan-genome. Mol. Plant Microbe Interact. 2008, 21, 1549-1560.
43. Park, S.Y.; Hwang, B.J.; Shin, M.H.; Kim, J.A.; Kim, H.K.; Lee, J.K. N-Acylhomoserine lactonase producing Rhodococcus spp. with different AHL-degrading activities. FEMS Microbiol. Lett. 2006, 261, 102-108.
44. Uroz, S.; Oger, P.M.; Chapelle, E.; Adeline, M.T.; Faure, D.; Dessaux, Y. A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl. Environ. Microbiol. 2008, 74, 1357-1366.
45. Uroz, S.; Chhabra, S.R.; Camara, M.; Williams, P.; Oger, P.; Dessaux, Y. N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 2005, 151, 3313-3322.
46. Zhang, H.B.; Wang, L.H.; Zhang, L.H. Genetic control of quorum sensing signal turnover in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 2002, 99, 4638-4643.
47. Carlier, A.; Chevrot, R.; Dessaux, Y.; Faure, D. In Agrobacterium tumefaciens strain C58, the assimilation of gamma-butyrolactone interferes with the accumulation of the N-acyl-homoserine lactone signal. Mol. Plant Microbe Interact. 2004, 17, 951-957.
48. Yang, S.; Zhang, Q.; Guo, J.; Charkowski, A.O.; Glick, B.R.; Ibekwe, A.M.; Cooksey, D.A.; Yang, C.H. Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl. Environ. Microbiol. 2007, 73, 1079-1088.
49. Yang, S.; Peng, Q.; San Francisco, M.; Wang, Y.; Zeng, Q.; Yang, C.H. Type III secretion system genes of Dickeya dadantii 3937 are induced by plant phenolic acids. PLoS One 2008, 3, e2973.
50. Effantin, G.; Rivasseau, C.; Gromova, M.; Bligny, R.; Hugouvieux-Cotte-Pattat, N. Massive production of butanediol during plant infection by phytopathogenic bacteria of the genera Dickeya and Pectobacterium. Mol. Microbiol. 2011, 82, 988-997.
51. Mhedbi-Hajri, N.; Malfatti, P.; Pédron, J.; Gaubert, S.; Reverchon, S.; van Gijsegem, F. PecS is an important player in the regulatory network governing the coordinated expression of virulence genes during the interaction between Dickeya dadantii 3937 and plants. Environ. Microbiol. 2011, 13, 2901-2914.
52. Faure, D.; Dessaux, Y. Quorum sensing as a target for developing control strategies for the plant pathogen Pectobacterium. Eur. J. Plant Pathol. 2007, 119, 353-365.
53. Cirou, A.; Raffoux, A.; Diallo, S.; Latour, X.; Dessaux, Y.; Faure, D. Gamma-caprolactone stimulates the growth of quorum-quenching Rhodococcus populations in a large-scale hydroponic system for culturing Solanum tuberosum. Res. Microbiol. 2011, 162, 945-950.
54. Cirou, A.; Mondy, S.; An, S.; Charrier, A.; Sarrazin, A.; Thoison, O.; DuBow, M.; Faure, D. Efficient biostimulation of the native and introduced quorum-quenching Rhodococcus erythropolis is revealed by a combination of analytical chemistry, microbiology and pyrosequencing. Appl. Environ. Microbiol. 2012, 78, 481-492.
55. Barbey, C.; Crépin, A.; Cirou, A.; Budin-Verneuil, A.; Orange, N.; Feuilloley, M.; Faure, D.; Dessaux, Y.; Burini, J.F.; Latour, X. Catabolic pathway of gamma-caprolactone in the biocontrol agent Rhodococcus erythropolis. J. Proteome Res. 2012, 11, 206-216.