1887

Abstract

3937 (ex ), a member of the , causes soft rot in many economically important crops. A successful pathogen has to reach the interior of the plant in order to cause disease. To study the role of motility and chemotaxis in the pathogenicity of 3937, genes involved in the chemotactic signal transduction system (, , and ) and in the structure of the flagellar motor () were mutagenized. All the mutant strains grew like the wild-type in culture media, and the production and secretion of pectolytic enzymes was not affected. As expected, the swimming ability of the mutant strains was reduced with respect to the wild-type: (94 %), (80 %), (74 %), (54 %) and (48 %). The virulence of the mutant strains was analysed in chicory, Saintpaulia and potato. The mutant strains were also tested for their capability to enter into Arabidopsis leaves. All the mutants showed a significant decrease of virulence in certain hosts; however, the degree of virulence reduction varied depending on the virulence assay. The ability to penetrate Arabidopsis leaves was impaired in all the mutants, whereas the capacity to colonize potato tubers after artificial inoculation was affected in only two mutant strains. In general, the virulence of the mutants could be ranked as <<=<, which correlated with the degree to which swimming was affected. These results clearly indicate that motility plays an important role in the pathogenicity of this bacterium.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.022244-0
2009-02-01
2019-12-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/2/434.html?itemId=/content/journal/micro/10.1099/mic.0.022244-0&mimeType=html&fmt=ahah

References

  1. Alfano, J. R. & Collmer, A. ( 1997; ). The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179, 5655–5662.
    [Google Scholar]
  2. Armitage, J. P. & Macnab, R. M. ( 1987; ). Unidirectional, intermittent rotation of the flagellum of Rhodobacter sphaeroides. J Bacteriol 169, 514–518.
    [Google Scholar]
  3. Barras, F., Van Gijsegem, F. & Chatterjee, A. K. ( 1994; ). Extracellular enzymes and pathogenesis of soft-rot Erwinia. Annu Rev Phytopathol 32, 201–234.[CrossRef]
    [Google Scholar]
  4. Bauer, D. W., Bogdanove, A. J., Beer, S. V. & Collmer, A. ( 1994; ). Erwinia chrysanthemi hrp genes and their involvement in soft rot pathogenesis and elicitation of the hypersensitive response. Mol Plant Microbe Interact 7, 573–581.[CrossRef]
    [Google Scholar]
  5. Blair, D. F. & Berg, H. C. ( 1990; ). The MotA protein of E. coli is a proton-conducting component of the flagellar motor. Cell 60, 439–449.[CrossRef]
    [Google Scholar]
  6. Boyd, A., Mandel, G. & Simon, M. I. ( 1982; ). Integral membrane proteins required for bacterial motility and chemotaxis. Symp Soc Exp Biol 35, 123–137.
    [Google Scholar]
  7. Burall, L. S., Harro, J. M., Li, X., Lockatell, C. V., Himpsl, S. D., Hebel, J. R., Johnson, D. E. & Mobley, H. L. ( 2004; ). Proteus mirabilis genes that contribute to pathogenesis of urinary tract infection: identification of 25 signature-tagged mutants attenuated at least 100-fold. Infect Immun 72, 2922–2938.[CrossRef]
    [Google Scholar]
  8. Burkart, M., Toguchi, A. & Harshey, R. M. ( 1998; ). The chemotaxis system, but not chemotaxis, is essential for swarming motility in Escherichia coli. Proc Natl Acad Sci U S A 95, 2568–2573.[CrossRef]
    [Google Scholar]
  9. Butler, S. M. & Camilli, A. ( 2004; ). Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae. Proc Natl Acad Sci U S A 101, 5018–5023.[CrossRef]
    [Google Scholar]
  10. Butler, S. M. & Camilli, A. ( 2005; ). Going against the grain: chemotaxis and infection in Vibrio cholerae. Nat Rev Microbiol 3, 611–620.[CrossRef]
    [Google Scholar]
  11. Collmer, A., Schoedel, C., Roeder, D. L., Ried, J. L. & Rissler, J. F. ( 1985; ). Molecular cloning in Escherichia coli of Erwinia chrysanthemi genes encoding multiple forms of pectate lyase. J Bacteriol 161, 913–920.
    [Google Scholar]
  12. Dons, L., Eriksson, E., Jin, Y., Rottenberg, M. E., Kristensson, K., Larsen, C. N., Bresciani, J. & Olsen, J. E. ( 2004; ). Role of flagellin and the two-component CheA/CheY system of Listeria monocytogenes in host cell invasion and virulence. Infect Immun 72, 3237–3244.[CrossRef]
    [Google Scholar]
  13. Dowd, J. P. & Matsumura, P. ( 1997; ). The use of flash photolysis for a high-resolution temporal and spatial analysis of bacterial chemotactic behaviour: CheZ is not always necessary for chemotaxis. Mol Microbiol 25, 295–302.[CrossRef]
    [Google Scholar]
  14. Eisenbach, M. ( 1996; ). Control of bacterial chemotaxis. Mol Microbiol 20, 903–910.[CrossRef]
    [Google Scholar]
  15. el Hassouni, M., Chambost, J. P., Expert, D., Van Gijsegem, F. & Barras, F. ( 1999; ). The minimal gene set member msrA, encoding peptide methionine sulfoxide reductase, is a virulence determinant of the plant pathogen Erwinia chrysanthemi. Proc Natl Acad Sci U S A 96, 887–892.[CrossRef]
    [Google Scholar]
  16. Expert, D. ( 1999; ). Withholding and exchanging iron: interactions between Erwinia spp. and their plant hosts. Annu Rev Phytopathol 37, 307–334.[CrossRef]
    [Google Scholar]
  17. Franza, T., Sauvage, C. & Expert, D. ( 1999; ). Iron regulation and pathogenicity in Erwinia chrysanthemi 3937: role of the Fur repressor protein. Mol Plant Microbe Interact 12, 119–128.[CrossRef]
    [Google Scholar]
  18. Hanahan, D. ( 1983; ). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557–580.[CrossRef]
    [Google Scholar]
  19. Harshey, R. M. ( 2003; ). Bacterial motility on a surface: many ways to a common goal. Annu Rev Microbiol 57, 249–273.[CrossRef]
    [Google Scholar]
  20. King, E. O., Ward, M. K. & Raney, O. E. ( 1954; ). Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med 44, 301–307.
    [Google Scholar]
  21. Kotoujansky, A., Diolez, A., Boccara, M., Bertheau, Y., Andro, T. & Coleno, A. ( 1985; ). Molecular cloning of Erwinia chrysanthemi pectinase and cellulase structural genes. EMBO J 4, 781–785.
    [Google Scholar]
  22. Llama-Palacios, A., Lopez-Solanilla, E., Poza-Carrion, C., Garcia-Olmedo, F. & Rodriguez-Palenzuela, P. ( 2003; ). The Erwinia chrysanthemi phoP-phoQ operon plays an important role in growth at low pH, virulence and bacterial survival in plant tissue. Mol Microbiol 49, 347–357.[CrossRef]
    [Google Scholar]
  23. Lopez-Solanilla, E., Garcia-Olmedo, F. & Rodriguez-Palenzuela, P. ( 1998; ). Inactivation of the sapA to sapF locus of Erwinia chrysanthemi reveals common features in plant and animal bacterial pathogenesis. Plant Cell 10, 917–924.
    [Google Scholar]
  24. Lopez-Solanilla, E., Llama-Palacios, A., Collmer, A., Garcia-Olmedo, F. & Rodriguez-Palenzuela, P. ( 2001; ). Relative effects on virulence of mutations in the sap, pel, and hrp loci of Erwinia chrysanthemi. Mol Plant Microbe Interact 14, 386–393.[CrossRef]
    [Google Scholar]
  25. Lux, R. & Shi, W. ( 2004; ). Chemotaxis-guided movements in bacteria. Crit Rev Oral Biol Med 15, 207–220.[CrossRef]
    [Google Scholar]
  26. Miguel, E., Poza-Carrion, C., Lopez-Solanilla, E., Aguilar, I., Llama-Palacios, A., Garcia-Olmedo, F. & Rodriguez-Palenzuela, P. ( 2000; ). Evidence against a direct antimicrobial role of H2O2 in the infection of plants by Erwinia chrysanthemi. Mol Plant Microbe Interact 13, 421–429.[CrossRef]
    [Google Scholar]
  27. Parkinson, J. S., Ames, P. & Studdert, C. A. ( 2005; ). Collaborative signaling by bacterial chemoreceptors. Curr Opin Microbiol 8, 116–121.[CrossRef]
    [Google Scholar]
  28. Rodríguez, A., Guil, N., Shotton, D. M. & Trelles, O. ( 2004; ). Automatic analysis of the content of cell biological videos and database organization of their metadata descriptors. IEEE Trans Multimed 6, 119–128.[CrossRef]
    [Google Scholar]
  29. Sambrook, J., Fritsch, E. F. & Maniatis, T. A. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  30. Sanna, M. G. & Simon, M. I. ( 1996; ). In vivo and in vitro characterization of Escherichia coli protein CheZ gain- and loss-of-function mutants. J Bacteriol 178, 6275–6280.
    [Google Scholar]
  31. Sourjik, V. & Berg, H. C. ( 2004; ). Functional interactions between receptors in bacterial chemotaxis. Nature 428, 437–441.[CrossRef]
    [Google Scholar]
  32. Stecher, B., Hapfelmeier, S., Muller, C., Kremer, M., Stallmach, T. & Hardt, W. D. ( 2004; ). Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72, 4138–4150.[CrossRef]
    [Google Scholar]
  33. Stephens, B. B., Loar, S. N. & Alexandre, G. ( 2006; ). Role of CheB and CheR in the complex chemotactic and aerotactic pathway of Azospirillum brasilense. J Bacteriol 188, 4759–4768.[CrossRef]
    [Google Scholar]
  34. Studdert, C. A. & Parkinson, J. S. ( 2004; ). Crosslinking snapshots of bacterial chemoreceptor squads. Proc Natl Acad Sci U S A 101, 2117–2122.[CrossRef]
    [Google Scholar]
  35. Terry, K., Williams, S. M., Connolly, L. & Ottemann, K. M. ( 2005; ). Chemotaxis plays multiple roles during Helicobacter pylori animal infection. Infect Immun 73, 803–811.[CrossRef]
    [Google Scholar]
  36. Wadhams, G. H. & Armitage, J. P. ( 2004; ). Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5, 1024–1037.[CrossRef]
    [Google Scholar]
  37. Yamaguchi, S., Aizawa, S., Kihara, M., Isomura, M., Jones, C. J. & Macnab, R. M. ( 1986; ). Genetic evidence for a switching and energy-transducing complex in the flagellar motor of Salmonella typhimurium. J Bacteriol 168, 1172–1179.
    [Google Scholar]
  38. Yang, S., Perna, N. T., Cooksey, D. A., Okinaka, Y., Lindow, S. E., Ibekwe, A. M., Keen, N. T. & Yang, C. H. ( 2004; ). Genome-wide identification of plant-upregulated genes of Erwinia chrysanthemi 3937 using a GFP-based IVET leaf array. Mol Plant Microbe Interact 17, 999–1008.[CrossRef]
    [Google Scholar]
  39. Yao, J. & Allen, C. ( 2006; ). Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J Bacteriol 188, 3697–3708.[CrossRef]
    [Google Scholar]
  40. Yao, R., Burr, D. H. & Guerry, P. ( 1997; ). CheY-mediated modulation of Campylobacter jejuni virulence. Mol Microbiol 23, 1021–1031.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.022244-0
Loading
/content/journal/micro/10.1099/mic.0.022244-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error