Log in

Variation of swimming speed enhances the chemotactic migration of Escherichia coli

  • Research Article
  • Published:
Systems and Synthetic Biology

Abstract

Studies on chemotaxis of Escherichia coli have shown that modulation of tumble frequency causes a net drift up the gradient of attractants. Recently, it has been demonstrated that the bacteria is also capable of varying its runs speed in uniform concentration of attractant. In this study, we investigate the role of swimming speed on the chemotactic migration of bacteria. To this end, cells are exposed to gradients of a non-metabolizable analogue of glucose which are sensed via the Trg sensor. When exposed to a gradient, the cells modulate their tumble duration, which is accompanied with variation in swimming speed leading to drift velocities that are much higher than those achieved through the modulation of the tumble duration alone. We use an existing intra-cellular model developed for the Tar receptor and incorporate the variation of the swimming speed along with modulation of tumble frequency to predict drift velocities close to the measured values. The main implication of our study is that E. coli not only modulates the tumble frequency, but may also vary the swimming speed to affect chemotaxis and thereby efficiently sample its nutritionally rich environment.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adler J (1966) Chemotaxis in bacteria. Science 153:708–716

    Article  CAS  PubMed  Google Scholar 

  • Adler J, Epstein W (1974) Phosphotransferase-system enzymes as chemoreceptors for certain sugars in Escherichia coli chemotaxis. Proc Natl Acad Sci USA 71:2895–2899

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Adler J, Hazelbauer G, Dahl M (1973) Chemotaxis toward sugars in Escherichia coli. J Bacteriol 115:824–847

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ahmed T, Stocker R (2008) Experimental verification of the behavioral foundation of bacterial transport parameters using microfluidics. Biophys J 95(9):4481–93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Alon U, Camarena L, Surette MG, y Arcas BA, Liu Y, Leibler S, Stock JB (1998) Response regulator output in bacterial chemotaxis. EMBO J 17:4238–4248

    Article  PubMed Central  PubMed  Google Scholar 

  • Barkai N, Leibler S (1997) Robustness in simple bionetworks. Nature 387:913–917

    Article  CAS  PubMed  Google Scholar 

  • Berg H, Brown D (1972) Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature 239:502–507

    Article  Google Scholar 

  • Berg HC (2000) Random walks in biology. Princeton University Press, Princeton

    Google Scholar 

  • Berg HC (2004) E. coli in motion. Springer, New York

    Book  Google Scholar 

  • Boehm A, Kaiser M, Li H, Spangler C, Kasper C, Ackermann M, Kaever V, Sourjik V, Roth V, Jenal U (2010) Second messenger mediated adjustment of bacterial swimming velocity. Cell 141:107–116

    Article  CAS  PubMed  Google Scholar 

  • Deepika D, Karmakar R, Tirumkudulu MS, Venkatesh KV (2015) Variation in swimming speed of Escherichia coli in response to attractant. Arch Microbiol 197(2):211–222

  • Demir M, Salman H (2012) Bacterial thermotaxis by speed modulation. Biophys J 103:1683–1690

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eisenbach M (2004) Chemotaxis. Imperial college press, London

    Book  Google Scholar 

  • Eisenbach M, Wolf A, Welch M, Caplan S, Lapidus I, Macnab R, Aloni H, Asher O (1990) Pausing, switching and speed fluctuation of the bacterial flagellar motor and their relation to motility and chemotaxis. J Mol Biol 211:551–563

    Article  CAS  PubMed  Google Scholar 

  • Feng X, Lilly A, Hazelbauer G (1999) Enhanced function conferred on low-abundance chemoreceptor trg by a methyltransferase-docking site. J Bacteriol 181:3164–3171

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hayashi K, Morooka N, Yamamoto Y, Fujita K, Isono K, Choi S, Ohtsubo E, Baba T, Wanner BL, Mori H, Horiuchi T (2006) Highly accurate genome sequences of Escherichia coli k-12 strains mg1655 and w3110. Mol Syst Biol 2:2006.2007:1–5

  • Hazelbauer G, Engstrom P (1980) Parallel pathways for transduction of chemotactic signals in Escherichia coli. Nature 283:98–100

    Article  CAS  PubMed  Google Scholar 

  • Li M, Hazelbauer G (2005) Adaptational assistance in clusters of bacterial chemoreceptors. Mol Microbiol 56:1617–1626

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Papadopoulos K (1995) Unidirectional motility of Escherichia coli in restrictive capillaries. Appl Environ Microbiol 61(10):3567–3572

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Z, Papadopoulos K (1996) A method for measuring bacterial chemotaxis parameters in a microcapillary. Biotechnol Bioeng 51(1):120–125

    Article  CAS  PubMed  Google Scholar 

  • Lux R, Jahreis K, Bettenbrock K, Parkinson JS, Lengeler JW (1995) Coupling the phosphotransferase system and the methyl-accepting chemotaxis protein-dependent chemotaxis signaling pathways of Escherichia coli. Proc Natl Acad Sci USA 92:11583–11587

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Macnab R, Koshland D (1972) The gradient-sensing mechanism in bacterial chemotaxis. Proc Natl Acad Sci USA 69:2509–2512

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Masson JB, Voisinne G, Wong-Nga J, Celania A, Vergassola M (2012) Noninvasive inference of the molecular chemotactic response using bacterial trajectories. Proc Natl Acad Sci USA 109:1802–1807

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mesibov R, Ordal W, Adler J (1973) The range of attractant concentrations for bacterial chemotaxis and the threshold and the size of response aver this range. J Gen Physiol 62:203–223

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Neumann S, Grosse K, Sourjik V (2012) Chemotactic signaling via carbohydrate phosphotransferase systems in Escherichia coli. Proc Natl Acad Sci USA 109:12159–12164

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rivero M, Tranquillo R, Buettner H, Lauffenburger D (1989) Transport models for chemotactic cellpopulations based on individual cell behaviour. Chem Eng Sci 44(12):2881–2897

    Article  Google Scholar 

  • Saragosti J, Calvez V, Bournaveas N, Perthame B, Buguin A, Silberzan P (2011) Directional persistence of chemotactic bacteria in a traveling concentration wave. Proc Natl Acad Sci USA 108:16235–16240

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Subramanian G, Koch DL (2009) Critical bacterial concentration for the onset of collective swimming. J Fluid Mech 632:359–400

    Article  Google Scholar 

  • Vuppala RV, Tirumkudulu MS, Venkatesh KV (2010a) Chemotaxis of Escherichia coli to l-serine. Phys Biol 7(026):007

    Google Scholar 

  • Vuppala RV, Tirumkudulu MS, Venkatesh KV (2010b) Mathematical modeling and experimental validation of chemotaxis under controlled gradients of methyl-aspartate in Escherichia coli. Mol Biosyst 6:1082–1092

    Article  Google Scholar 

  • Wadhams G, Armitage J (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1024–1037

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors acknowledge financial support from the Department of Science and Technology, India. MST also acknowledges support from the Swaranajayanti Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. V. Venkatesh.

Additional information

R. V. S. Uday Bhaskar and Richa Karmakar have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (pdf 563 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Uday Bhaskar, R.V.S., Karmakar, R., Deepika, D. et al. Variation of swimming speed enhances the chemotactic migration of Escherichia coli . Syst Synth Biol 9, 85–95 (2015). https://doi.org/10.1007/s11693-015-9174-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11693-015-9174-x

Keywords

Navigation