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Interdependence of behavioural variability and response to small stimuli in bacteria

Nature volume 468, pages 819–823 (2010)Cite this article

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Abstract

The chemotaxis signalling network in Escherichia coli that controls the locomotion of bacteria is a classic model system for signal transduction1,2. This pathway modulates the behaviour of flagellar motors to propel bacteria towards sources of chemical attractants. Although this system relaxes to a steady state in response to environmental changes, the signalling events within the chemotaxis network are noisy and cause large temporal variations of the motor behaviour even in the absence of stimulus3. That the same signalling network governs both behavioural variability and cellular response raises the question of whether these two traits are independent. Here, we experimentally establish a fluctuation–response relationship in the chemotaxis system of living bacteria. Using this relationship, we demonstrate the possibility of inferring the cellular response from the behavioural variability measured before stimulus. In monitoring the pre- and post-stimulus switching behaviour of individual bacterial motors, we found that variability scales linearly with the response time for different functioning states of the cell. This study highlights that the fundamental relationship between fluctuation and response is not constrained to physical systems at thermodynamic equilibrium4 but is extensible to living cells5. Such a relationship not only implies that behavioural variability and cellular response can be coupled traits, but it also provides a general framework within which we can examine how the selection of a network design shapes this interdependence.

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Figure 1: CCW interval lengths pre- and post-stimulus.
Figure 2: Relationship between response to stimulus and fluctuations before stimulus.
Figure 3: Low-frequency noise in non-stimulated cells.
Figure 4: Relationship between signalling noise and response time to a small external stimulus.

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  • 09 December 2010

    The position of a sentence was changed in the first paragraph of the text.

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Acknowledgements

This research was funded by an NSF DMR award 0213745 to the Materials Research Science and Engineering Center at the University of Chicago, and NIH award R01AI059195-03 (to P.C.). W.P. and T.E. were supported by NSF CCF0829836, an Alfred P. Sloan Research Fellowship, and a National Academies Keck Futures Initiative award (to T.E.). J.F.M. was supported by NSF awards PHY-0852130 and DMR-0715099 and NIH grant 1U54CA143869-01. This work was also supported by the Chicago Biomedical Consortium with support from The Searle Funds at The Chicago Community Trust. D. Trentham supplied caged l-aspartate. We thank J. S. Parkinson for ΔCheB mutant strains RP4972 and RP4992. We thank T. Shimizu for discussions and sharing unpublished work. We thank H. Lee for help with the HPLC measurements. We thank J. Moffitt and K. Wood for comments on the manuscript and all members of the Cluzel laboratory for many discussions. W. Grus provided editorial assistance.

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Authors and Affiliations

  1. and The Department of Physics, The James Franck Institute, The Institute for Biophysical Dynamics, University of Chicago, Chicago, 60637, Illinois, USA

    Heungwon Park

  2. Department of Molecular, and Developmental Biology and Department of Physics, Cellular, Yale University, New Haven, 06520, Connecticut, USA

    William Pontius & Thierry Emonet

  3. Department of Molecular and Cellular Biology, FAS Center for Systems Biology, and School of Engineering and Applied Sciences, Harvard University, 52 Oxford Street, Cambridge, 02138, Massachusetts, USA

    Calin C. Guet & Philippe Cluzel

  4. Department of Molecular Biosciences and Department of Physics and Astronomy, Northwestern University, Evanston, 60208, Illinois, USA

    John F. Marko

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  1. Heungwon Park
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Contributions

P.C. conceived and designed the research. H.P. performed all the experiments. H.P., P.C., T.E., W.P. and J.F.M. analysed the data. H.P., P.C., J.F.M. and T.E. wrote the paper. C.C.G. constructed the pZE21-CheR plasmid.

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Correspondence to Philippe Cluzel.

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The authors declare no competing financial interests.

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Park, H., Pontius, W., Guet, C. et al. Interdependence of behavioural variability and response to small stimuli in bacteria. Nature 468, 819–823 (2010). https://doi.org/10.1038/nature09551

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