1887

Abstract

This report describes a new behavioural response of that consists of a surface-induced differentiation of elongated and hyperflagellated swarm cells exhibiting the ability to move collectively across the surface of the medium. The discovery of swarming motility in paralleled the isolation of a spontaneous non-swarming mutant that was found to carry a deletion of , the homologue of which, in , encodes an essential component of the flagellar motor-switch complex. However, in contrast to , the mutant of was flagellated and motile, thus suggesting a different role for FliY in this organism. The mutant was completely deficient in chemotaxis and in the secretion of the L component of the tripartite pore-forming necrotizing toxin, haemolysin BL, which was produced exclusively by the wild-type strain during swarm-cell differentiation. All the defects in the mutant of could be complemented by a plasmid harbouring the gene. These results demonstrate that the activity of is required for swarming and chemotaxis in , and suggest that swarm-cell differentiation is coupled with virulence in this organism.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-6-1785
2002-06-01
2020-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/6/1481785a.html?itemId=/content/journal/micro/10.1099/00221287-148-6-1785&mimeType=html&fmt=ahah

References

  1. Albertini A. M., Caramori T., Crabb W. D., Scoffone F., Galizzi A. 1991; The flaA locus of Bacillus subtilis is part of a large operon coding for flagellar structures, motility functions, and an ATPase-like polypeptide. J Bacteriol173:3573–3579
    [Google Scholar]
  2. Allison C., Coleman N., Jones P. L., Hughes C. 1992a; Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect Immun60:4740–4746
    [Google Scholar]
  3. Allison C., Lai H. C., Hughes C. 1992b; Co-ordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis . Mol Microbiol6:1583–1591[CrossRef]
    [Google Scholar]
  4. Allison C., Emody L., Coleman N., Hughes C. 1994; The role of swarm-cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis . J Infect Dis69:1155–1158
    [Google Scholar]
  5. Arantes O., Lereclus D. 1991; Construction of cloning vectors for Bacillus thuringiensis . Gene108:115–119[CrossRef]
    [Google Scholar]
  6. Beecher D. J., Wong A. C. L. 1994; Identification of hemolysin BL-producing Bacillus cereus isolates by a discontinuous hemolytic pattern in blood agar. Appl Environ Microbiol60:1646–1651
    [Google Scholar]
  7. Beecher D. J., Pulido J. S., Barney N. P., Wong A. C. L. 1995a; Extracellular virulence factors in Bacillus cereus endophthalmitis: methods and implication of involvement of hemolysin BL. Infect Immun63:632–639
    [Google Scholar]
  8. Beecher D. J., Schoeni J. L., Wong A. C. L. 1995b; Enterotoxic activity of hemolysin BL from Bacillus cereus . Infect Immun63:4423–4428
    [Google Scholar]
  9. Belas M. R., Colwell R. R. 1982; Adsorption kinetics of laterally and polarly flagellated Vibrio . J Bacteriol151:1568–1580
    [Google Scholar]
  10. Belas R., Erskine D., Flaherty D. 1991; Proteus mirabilis mutants defective in swarmer cell differentiation and multicellular behavior. J Bacteriol173:6279–6288
    [Google Scholar]
  11. Belas R., Goldman M., Ashliman K. 1995; Genetic analysis of Proteus mirabilis mutants defective in swarmer cell elongation. J Bacteriol177:823–828
    [Google Scholar]
  12. Bischoff D. S., Ordal G. W. 1992; Identification and characterization of FliY, a novel component of the Bacillus subtilis flagellar switch complex. Mol Microbiol18:2715–2723
    [Google Scholar]
  13. 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 USA95:2568–2573[CrossRef]
    [Google Scholar]
  14. Celandroni F., Ghelardi E., Pastore M., Lupetti A., Kolstø A.-B., Senesi S. 2000; Characterization of the chemotaxis fliY and cheA genes in Bacillus cereus . FEMS Microbiol Lett190:247–253[CrossRef]
    [Google Scholar]
  15. Eberl L., Christiansen G., Molin S., Givskov M. 1996; Differentiation of Serratia liquefaciens into swarm cells is controlled by the expression of the flhD master operon. J Bacteriol178:554–559
    [Google Scholar]
  16. Eberl L., Molin S., Givskov M. 1999; Surface motility of Serratia liquefaciens MG1. J Bacteriol181:1703–1712
    [Google Scholar]
  17. Givaudan A., Lanois A. 2000; flhDC , the flagellar master operon of Xenorhabdus nematophilus : requirement for motility, lipolysis, extracellular hemolysis, and full virulence in insects. J Bacteriol182:107–115[CrossRef]
    [Google Scholar]
  18. Gygi D., Bailey M. J., Allison C., Huges C. 1995; Requirement for FlhA in flagella assembly and swarm-cell differentiation by Proteus mirabilis . Mol Microbiol15:761–769
    [Google Scholar]
  19. Hanson R. S., Srinivasan V. R., Harvonson H. O. 1961; Citrate formation in B. cereus strain T. Biochem Biophys Res Commun5:458–461
    [Google Scholar]
  20. Harshey R. M. 1994; Bees aren’t the only ones: swarming in Gram-negative bacteria. Mol Microbiol13:389–394[CrossRef]
    [Google Scholar]
  21. Harshey R. M., Matsuyama T. 1994; Dimorphic transition in Escherichia coli and Salmonella typhimurium : surface-induced differentiation into hyperflagellate swarmer cells. Proc Natl Acad Sci USA91:8631–8635[CrossRef]
    [Google Scholar]
  22. Henderson I., Duggleby C. J., Turnbull P. C. B. 1994; Differentiation of Bacillus anthracis from other Bacillus cereus group bacteria with the PCR. Int J Syst Bacteriol44:99–105[CrossRef]
    [Google Scholar]
  23. Henrichsen J. 1972; Bacterial surface translocation: a survey and a classification. Bacteriol Rev36:478–503
    [Google Scholar]
  24. Hoeniger J. F. M., Taushel H.-D. 1974; Sequence of structural changes in cultures of Clostridium tetani grown on a solid medium. J Med Microbiol7:425–432[CrossRef]
    [Google Scholar]
  25. Lereclus D., Arantes O, Chaufaux J., Lecadet M. M. 1989; Transformation and expression of a cloned δ-endotoxin gene in Bacillus thuringiensis . FEMS Microbiol Lett60:211–218
    [Google Scholar]
  26. Macfarlane S., Hopkins M. J., Macfarlane G. T. 2001; Toxin synthesis and mucin breakdown are related to swarming phenomenon in Clostridium septicum . Infect Immun69:1120–1126[CrossRef]
    [Google Scholar]
  27. Macnab R. M. 1996; Flagella and motility. Escherichia coli and Salmonella: Cellular and Molecular Biology123–145 Washington, DC: American Society for Microbiology;
    [Google Scholar]
  28. Miller J. M., Hair J. G., Hebert M., Hebert L., Roberts F. J. Jr, Weyant R. S. 1997; Fulminating bacteremia and pneumonia due to Bacillus cereus . J Clin Microbiol35:504–507
    [Google Scholar]
  29. Ordal G. W., Goldman D. J. 1975; Chemotaxis away from uncouplers of oxidative phosphorylation in Bacillus subtilis . Science189:802–805[CrossRef]
    [Google Scholar]
  30. O’Rear J., Alberti L., Harshey R. M. 1992; Mutations that impair swarming motility in Serratia marcescens 274 include but are not limited to those affecting chemotaxis or flagellar functions. J Bacteriol174:6125–6137
    [Google Scholar]
  31. Prüb B. M., Dietrich R., Nibler B., Märtlbauer E., Scherer S. 1999; The hemolytic enterotoxin HBL is broadly distributed among species of the Bacillus cereus group. Appl Environ Microbiol65:5436–5442
    [Google Scholar]
  32. Rashid M. H., Kornberg A. 2000; Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa . Proc Natl Acad Sci USA97:4885–4890[CrossRef]
    [Google Scholar]
  33. Sambrook J., Fritsch E. F., Maniatis T. 1989; Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  34. Schoeni J. L., Wong A C. L. 1999; Heterogeneity observed in the components of hemolysin BL, and enterotoxin produced by Bacillus cereus . Int J Food Microbiol53:159–167[CrossRef]
    [Google Scholar]
  35. Senesi S., Cercignani G., Freer G., Batoni G., Barnini S., Ota F. 1991; Structural and stereospecific requirements for the nucleoside-triggered germination of Bacillus cereus spores. J Gen Microbiol137:399–404[CrossRef]
    [Google Scholar]
  36. Steen K., Bruno-Murtha L. A., Chaux G., Lazar H., Bernard S., Sulis C. 1992; Bacillus cereus endocarditis: report of a case and review. Clin Infect Dis14:945–946[CrossRef]
    [Google Scholar]
  37. Stewart B. J., Enos-Berlage J. L., McCarter L. L. 1997; The lonS gene regulates swarmer cell differentiation of Vibrio parahaemolyticus . J Bacteriol179:107–114
    [Google Scholar]
  38. Vahey J. B., Flynn H. W. Jr. 1991; Results in the management of Bacillus endophthalmitis. Ophthalmic Surg22:681–686
    [Google Scholar]
  39. Young M. G., Smith M. J., Minnich S. A., Miller V. L. 1999; The Yersinia enterocolitica motility master operon, flhDC , is required for flagellin production, swimming motility and swarming motility. J Bacteriol181:2823–2833
    [Google Scholar]
  40. Zuberi A. R., Bischoff O. S., Ordal G. W. 1991; Nucleotide sequence and characterization of a Bacillus subtilis gene encoding a flagellar switch protein. J Bacteriol173:710–719
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-6-1785
Loading
/content/journal/micro/10.1099/00221287-148-6-1785
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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