Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Biological Physics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Waters, C.M., Bassler, B.L.: Quorum sensing: cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol. 21, 319–346 (2005)

    Article  Google Scholar 

  2. Boyer, M., Wisniewski-Dye, F.: Cell-cell signalling in bacteria: not simply a matter of quorum. FEMS Microbiol. Ecol. 70, 1–19 (2009)

    Article  Google Scholar 

  3. Dunn, A.K., Stabb, E.V.: Beyond quorum sensing: the complexities of prokaryotic parliamentary procedures. Anal. Bioanal. Chem. 387, 391–398 (2007)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  5. Redfield, R.J.: Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365–370 (2002)

    Article  Google Scholar 

  6. Dunlap, P.V.: Quorum regulation of luminescence in Vibrio fischeri. J. Mol. Microbiol. Biotechnol. 1, 5–12 (1999)

    Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  ADS  Google Scholar 

  9. March, J.C., Bentley, W.E.: Quorum sensing and bacterial cross-talk in biotechnology. Curr. Opin. Biotechnol. 15, 495–502 (2004)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  11. Zhou, T.S., Chen, L.N., Aihara, K.: Molecular communication through stochastic synchronization induced by extracellular fluctuations. Phys. Rev. Lett. 95, 178103 (2005)

    Article  ADS  Google Scholar 

  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)

    Article  Google Scholar 

  13. Sia, S.K., Whitesides, G.M.: Microfluidic devices fabricated in poly(dimethylsiloxane) for biological studies. Electrophoresis 24, 3563–3576 (2003)

    Article  Google Scholar 

  14. Eberhard, A.: Inhibition and activation of bacterial luciferase synthesis. J. Bacteriol. 109, 1101 (1972)

    Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  Google Scholar 

  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)

    Article  ADS  Google Scholar 

  19. Kubitschek, H.E., Friske, J.A.: Determination of bacterial cell volume with the Coulter Counter. J. Bacteriol. 168, 1466–1467 (1986)

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

  1. Physics Department, University of Florida, PO Box 118440, Gainesville, FL, 32611-8440, USA

    Stephen J. Hagen, Minjun Son, Joel T. Weiss & Jonathan H. Young

Authors
  1. Stephen J. Hagen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Minjun Son
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joel T. Weiss
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jonathan H. Young
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stephen J. Hagen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hagen, S.J., Son, M., Weiss, J.T. et al. Bacterium in a box: sensing of quorum and environment by the LuxI/LuxR gene regulatory circuit. J Biol Phys 36, 317–327 (2010). https://doi.org/10.1007/s10867-010-9186-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10867-010-9186-4

Keywords

Search

Navigation