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Design of a MAPK signalling cascade balances energetic cost versus accuracy of information transmission

Author

Listed:
  • Alexander Anders

    (Max Planck Institute for Terrestrial Microbiology
    LOEWE Center for Synthetic Microbiology (SYNMIKRO))

  • Bhaswar Ghosh

    (Max Planck Institute for Terrestrial Microbiology
    LOEWE Center for Synthetic Microbiology (SYNMIKRO)
    International Institute of Information Technology)

  • Timo Glatter

    (Max Planck Institute for Terrestrial Microbiology)

  • Victor Sourjik

    (Max Planck Institute for Terrestrial Microbiology
    LOEWE Center for Synthetic Microbiology (SYNMIKRO))

Abstract

Cellular processes are inherently noisy, and the selection for accurate responses in presence of noise has likely shaped signalling networks. Here, we investigate the trade-off between accuracy of information transmission and its energetic cost for a mitogen-activated protein kinase (MAPK) signalling cascade. Our analysis of the pheromone response pathway of budding yeast suggests that dose-dependent induction of the negative transcriptional feedbacks in this network maximizes the information per unit energetic cost, rather than the information transmission capacity itself. We further demonstrate that futile cycling of MAPK phosphorylation and dephosphorylation has a measurable effect on growth fitness, with energy dissipation within the signalling cascade thus likely being subject to evolutionary selection. Considering optimization of accuracy versus the energetic cost of information processing, a concept well established in physics and engineering, may thus offer a general framework to understand the regulatory design of cellular signalling systems.

Suggested Citation

  • Alexander Anders & Bhaswar Ghosh & Timo Glatter & Victor Sourjik, 2020. "Design of a MAPK signalling cascade balances energetic cost versus accuracy of information transmission," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17276-4
    DOI: 10.1038/s41467-020-17276-4
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    References listed on IDEAS

    as
    1. Ingmar Kanitscheider & Ruben Coen-Cagli & Adam Kohn & Alexandre Pouget, 2015. "Measuring Fisher Information Accurately in Correlated Neural Populations," PLOS Computational Biology, Public Library of Science, vol. 11(6), pages 1-27, June.
    2. Alvaro Banderas & Mihaly Koltai & Alexander Anders & Victor Sourjik, 2016. "Sensory input attenuation allows predictive sexual response in yeast," Nature Communications, Nature, vol. 7(1), pages 1-9, November.
    3. Attila Becskei & Luis Serrano, 2000. "Engineering stability in gene networks by autoregulation," Nature, Nature, vol. 405(6786), pages 590-593, June.
    4. Mohan K. Malleshaiah & Vahid Shahrezaei & Peter S. Swain & Stephen W. Michnick, 2010. "The scaffold protein Ste5 directly controls a switch-like mating decision in yeast," Nature, Nature, vol. 465(7294), pages 101-105, May.
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