Identification of genes in the VirR regulon of Pectobacterium atrosepticum and characterization of their roles in quorum sensing-dependent virulence

Environmental Microbiology

Volumn 15, Issue 3, 2013, Pages 687-701

  Monson, Rita ^a   Burr, Tom ^a   Carlton, Timothy ^a   Liu, Hui ^b   Hedley, Peter ^b   Toth, Ian ^b   Salmond, George P C ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DRUG DERIVATIVE; GAMMA BUTYROLACTONE; HOMOSERINE LACTONE; SIDEROPHORE; TRANSCRIPTOME;

ARTICLE; BINDING SITE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PECTOBACTERIUM; PLANT; PROMOTER REGION; PROTEIN BINDING; QUORUM SENSING; REGULON; VIRULENCE;

4-BUTYROLACTONE; BACTERIAL PROTEINS; BINDING SITES; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MUTATION; PECTOBACTERIUM; PLANTS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; QUORUM SENSING; REGULON; SIDEROPHORES; TRANSCRIPTOME; VIRULENCE;

NEGIBACTERIA; PECTOBACTERIUM; PECTOBACTERIUM ATROSEPTICUM;

EID: 84874704875     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2012.02822.x     Document Type: Article

References (51)

1. Barnard, A.M., Bowden, S.D., Burr, T., Coulthurst, S.J., Monson, R.E., and Salmond, G.P. (2007) Quorum sensing, virulence and secondary metabolite production in plant soft-rotting bacteria. Philos Trans R Soc Lond B Biol Sci 362: 1165-1183.
2. Bartz, J.A., and Kelman, A. (1984) Bacterial soft rot potential in washed potato-tubers in relation to temperatures of tubers and water during simulated commercial handling practices. Am Potato J 61: 485-493.
3. Bell, K.S., Sebaihia, M., Pritchard, L., Holden, M.T., Hyman, L.J., Holeva, M.C., etal. (2004) Genome sequence of the enterobacterial phytopathogen Erwinia carotovora subsp. atroseptica and characterization of virulence factors. Proc Natl Acad Sci USA 101: 11105-11110.
4. Bohlander, S.K., Espinosa, R., 3rd, Le Beau, M.M., Rowley, J.D., and Diaz, M.O. (1992) A method for the rapid sequence-independent amplification of microdissected chromosomal material. Genomics 13 : 1322-1324.
5. Brockhurst, M.A., Buckling, A., Racey, D., and Gardner, A. (2008) Resource supply and the evolution of public-goods cooperation in bacteria. BMC Biol 6: 20.
6. Burr, T., Barnard, A.M., Corbett, M.J., Pemberton, C.L., Simpson, N.J., and Salmond, G.P. (2006) Identification of the central quorum sensing regulator of virulence in the enteric phytopathogen, Erwinia carotovora: the VirR repressor. Mol Microbiol 59: 113-125.
7. Castang, S., Reverchon, S., Gouet, P., and Nasser, W. (2006) Direct evidence for the modulation of the activity of the Erwinia chrysanthemi quorum-sensing regulator ExpR by acylhomoserine lactone pheromone. J Biol Chem 281: 29972-29987.
8. Chatterjee, A., Cui, Y., Liu, Y., Dumenyo, C.K., and 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.
9. Chatterjee, A., Cui, Y., and Chatterjee, A.K. (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: 4089-4095.
10. Corbett, M., Virtue, S., Bell, K., Birch, P., Burr, T., Hyman, L., etal. (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: 334-342.
11. Cui, Y., Chatterjee, A., Hasegawa, H., and Chatterjee, A.K. (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: 4715-4726.
12. Enard, C., Diolez, A., and Expert, D. (1988) Systemic virulence of Erwinia chrysanthemi 3937 requires a functional iron assimilation system. J Bacteriol 170: 2419-2426.
13. Franza, T., Sauvage, C., and Expert, D. (1999) Iron regulation and pathogenicity in Erwinia chrysanthemi 3937: role of the Fur repressor protein. Mol Plant Microbe Interact 12: 119-128.
14. Gardan, L., Gouy, C., Christen, R., and Samson, R. (2003) 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 53: 381-391.
15. Grainger, D.C., Overton, T.W., Reppas, N., Wade, J.T., Tamai, E., Hobman, J.L., etal. (2004) Genomic studies with Escherichia coli MelR protein: applications of chromatin immunoprecipitation and microarrays. J Bacteriol 186: 6938-6943.
16. Grinter, N.J. (1983) A broad-host-range cloning vector transposable to various replicons. Gene 21 : 133-143.
17. Gristwood, T., Fineran, P.C., Everson, L., and Salmond, G.P. (2008) PigZ, a TetR/AcrR family repressor, modulates secondary metabolism via the expression of a putative four-component resistance-nodulation-cell-division efflux pump, ZrpADBC, in Serratia sp. ATCC 39006. Mol Microbiol 69: 418-435.
18. Harris, S.J., Shih, Y.L., Bentley, S.D., and Salmond, G.P.C. (1998) The hexA gene of Erwinia carotovoa encodes a LysR homologue and regulates motility and the expression of multiple virulence determinants. Mol Micriobiol 28 : 705-707.
19. Harrison, F., and Buckling, A. (2009) Cooperative production of siderophores by Pseudomonas aeruginosa. Front Biosci 14: 4113-4126.
20. van Helden, J., Andre, B., and Collado-Vides, J. (2000) A web site for the computational analysis of yeast regulatory sequences. Yeast 16: 177-187.
21. Herrero, M., De Lorenzo, V., and Timmis, K.N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gram-negative bacteria. J Bacteriol 172 : 6557-6567.
22. Jones, S., Yu, B., Bainton, N.J., Birdsall, M., Bycroft, B.W., Chhabra, S.R., etal. (1993) The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J 12: 2477-2482.
23. Juhas, M., Wiehlmann, L., Huber, B., Jordan, D., Lauber, J., Salunkhe, P., etal. (2004) Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150: 831-841.
24. Kaniga, K., Delor, I., and Cornelis, G.R. (1991) A wide-host-range suicide vector for improving reverse genetics in gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109: 137-141.
25. Lamont, I.L., Beare, P.A., Ochsner, U., Vasil, A.I., and Vasil, M.L. (2002) Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 99: 7072-7077.
26. Liu, H., Coulthurst, S.J., Pritchard, L., Hedley, P.E., Ravensdale, M., Humphris, S., etal. (2008) Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog 4: e1000093.
27. Liu, X., Brutlag, D.L., and Liu, J.S. (2001) BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes. Pac Symp Biocomput 6: 127-138.
28. Liu, Y., Cui, Y., Mukherjee, A., and Chatterjee, A.K. (1998) Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Mol Microbiol 29: 219-234.
29. Lodge, J., Fear, J., Busby, S., Gunasekaran, P., and Kamini, N.R. (1992) Broad host range plasmids carrying the Escherichia coli lactose and galactose operons. FEMS Microbiol Lett 74: 271-276.
30. de Lorenzo, V., Herrero, M., Jakubzik, U., and Timmis, K.N. (1990) Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol 172 : 6568-6572.
31. McGowan, S.J., Barnard, A.M., Bosgelmez, G., Sebaihia, M., Simpson, N.J., Thomson, N.R., etal. (2005) Carbapenem antibiotic biosynthesis in Erwinia carotovora is regulated by physiological and genetic factors modulating the quorum sensing-dependent control pathway. Mol Microbiol 55: 526-545.
32. McGuire, R.G., and Kelman, A. (1983) Susceptibility of potato cultivars to Erwinia soft rot. Phytopathology 73: 809.
33. Miller, J. (1972) Experiments in Molecular Genetics. New York, USA: Cold Spring Harbour Laboratory Press.
34. Minogue, T.D., Wehland-von Trebra, M., Bernhard, F., and 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.
35. Mulholland, V., Hinton, J.C., Sidebotham, J., Toth, I.K., Hyman, L.J., Perombelon, M.C., etal. (1993) A pleiotropic reduced virulence (Rvi-) mutant of Erwinia carotovora subspecies atroseptica is defective in flagella assembly proteins that are conserved in plant and animal bacterial pathogens. Mol Microbiol 10: 1154.
36. Pearson, J.P., Van Delden, C., and Iglewski, B.H. (1999) Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J Bacteriol 181: 1203-1210.
37. Pemberton, C.L., Whitehead, N.A., Sebaihia, M., Bell, K.S., Hyman, L.J., Harris, S.J., etal. (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: 343-353.
38. Perombelon, M.C.M. (2002) Potato diseases caused by soft rot erwinias: an overview of pathogenesis. Plant Pathol 51: 1-12.
39. Pirhonen, M., Flego, D., Heikinheimo, R., and 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.
40. Roux, A., Payne, S.M., and Gilmore, M.S. (2009) Microbial telesensing: probing the environment for friends, foes, and food. Cell Host Microbe 6: 115-124.
41. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York, NY, USA: Cold Spring Harbour Laboratory Press.
42. Schwyn, B., and Neilands, J.B. (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160: 47-56.
43. Shih, Y.L., Harris, S.J., Borner, G., Rivet, M.M., and Salmond, G.P. (1999) The hexY genes of Erwinia carotovora ssp. carotovora and ssp. atroseptica encode novel proteins that regulate virulence and motility co-ordinately. Environ Microbiol 1: 535-547.
44. Sjoblom, S., Brader, G., Koch, G., and Palva, E.T. (2006) Cooperation of two distinct ExpR regulators controls quorum sensing specificity and virulence in the plant pathogen Erwinia carotovora. Mol Microbiol 60: 1474-1489.
45. Slater, H., Crow, M., Everson, L., and Salmond, G.P. (2003) Phosphate availability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol Microbiol 47: 303-320.
46. Song, Y., Xie, C., Ong, Y.M., Gan, Y.H., and Chua, K.L. (2005) The BpsIR quorum-sensing system of Burkholderia pseudomallei. J Bacteriol 187: 785-790.
47. Toth, I.K., and Birch, P.R. (2005) Rotting softly and stealthily. Curr Opin Plant Biol 8: 424-429.
48. Toth, I.K., Bell, K.S., Holeva, M.C., and Birch, P.R. (2003) Soft rot erwiniae: from genes to genomes. Mol Plant Pathol 4: 17-30.
49. Tsai, C.S., and Winans, S.C. (2010) LuxR-type quorum-sensing regulators that are detached from common scents. Mol Microbiol 77: 1072-1082.
50. Tsai, C.S., and Winans, S.C. (2011) The quorum-hindered transcription factor YenR of Yersinia enterocolitica inhibits pheromone production and promotes motility via a small non-coding RNA. Mol Microbiol 80: 556-571.
51. Von Bodman, S.B., Bauer, W.D., and Coplin, D.L. (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41: 455-482.