1. Computational and Systems Biology
  2. Microbiology and Infectious Disease

Multiple sources of slow activity fluctuations in a bacterial chemosensory network

  1. Remy Colin  Is a corresponding author
  2. Christelle Rosazza
  3. Ady Vaknin
  4. Victor Sourjik  Is a corresponding author
  1. Max Planck Institute for Terrestrial Microbiology, Germany
  2. The Hebrew University, Israel
https://doi.org/10.7554/eLife.26796
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  1. Remy Colin
  2. Christelle Rosazza
  3. Ady Vaknin
  4. Victor Sourjik
(2017)
Multiple sources of slow activity fluctuations in a bacterial chemosensory network
eLife 6:e26796.
https://doi.org/10.7554/eLife.26796
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Abstract

Cellular networks are intrinsically subject to stochastic fluctuations, but analysis of the resulting noise remained largely limited to gene expression. The pathway controlling chemotaxis of Escherichia coli provides one example where posttranslational signaling noise has been deduced from cellular behavior. This noise was proposed to result from stochasticity in chemoreceptor methylation, and it is believed to enhance environment exploration by bacteria. Here we combined single-cell FRET measurements with analysis based on the fluctuation-dissipation theorem (FDT) to characterize origins of activity fluctuations within the chemotaxis pathway. We observed surprisingly large methylation-independent thermal fluctuations of receptor activity, which contribute to noise comparably to the energy-consuming methylation dynamics. Interactions between clustered receptors involved in amplification of chemotactic signals are also necessary to produce the observed large activity fluctuations. Our work thus shows that the high response sensitivity of this cellular pathway also increases its susceptibility to noise, from thermal and out-of-equilibrium processes.

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Author details

  1. Remy Colin

    Department of Systems and Synthetic Microbiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    For correspondence
    remy.colin@synmikro.mpi-marburg.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9051-8003

  2. Christelle Rosazza

    Department of Systems and Synthetic Microbiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.

  3. Ady Vaknin

    The Racah Institute of Physics, The Hebrew University, Jerusalem, Israel
    Competing interests
    The authors declare that no competing interests exist.

  4. Victor Sourjik

    Department of Systems and Synthetic Microbiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    For correspondence
    victor.sourjik@synmikro.mpi-marburg.mpg.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1053-9192

Funding

European Research Council (294761-MicRobE)

  • Remy Colin
  • Christelle Rosazza
  • Victor Sourjik

German-Israeli Project Cooperation (SO568/1-1)

  • Remy Colin
  • Christelle Rosazza
  • Victor Sourjik

German-Israeli Project Cooperation (AM441/1-1)

  • Ady Vaknin

Max-Planck-Institut für Terrestrische Mikrobiologie (Open-access funding)

  • Remy Colin

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2017, Colin et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Remy Colin
  2. Christelle Rosazza
  3. Ady Vaknin
  4. Victor Sourjik
(2017)
Multiple sources of slow activity fluctuations in a bacterial chemosensory network
eLife 6:e26796.
https://doi.org/10.7554/eLife.26796

Share this article

https://doi.org/10.7554/eLife.26796

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Further reading

    1. Computational and Systems Biology

    Phenotypic diversity and temporal variability in a bacterial signaling network revealed by single-cell FRET

    Johannes M Keegstra, Keita Kamino ... Thomas S Shimizu
    Research Article Updated

    We present in vivo single-cell FRET measurements in the Escherichia coli chemotaxis system that reveal pervasive signaling variability, both across cells in isogenic populations and within individual cells over time. We quantify cell-to-cell variability of adaptation, ligand response, as well as steady-state output level, and analyze the role of network design in shaping this diversity from gene expression noise. In the absence of changes in gene expression, we find that single cells demonstrate strong temporal fluctuations. We provide evidence that such signaling noise can arise from at least two sources: (i) stochastic activities of adaptation enzymes, and (ii) receptor-kinase dynamics in the absence of adaptation. We demonstrate that under certain conditions, (ii) can generate giant fluctuations that drive signaling activity of the entire cell into a stochastic two-state switching regime. Our findings underscore the importance of molecular noise, arising not only in gene expression but also in protein networks.