Advertisement

Journal of Biological Physics

, Volume 36, Issue 3, pp 317–327 | Cite as

Bacterium in a box: sensing of quorum and environment by the LuxI/LuxR gene regulatory circuit

  • Stephen J. HagenEmail author
  • Minjun Son
  • Joel T. Weiss
  • Jonathan H. Young
Original Paper

Abstract

The chemical signaling mechanism known as “bacterial quorum sensing” (QS) is normally interpreted as allowing bacteria to detect their own population density, in order to coordinate gene expression across a colony. However, the release of the chemical signal can also be interpreted as a means for one or a few cells to probe the local physical properties of their microenvironment. We have studied the behavior of the LuxI/LuxR QS circuit of Vibrio fischeri in tightly confining environments where individual cells detect their own released signals. We find that the lux genes become activated in these environments, although the activation onset time shows substantial cell-to-cell variability and little sensitivity to the confining volume. Our data suggest that noise in gene expression could significantly impact the utility of LuxI/LuxR as a probe of the local physical environment.

Keywords

Quorum sensing Noise Microenvironments Fluorescence GFP Diffusion Bacteria LuxIR Stochastic Bioluminescence Autoinduction Vibrio fischeri 

Notes

Acknowledgements

The authors thank Drs. Mark Mandel, Ned Ruby, Rena Hill, and Christopher Voigt for providing bacterial strains used in this study. The authors also gratefully acknowledge funding support from the National Science Foundation MCB no. 0347124 and the National Institutes of Health NIDCR 1R21DE018826.

References

  1. 1.
    Waters, C.M., Bassler, B.L.: Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319–346 (2005)CrossRefGoogle Scholar
  2. 2.
    Boyer, M., Wisniewski-Dye, F.: Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol. Ecol. 70, 1–19 (2009)CrossRefGoogle Scholar
  3. 3.
    Dunn, A.K., Stabb, E.V.: Beyond quorum sensing: the complexities of prokaryotic parliamentary procedures. Anal. Bioanal. Chem. 387, 391–398 (2007)CrossRefGoogle Scholar
  4. 4.
    Hense, B.A., Kuttler, C., Mueller, J., Rothballer, M., Hartmann, A., Kreft, J.: Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5, 230–239 (2007)CrossRefGoogle Scholar
  5. 5.
    Redfield, R.J.: Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365–370 (2002)CrossRefGoogle Scholar
  6. 6.
    Dunlap, P.V.: Quorum regulation of luminescence in Vibrio fischeri. J. Mol. Microbiol. Biotechnol. 1, 5–12 (1999)Google Scholar
  7. 7.
    Lupp, C., Urbanowski, M., Greenberg, E.P., Ruby, E.G.: The Vibrio fischeri quorum-sensing systems ain and lux sequentially induce luminescence gene expression and are important for persistence in the squid host. Mol. Microbiol. 50, 319–331 (2003)CrossRefGoogle Scholar
  8. 8.
    You, L.C., Cox, R.S., Weiss, R., Arnold, F.H.: Programmed population control by cell-cell communication and regulated killing. Nature 428, 868–871 (2004)CrossRefADSGoogle Scholar
  9. 9.
    March, J.C., Bentley, W.E.: Quorum sensing and bacterial cross-talk in biotechnology. Curr. Opin. Biotechnol. 15, 495–502 (2004)CrossRefGoogle Scholar
  10. 10.
    James, S., Nilsson, P., James, G., Kjelleberg, S., Fagerstrom, T.: Luminescence control in the marine bacterium Vibrio fischeri: an analysis of the dynamics of lux regulation. J. Mol. Biol. 296, 1127–1137 (2000)CrossRefGoogle Scholar
  11. 11.
    Zhou, T.S., Chen, L.N., Aihara, K.: Molecular communication through stochastic synchronization induced by extracellular fluctuations. Phys. Rev. Lett. 95, 178103 (2005)CrossRefADSGoogle Scholar
  12. 12.
    Cox, C.D., Peterson, G.D., Allen, M.S., Lancaster, J.M., McCollum, J.M., Austin, D., Yan, L., Sayler, G.S., Simpson, M.L.: Analysis of noise in quorum sensing. OMICS: A J. Integr. Biol. 7, 317–334 (2003)CrossRefGoogle Scholar
  13. 13.
    Sia, S.K., Whitesides, G.M.: Microfluidic devices fabricated in poly(dimethylsiloxane) for biological studies. Electrophoresis 24, 3563–3576 (2003)CrossRefGoogle Scholar
  14. 14.
    Eberhard, A.: Inhibition and activation of bacterial luciferase synthesis. J. Bacteriol. 109, 1101 (1972)Google Scholar
  15. 15.
    Anderson, J.C., Clarke, E.J., Arkin, A.P., Voigt, C.A.: Environmentally controlled invasion of cancer cells by engineered bacteria. J. Mol. Biol. 355, 619–627 (2006)CrossRefGoogle Scholar
  16. 16.
    Boedicker, J.Q., Vincent, M.E., Ismagilov, R.F.: Microfluidic confinement of single cells of bacteria in small volumes initiates high-density behavior of quorum sensing and growth and reveals its variability. Angew. Chem. Int. Ed. 48, 5908–5911 (2009)CrossRefGoogle Scholar
  17. 17.
    Carnes, E.C., Lopez, D.M., Donegan, N.P., Cheung, A., Gresham, H., Timmins, G.S., Brinker, C.J.: Confinement-induced quorum sensing of individual Staphylococcus aureus bacteria. Nat. Chem. Biol. 6, 41–45 (2010)CrossRefGoogle Scholar
  18. 18.
    Schaefer, A.L., Val, D.L., Hanzelka, B.L., Cronan, J.E., Greenberg, E.P.: Generation of cell-to-cell signals in quorum sensing: Acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Natl. Acad. Sci. U. S. A. 93, 9505–9509 (1996)CrossRefADSGoogle Scholar
  19. 19.
    Kubitschek, H.E., Friske, J.A.: Determination of bacterial cell volume with the Coulter Counter. J. Bacteriol. 168, 1466–1467 (1986)Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Stephen J. Hagen
    • 1
    Email author
  • Minjun Son
    • 1
  • Joel T. Weiss
    • 1
  • Jonathan H. Young
    • 1
  1. 1.Physics DepartmentUniversity of FloridaGainesvilleUSA

Personalised recommendations