Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

Escherichia coli swim on the right-hand side

Abstract

The motion of peritrichously flagellated bacteria close to surfaces is relevant to understanding the early stages of biofilm formation and of pathogenic infection1,2,3,4. This motion differs from the random-walk trajectories5 of cells in free solution. Individual Escherichia coli cells swim in clockwise, circular trajectories near planar glass surfaces6,7. On a semi-solid agar substrate, cells differentiate into an elongated, hyperflagellated phenotype and migrate cooperatively over the surface8, a phenomenon called swarming. We have developed a technique for observing isolated E. coli swarmer cells9 moving on an agar substrate and confined in shallow, oxidized poly(dimethylsiloxane) (PDMS) microchannels. Here we show that cells in these microchannels preferentially ‘drive on the right’, swimming preferentially along the right wall of the microchannel (viewed from behind the moving cell, with the agar on the bottom). We propose that when cells are confined between two interfaces—one an agar gel and the second PDMS—they swim closer to the agar surface than to the PDMS surface (and for much longer periods of time), leading to the preferential movement on the right of the microchannel. Thus, the choice of materials guides the motion of cells in microchannels.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Cells swim in clockwise, circular trajectories at solid, planar surfaces.
Figure 2: Images of cells in composite agar/ox-PDMS microchannels.
Figure 3: Quantification of cells displaying a preference to travel to the right by using a microchannel junction.
Figure 4: Preference of cells to move on the right in microchannels as a function of the height of the channel.

References

  1. 1

    Pratt, L. A. & Kolter, R. Genetic analysis of Escherichia coli biofilm formation: Roles of flagella, motility, chemotaxis and type I pili. Mol. Microbiol. 30, 285–293 (1998)

    CAS  Article  PubMed  Google Scholar 

  2. 2

    Harshey, R. M. Bacterial motility on a surface: Many ways to a common goal. Annu. Rev. Microbiol. 57, 249–273 (2003)

    CAS  Article  PubMed  Google Scholar 

  3. 3

    Ottemann, K. M. & Miller, J. F. Roles for motility in bacterial–host interactions. Mol. Microbiol. 24, 1109–1117 (1997)

    CAS  Article  PubMed  Google Scholar 

  4. 4

    Vigeant, M. A. S., Ford, R. M., Wagner, M. & Tamm, L. K. Reversible and irreversible adhesion of motile Escherichia coli cells analyzed by total internal reflection aqueous fluorescence microscopy. Appl. Environ. Microbiol. 68, 2794–2801 (2002)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. 5

    Berg, H. C. & Brown, D. A. Chemotaxis in Escherichia coli analyzed by three-dimensional tracking. Nature 239, 500–504 (1972)

    ADS  CAS  Article  Google Scholar 

  6. 6

    Berg, H. C. & Turner, L. Chemotaxis of bacteria in glass-capillary arrays. Biophys. J. 58, 919–930 (1990)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7

    Frymier, P. D., Ford, R. M., Berg, H. C. & Cummings, P. T. Three-dimensional tracking of motile bacteria near a solid planar surface. Proc. Natl Acad. Sci. USA 92, 6195–6199 (1995)

    ADS  CAS  Article  PubMed  Google Scholar 

  8. 8

    Henrichsen, J. Bacterial surface translocation: A survey and classification. Bacteriol. Rev. 36, 478–503 (1972)

    CAS  PubMed  PubMed Central  Google Scholar 

  9. 9

    Harshey, R. M. & Matsuyama, T. Dimorphic transition in Escherichia coli and Salmonella typhimurium—surface-induced differentiation into hyperflagellate swarmer cells. Proc. Natl Acad. Sci. USA 91, 8631–8635 (1994)

    ADS  CAS  Article  PubMed  Google Scholar 

  10. 10

    Berg, H. C. & Anderson, R. A. Bacteria swim by rotating their flagellar filaments. Nature 245, 380–382 (1973)

    ADS  CAS  Article  PubMed  Google Scholar 

  11. 11

    Berg, H. C. The rotary motor of bacterial flagella. Annu. Rev. Biochem. 72, 19–54 (2003)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12

    Turner, L., Ryu, W. S. & Berg, H. C. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182, 2793–2801 (2000)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. 13

    Taylor, G. The action of waving cylindrical tails in propelling microscopic organisms. Proc. R. Soc. Lond. A 211, 225–239 (1952)

    ADS  MathSciNet  Article  Google Scholar 

  14. 14

    Ramia, M., Tullock, D. L. & Phan-Thien, N. The role of hydrodynamic interaction in the locomotion of microorganisms. Biophys. J. 65, 755–778 (1993)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. 15

    Vigeant, M. A. S. & Ford, R. M. Interactions between motile Escherichia coli and glass in media with various ionic strengths, as observed with a three- dimensional-tracking microscope. Appl. Environ. Microbiol. 63, 3474–3479 (1997)

    CAS  PubMed  PubMed Central  Google Scholar 

  16. 16

    Xia, Y. & Whitesides, G. M. Soft lithography. Angew. Chem. Int. Edn Engl. 37, 550–575 (1998)

    CAS  Article  Google Scholar 

  17. 17

    Brandrup, J., Immergut, E. H. & Grulke, E. A. (eds) Polymer Handbook, 4th edn (Wiley, New York, 1999)

  18. 18

    Toguchi, A., Siano, M., Burkart, M. & Harshey, R. M. Genetics of swarming motility in Salmonella enterica Serovar Typhimurium: Critical role for lipopolysaccharide. J. Bacteriol. 182, 6308–6321 (2000)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. 19

    Frymier, P. D. & Ford, R. M. Analysis of bacterial swimming speed approaching a solid–liquid interface. AIChE J. 43, 1341–1347 (1997)

    CAS  Article  Google Scholar 

  20. 20

    Biondi, S. A., Quinn, J. A. & Goldfine, H. Random motility of swimming bacteria in restricted geometries. AIChE J. 44, 1923–1929 (1998)

    CAS  Article  Google Scholar 

  21. 21

    Pernodet, N., Maaloum, M. & Tinland, B. Pore size of agarose gels by atomic force microscopy. Electrophoresis 18, 55–58 (1997)

    CAS  Article  PubMed  Google Scholar 

  22. 22

    Damiano, E. R., Long, D. S., El-Khatib, F. H. & Stace, T. M. On the motion of a sphere in a Stokes flow parallel to a Brinkman half-space. J. Fluid Mech. 500, 75–101 (2004)

    ADS  MathSciNet  Article  Google Scholar 

  23. 23

    Allison, C., Lai, H. C. & Hughes, C. Coordinate expression of virulence genes during swarm-cell differentiation and population migration of Proteus mirabilis. Mol. Microbiol. 6, 1583–1591 (1992)

    CAS  Article  PubMed  Google Scholar 

  24. 24

    Visick, K. L. & McFall-Ngai, M. J. An exclusive contract: Specificity in the Vibrio fischeri Euprymna scolopes partnership. J. Bacteriol. 182, 1779–1787 (2000)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25

    Darnton, N., Turner, L., Breuer, K. & Berg, H. C. Moving fluid with bacterial carpets. Biophys. J. 86, 1863–1870 (2004)

    ADS  CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26

    Armstrong, J. B., Adler, J. & Dahl, M. M. Nonchemotactic mutants of Escherichia coli. J. Bacteriol. 93, 390–398 (1967)

    CAS  PubMed  PubMed Central  Google Scholar 

  27. 27

    Wolfe, A. J., Conley, M. P., Kramer, T. J. & Berg, H. C. Reconstitution of signalling in bacterial chemotaxis. J. Bacteriol. 169, 1878–1885 (1987)

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  28. 28

    Parkinson, J. S. Complementation analysis and deletion mapping of Escherichia coli mutants defective in chemotaxis. J. Bacteriol. 135, 45–53 (1978)

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank W. S. Ryu, D. Ryan, M. P. Brenner and H. A. Stone for discussions, and S. Rojevskaya for technical assistance. This research was supported by the NIH and DOE. W.R.D. acknowledges an NSF-IGERT Biomechanics Training Grant. M.M. acknowledges a postdoctoral fellowship from the Swiss National Science Foundation. P.G. thanks the Foundation for Polish Science for a postdoctoral fellowship. D.B.W. thanks the NIH for a postdoctoral fellowship.

Author information

Affiliations

Authors

Corresponding author

Correspondence to George M. Whitesides.

Ethics declarations

Competing interests

Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Data

Results from experiments where the surfactant and ionic strength of the motility agar was varied, presented in Supplementary Table S1, and histograms of the lengths and speeds of cells traveling along the right and left channel wall. (DOC 311 kb)

Supplementary Methods

Methods used to grow swarmer cells, the preparation of PDMS films, image acquisition and data analysis, the fabrication of silicon masters, and the preparation of GFP-cells. (DOC 29 kb)

Supplementary Video S1

Real-time movement to the right of E. coli swarmer cells (AW405) in composite agar/PDMS microchannels that are 10 m wide and 1.4 µm tall. Nutrient agar forms the floor of the channel and a patterned PDMS film forms the sidewalls and ceiling. (MPG 975 kb)

Supplementary Video S2

Real-time movement to the right of E. coli swarmer cells (AW405) in composite agar/PDMS microchannels that are 3 m wide and 1.4 µm tall. Nutrient agar forms the floor of the channel and a patterned PDMS film forms the sidewalls and ceiling. (MPG 808 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

DiLuzio, W., Turner, L., Mayer, M. et al. Escherichia coli swim on the right-hand side. Nature 435, 1271–1274 (2005). https://doi.org/10.1038/nature03660

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing