1887

Abstract

Halogenated furanones produced by the benthic marine macroalga inhibit swarming motility of MG1. This study demonstrates that exogenously added furanones control transcription of the quorum sensing regulated gene in competition with the cognate signal molecule -butanoyl-L-homoserine lactone. This in turn results in reduced production of the surface-active compound serrawettin W2, which is crucial for surface translocation of the differentiated swarm cells. It is demonstrated that furanones interfere with interspecies communication during swarming of mixed cultures and that the mode of interference in quorum-sensing control and interspecies communication is not through inhibition of autoinducer synthesis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-146-12-3237
2000-12-01
2020-04-07
Loading full text...

Full text loading...

/deliver/fulltext/micro/146/12/1463237a.html?itemId=/content/journal/micro/10.1099/00221287-146-12-3237&mimeType=html&fmt=ahah

References

  1. Allison C., Lai H. C., Hughes C.. 1992a; Co-ordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis. Mol Microbiol6:1583–1591[CrossRef]
    [Google Scholar]
  2. Allison C., Jones P., Coleman N., Hughes C.. 1992b; Ability of Proteus mirabilis to invade human urothelial cells is coupled to motility and swarming differentiation. Infect Immun60:4740–4746
    [Google Scholar]
  3. Andersen J. B., Sternberg C., Poulsen L. K., Bjorn S. P., Givskov M., Molin S.. 1998; New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol64:2240–2246
    [Google Scholar]
  4. Bassler B. L., Greenberg P., Stevens A. M.. 1997; Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J Bacteriol179:4043–4045
    [Google Scholar]
  5. Costerton J. W., Lewandowski Z., Caldwell D. E., Korber D. R., Lappin-Scott H. M.. 1995; Microbial biofilms. Annu Rev Microbiol49:711–747[CrossRef]
    [Google Scholar]
  6. Davies D. G., Parsek M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P.. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science280:295–298[CrossRef]
    [Google Scholar]
  7. Eberl L., Winson M. K., Sternberg C..7 other authors 1996a; Involvement of N-acyl-l-homoserine lactone autoinducers in control of multicellular behaviour of. Serratia liquefaciens. Mol Microbiol20:127–136[CrossRef]
    [Google Scholar]
  8. Eberl L., Christiansen G., Molin S., Givskov M.. 1996b; Differentiation of Serratia liquefaciens into swarm cells is controlled by the expression of the flhD master operon. J Bacteriol178:554–559
    [Google Scholar]
  9. Eberl L., Molin S., Givskov M.. 1999; Surface motility of Serratia liquefaciens MG1. J Bacteriol181:1703–1712
    [Google Scholar]
  10. Geisenberger O., Givskov M., Riedel K., Høiby N., Tümmler B., Eberl L.. 2000; Production of N-acyl-l-homoserine lactones by Pseudomonas aeruginosa isolates from chronic lung infections associated with cystic fibrosis. . FEMS Microbiol Lett184:273–277
    [Google Scholar]
  11. Givskov M., Olsen L., Molin S.. 1988; Cloning and expression in Escherichia coli of the gene for extracellular phospholipase A1 from Serratia liquefaciens. J Bacteriol170:5855–5862
    [Google Scholar]
  12. Givskov M., Eberl L., Christiansen G., Benedik M. J., Molin S.. 1995; Induction of phospholipase- and flagellar synthesis in Serratia liquefaciens is controlled by expression of the flagellar master operon flhD. . Mol Microbiol15:445–454[CrossRef]
    [Google Scholar]
  13. Givskov M., de Nys R., Manefield M., Gram L., Maximilien R., Eberl L., Molin S., Steinberg P., Kjelleberg S.. 1996; Eukaryotic interference with homoserine lactone mediated prokaryotic signaling. J Bacteriol178:6618–6622
    [Google Scholar]
  14. Givskov M., Eberl L., Molin S.. 1997; Control of exoenzyme production, motility and cell differentiation in Serratia liquefaciens. . FEMS Microbiol Lett148:115–122[CrossRef]
    [Google Scholar]
  15. Givskov M., Östling J., Lindum P. W., Eberl L., Christiansen G., Molin S., Kjelleberg S.. 1998; The participation of two separate regulatory systems in controlling swarming motility of Serratia liquefaciens. J Bacteriol180:742–745
    [Google Scholar]
  16. Gram L., de Nys R., Maximilien R., Givskov M., Steinberg P., Kjelleberg S.. 1996; Inhibitory effects of secondary metabolites from the red alga Delisea pulchra on swarming motility of Proteus mirabilis. Appl Environ Microbiol62:4284–4287
    [Google Scholar]
  17. Gram L., Christensen A. B., Ravn L., Molin S., Givskov M.. 1999; Production of acetylated homoserine lactones by psychrophilic members of the Enterobacteriaceae isolated from foods. Appl Environ Microbiol65:3458–3463
    [Google Scholar]
  18. Hardman A. M., Stewart G. S. A. B., Williams P.. 1998; Quorum sensing and the cell-cell communication dependent regulation of gene expression in pathogenic and non-pathogenic bacteria. Antonie Leeuwenhoek74:199–210[CrossRef]
    [Google Scholar]
  19. Hassett D. J., Ma J., Elkins J. G..10 other authors 1999; Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol34:1082–1093[CrossRef]
    [Google Scholar]
  20. Kjelleberg S., Steinberg P. D., Givskov M., Manefield M., de Nys R.. 1997; Do marine products interfere with procaryotic AHL regulatory systems?. Aquat Microbiol Ecol13:85–93[CrossRef]
    [Google Scholar]
  21. Koch C., Høiby N.. 1993; Pathogenesis of cystic fibrosis. Lancet341:1065–1069[CrossRef]
    [Google Scholar]
  22. Lindum P. W., Anthoni U., Christoffersen C., Eberl L., Molin S., Givskov M.. 1998; -acyl-l-homoserine lactone autoinducers control production of an extracellular surface active lipopeptide required for swarming motility of Serratia liquefaciens MG1. J Bacteriol180:6384–6388
    [Google Scholar]
  23. McKenney D., Brown K., Allison D. G.. 1995; Influence of Pseudomonas aeruginosa exoproducts on virulence factor production in Burkholderia cepacia: evidence of interspecies communication. J Bacteriol177:6989–6992
    [Google Scholar]
  24. Manefield M., de Nys R., Kumar N., Read R., Givskov M., Steinberg P., Kjelleberg S.. 1999; Evidence that halogenated furanones from Delisea pulchra inhibit acylated homoserine lactone (AHL)-mediated gene expression by displacing the AHL signal from its receptor protein. Microbiology145:283–292[CrossRef]
    [Google Scholar]
  25. Pearson J. P., Gray K. M., Passador L., Tucker K. D., Eberhard A., Iglewski B. H., Greenberg E. P.. 1994; Structure of the autoinducer required for the expression of Pseudomonas aeruginosa virulence genes. Proc Natl Acad Sci USA91:197–201[CrossRef]
    [Google Scholar]
  26. Pearson J. P., Pesci E. C., Iglewski B. H.. 1997; Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. . J Bacteriol179:5756–5767
    [Google Scholar]
  27. Shapiro J. A.. 1998; Thinking about bacterial populations as multicellular organisms. Annu Rev Microbiol52:81–104[CrossRef]
    [Google Scholar]
  28. Swift S., Karlyshev A., Fish L., Durant E., Winson M., Chhabra S., Williams P., Macintyre S., Stewart G.. 1997; Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J Bacteriol179:5271–5281
    [Google Scholar]
  29. Swift S., Williams P., Stewart G. S. A. B.. 1999; -acylhomoserine lactones and quorum sensing in proteobacteria. In Cell–Cell Signaling in Bacteria pp.291–313Edited by Dunny G. M. , Winans S. C.. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  30. Telford G., Wheeler D., Williams P., Tomkins P. T., Appleby P., Sewell H., Stewart G. S. A. B., Bycroft B. W., Pritchard D. I.. 1998; The Pseudomonas aeruginosa quorum-sensing signal molecule N-(3-oxododecanoyl)-l-homoserine lactone has immunomodulatory activity. Infect Immun66:36–42
    [Google Scholar]
  31. Tolker-Nielsen T., Christensen A. B., Eberl L., Rasmussen T. B., Sternberg C., Molin S., Givskov M.. 2000; Assessment of flhDC mRNA levels in individual Serratia liquefaciens swarm cells. J Bacteriol182:2680–2686[CrossRef]
    [Google Scholar]
  32. Winson M., Camara M., Latifi A..10 other authors 1995; Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in. Pseudomonas aeruginosa. Proc Natl Acad Sci USA92:9427–9431[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-146-12-3237
Loading
/content/journal/micro/10.1099/00221287-146-12-3237
Loading

Data & Media loading...

Most cited this month

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