LasI/R and RhlI/R quorum sensing in a strain of Pseudomonas aeruginosa beneficial to plants

Applied and Environmental Microbiology

Volumn 75, Issue 15, 2009, Pages 5131-5140

  Steindler, Laura ^a   Bertani, Iris ^a   De Sordi, Luisa ^a   Schwager, Stephan ^b   Eberl, Leo ^b   Venturi, Vittorio ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CLINICAL ISOLATES; INFECTION MODELS; N-ACYL HOMOSERINE LACTONES; P.AERUGINOSA; PLANT GROWTH; PSEUDOMONAS AERUGINOSA; QUORUM-SENSING; VIRULENCE FACTORS;

AMINO ACIDS; PLANT LIFE EXTENSION; SOILS;

ENVIRONMENTAL REGULATIONS;

N ACYLHOMOSERINE LACTONE;

BACTERIUM; GENE EXPRESSION; GENETIC ANALYSIS; MOLECULAR ANALYSIS; MUTATION; ORGANIC NITROGEN COMPOUND; PATHOGENICITY; RHIZOSPHERE; RICE; VIRULENCE;

ARTICLE; BACTERIAL COLONIZATION; BACTERIUM ISOLATE; CONTROLLED STUDY; GENE IDENTIFICATION; GENE MUTATION; MOLECULAR GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANT GROWTH; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; RHIZOSPHERE; RICE; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; CAENORHABDITIS ELEGANS; DNA, BACTERIAL; LIGASES; MOLECULAR SEQUENCE DATA; MOTHS; ORYZA SATIVA; PLANT ROOTS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; QUORUM SENSING; SEQUENCE ANALYSIS, DNA; SURVIVAL ANALYSIS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; VIRULENCE;

PSEUDOMONAS AERUGINOSA;

EID: 67651242032     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02914-08     Document Type: Article

References (63)

1. Alexeyev, M. F. 1999. The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria. BioTechniques 26:824-826, 828.
2. Arevalo-Ferro, C., M. Hentzer, G. Reil, A. Gorg, S. Kjelleberg, M. Givskov, K. Riedel, and L. Eberl. 2003. Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ. Microbiol. 5:1350-1369.
3. Beatson, S. A., C. B. Whitchurch, A. B. Semmler, and J. S. Mattick. 2002. Quorum sensing is not required for twitching motility in Pseudomonas aeruginosa. J. Bacteriol. 184:3598-3604.
4. Berg, G., L. Eberl, and A. Hartmann. 2005. The rhizosphere as a reservoir for opportunistic human pathogenic bacteria. Environ. Microbiol. 7:1673-1685.
5. Better, M., B. Lewis, D. Corbin, G. Ditta, and D. R. Helinski. 1983. Structural relationships among Rhizobium meliloti symbiotic promoters. Cell 35: 479-485.
6. Birnboim, H. C. 1983. A rapid alkaline extraction method for the isolation of plasmid DNA. Methods Enzymol. 100:243-255.
7. Cabrol, S., A. Olliver, G. B. Pier, A. Andremont, and R. Ruimy. 2003. Transcription of quorum-sensing system genes in clinical and environmental isolates of Pseudomonas aeruginosa. J. Bacteriol. 185:7222-7230.
8. Corbin, D., G. Ditta, and D. R. Helinski. 1982. Clustering of nitrogen fixation (nif) genes in Rhizobium meliloti. J. Bacteriol. 149:221-228.
9. Curran, B., D. Jonas, H. Grundmann, T. Pitt, and C. G. Dowson. 2004. Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J. Clin. Microbiol. 42:5644-5649.
10. Devescovi, G., J. Bigirimana, G. Degrassi, L. Cabrio, J. J. Lipuma, J. Kim, I. Hwang, and V. Venturi. 2007. Involvement of a quorum-sensing- regulated secreted lipase A clinical isolate of Burkholderia glumae in severe disease symptoms in rice. Appl. Environ. Microbiol. 73:4950-4958.
11. De Vleesschauwer, D., P. Cornelis, and M. Hofte. 2006. Redox-active pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporthe grisea but enhances Rhizoctonia solani susceptibility in rice. Mol. Plant-Microbe Interact. 19:1406-1419.
12. Duan, K., and M. G. Surette. 2007. Environmental regulation of Pseudomonas aeruginosa PAO1 Las and Rhl quorum-sensing systems. J. Bacteriol. 189:4827-4836.
13. Egamberdieva, D., F. Kamilova, S. Validov, L. Gafurova, Z. Kucharova, and B. Lugtenberg. 2008. High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environ. Microbiol. 10:1-9.
14. Erickson, D. L., R. Endersby, A. Kirkham, K. Stuber, D. D. Vollman, H. R. Rabin, I. Mitchell, and D. G. Storey. 2002. Pseudomonas aeruginosa quorumsensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis. Infect. Immun. 70:1783-1790.
15. Figurski, D. H., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
16. Fuqua, C., and E. P. Greenberg. 2002. Listening in on bacteria: acyl-homoserine lactone signalling. Nat. Rev. Mol. Cell Biol. 3:685-695.
17. Graner, G., P. Persson, J. Meijer, and S. Alstrom. 2003. A study on microbial diversity in different cultivars of Brassica napus in relation to its wilt pathogen, Verticillium longisporum. FEMS Microbiol. Lett. 224:269-276.
18. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
19. Hentzer, M., L. Eberl, J. Nielsen, and M. Givskov. 2003. Quorum sensing: a novel target for the treatment of biofilm infections. BioDrugs 17:241-250.
20. Hoagland, D. R., and D. I. Arnon. 1950. The water-culture method for growing plants without soil. Calif. Agric. Exp. Station Circular 347:1-39.
21. Holloway, B. W. 1955. Genetic recombination in Pseudomonas aeruginosa. J. Gen. Microbiol. 13:572-581.
22. Huber, B., K. Riedel, M. Hentzer, A. Heydorn, A. Gotschlich, M. Givskov, S. Molin, and L. Eberl. 2001. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147:2517-2528.
23. Jander, G., L. G. Rahme, and F. M. Ausubel. 2000. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J. Bacteriol. 182:3843-3845.
24. King, E. O., M. K. Ward, and D. E. Raney. 1954. Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44:301-307.
25. Kohler, T., L. K. Curty, F. Barja, C. van Delden, and J. C. Pechere. 2000. Swarming of Pseudomonas aeruginosa is dependent on cell-to-cell signaling and requires flagella and pili. J. Bacteriol. 182:5990-5996.
26. Kothe, M., M. Antl, B. Huber, K. Stoecker, D. Ebrecht, I. Steinmetz, and L. Eberl. 2003. Killing of Caenorhabditis elegans by Burkholderia cepacia is controlled by the cep quorum-sensing system. Cell. Microbiol. 5:343-351.
27. Krechel, A., A. Faupel, J. Hallmann, A. Ulrich, and G. Berg. 2002. Potatoassociated bacteria and their antagonistic potential towards plant-pathogenic fungi and the plant-parasitic nematode Meloidogyne incognita (Kofoid & White) Chitwood. Can. J. Microbiol. 48:772-786.
28. Kumar, R. S., N. Ayyadurai, P. Pandiaraja, A. V. Reddy, Y. Venkateswarlu, O. Prakash, and N. Sakthivel. 2005. Characterization of antifungal metabolite produced by a new strain Pseudomonas aeruginosa PUPa3 that exhibits broad-spectrum antifungal activity and biofertilizing traits. J. Appl. Microbiol. 98:145-154.
29. Latifi, A., M. Foglino, K. Tanaka, P. Williams, and A. Lazdunski. 1996. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21:1137-1146.
30. Lyczak, J. B., C. L. Cannon, and G. B. Pier. 2000. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect. 2:1051-1060.
31. Maddula, V. S., Z. Zhang, E. A. Pierson, and L. S. Pierson III. 2006. Quorum sensing and phenazines are involved in biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30-84. Microb. Ecol. 52:289-301.
32. Magazin, M. D., J. C. Moores, and J. Leong. 1986. Cloning of the gene coding for the outer membrane receptor protein for ferric pseudobactin, a siderophore from a plant growth-promoting Pseudomonas strain. J. Biol. Chem. 261:795-799.
33. Mahajan-Miklos, S., L. G. Rahme, and F. M. Ausubel. 2000. Elucidating the molecular mechanisms of bacterial virulence using non-mammalian hosts. Mol. Microbiol. 37:981-988.
34. Mahajan-Miklos, S., M. W. Tan, L. G. Rahme, and F. M. Ausubel. 1999. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96:47-56.
35. Martinez-Granero, F., R. Rivilla, and M. Martin. 2006. Rhizosphere selection of highly motile phenotypic variants of Pseudomonas fluorescens with enhanced competitive colonization ability. Appl. Environ. Microbiol. 72: 3429-3434.
36. McClean, K. H., M. K. Winson, L. Fish, A. Taylor, S. R. Chhabra, M. Camara, M. Daykin, J. H. Lamb, S. Swift, B. W. Bycroft, G. S. Stewart, and P. Williams. 1997. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703-3711.
37. Miyata, S., M. Casey, D. W. Frank, F. M. Ausubel, and E. Drenkard. 2003. Use of the Galleria mellonella caterpillar as a model host to study the role of the type III secretion system in Pseudomonas aeruginosa pathogenesis. Infect. Immun. 71:2404-2413.
38. Morales, A., J. L. Garland, and D. V. Lim. 1996. Survival of potentially pathogenic human-associated bacteria in the rhizosphere of hydroponically grown wheat. FEMS Microbiol. Ecol. 20:155-162.
39. Murray, T. S., and B. I. Kazmierczak. 2006. FlhF is required for swimming and swarming in Pseudomonas aeruginosa. J. Bacteriol. 188:6995-7004.
40. O'Toole, G. A., and R. Kolter. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
41. Pirnay, J. P., S. Matthijs, H. Colak, P. Chablain, F. Bilocq, J. Van Eldere, D. De Vos, M. Zizi, L. Triest, and P. Cornelis. 2005. Global Pseudomonas aeruginosa biodiversity as reflected in a Belgian river. Environ. Microbiol. 7:969-980.
42. Rampioni, G., M. Schuster, E. P. Greenberg, I. Bertani, M. Grasso, V. Venturi, E. Zennaro, and L. Leoni. 2007. RsaL provides quorum sensing homeostasis and functions as a global regulator of gene expression in Pseudomonas aeruginosa. Mol. Microbiol. 66:1557-1565.
43. Riedel, K., M. Hentzer, O. Geisenberger, B. Huber, A. Steidle, H. Wu, N. Hoiby, M. Givskov, S. Molin, and L. Eberl. 2001. N-acylhomoserine- lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147:3249- 3262.
44. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. Schuster, M., and E. P. Greenberg. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int. J. Med. Microbiol. 296:73-81.
46. 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. 185:2066-2079.
47. Seed, K. D., and J. J. Dennis. 2008. Development of Galleria mellonella as an alternative infection model for the Burkholderia cepacia complex. Infect. Immun. 76:1267-1275.
48. Smith, R. S., and B. H. Iglewski. 2003. P. aeruginosa quorum-sensing systems and virulence. Curr. Opin. Microbiol. 6:56-60.
49. Staskawicz, B., D. Dahlbeck, N. Keen, and C. Napoli. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:5789-5794.
50. Steidle, A., K. Sigl, R. Schuhegger, A. Ihring, M. Schmid, S. Gantner, M. Stoffels, K. Riedel, M. Givskov, A. Hartmann, C. Langebartels, and L. Eberl. 2001. Visualization of N-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl. Environ. Microbiol. 67:5761-5770.
51. Steindler, L., I. Bertani, L. De Sordi, J. Bigirimana, and V. Venturi. 2008. The presence, type and role of N-acyl homoserine lactone quorum sensing in fluorescent Pseudomonas originally isolated from rice rhizospheres are unpredictable. FEMS Microbiol. Lett. 288:102-111.
52. Steindler, L., G. Devescovi, S. Subramoni, and V. Venturi. 2008. A versatile plasmid biosensor useful to identify quorum sensing LuxR-family orphans in bacterial strains. J. Microbiol. Methods 73:273-275.
53. Steindler, L., and V. Venturi. 2007. Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol. Lett. 266:1-9.
54. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, I. T. Paulsen, J. Reizer, M. H. Saier, R. E. Hancock, S. Lory, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406:959-964.
55. Tripathi, A. K., S. C. Verma, and E. Z. Ron. 2002. Molecular characterization of a salt-tolerant bacterial community in the rice rhizosphere. Res. Microbiol. 153:579-584.
56. Venturi, V. 2006. Regulation of quorum sensing in Pseudomonas. FEMS Microbiol. Rev. 30:274-291.
57. Venturi, V., F. Zennaro, G. Degrassi, B. C. Okeke, and C. V. Bruschi. 1998. Genetics of ferulic acid bioconversion to protocatechuic acid in plant-growth-promoting Pseudomonas putida WCS358. Microbiology 144:965-973.
58. Wagner, V. E., D. Bushnell, L. Passador, A. I. Brooks, and B. H. Iglewski. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185:2080-2095.
59. Walker, T. S., H. P. Bais, E. Deziel, H. P. Schweizer, L. G. Rahme, R. Fall, and J. M. Vivanco. 2004. Pseudomonas aeruginosa-plant root interactions. Pathogenicity, biofilm formation, and root exudation. Plant Physiol. 134:320-331.
60. Wei, H. L., and L. Q. Zhang. 2006. Quorum-sensing system influences root colonization and biological control ability in Pseudomonas fluorescens 2P24. Antonie van Leeuwenhoek 89:267-280.
61. Winson, M. K., S. Swift, L. Fish, J. P. Throup, F. Jorgensen, S. R. Chhabra, B. W. Bycroft, P. Williams, and G. S. Stewart. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163:185-192.
62. Wopperer, J., S. T. Cardona, B. Huber, C. A. Jacobi, M. A. Valvano, and L. Eberl. 2006. A quorum-quenching approach to investigate the conservation of quorum-sensing-regulated functions within the Burkholderia cepacia complex. Appl. Environ. Microbiol. 72:1579-1587.
63. Yanisch-Peron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-109.