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Macromolecular condensation buffers intracellular water potential

Author

Listed:
  • Joseph L. Watson

    (MRC Laboratory of Molecular Biology)

  • Estere Seinkmane

    (MRC Laboratory of Molecular Biology)

  • Christine T. Styles

    (Imperial College London)

  • Andrei Mihut

    (MRC Laboratory of Molecular Biology)

  • Lara K. Krüger

    (MRC Laboratory of Molecular Biology)

  • Kerrie E. McNally

    (MRC Laboratory of Molecular Biology)

  • Vicente Jose Planelles-Herrero

    (MRC Laboratory of Molecular Biology)

  • Michal Dudek

    (University of Manchester)

  • Patrick M. McCall

    (TU Dresden
    Max Planck Institute of Molecular Cell Biology and Genetics
    Max Planck Institute for the Physics of Complex Systems)

  • Silvia Barbiero

    (MRC Laboratory of Molecular Biology)

  • Michael Vanden Oever

    (Imperial College London)

  • Sew Yeu Peak-Chew

    (MRC Laboratory of Molecular Biology)

  • Benjamin T. Porebski

    (MRC Laboratory of Molecular Biology)

  • Aiwei Zeng

    (MRC Laboratory of Molecular Biology)

  • Nina M. Rzechorzek

    (MRC Laboratory of Molecular Biology)

  • David C. S. Wong

    (MRC Laboratory of Molecular Biology)

  • Andrew D. Beale

    (MRC Laboratory of Molecular Biology)

  • Alessandra Stangherlin

    (MRC Laboratory of Molecular Biology
    University of Cologne)

  • Margot Riggi

    (University of Utah)

  • Janet Iwasa

    (University of Utah)

  • Jörg Morf

    (Babraham Institute)

  • Christos Miliotis

    (Babraham Institute)

  • Alina Guna

    (California Institute of Technology)

  • Alison J. Inglis

    (California Institute of Technology)

  • Jan Brugués

    (TU Dresden
    Max Planck Institute of Molecular Cell Biology and Genetics
    Max Planck Institute for the Physics of Complex Systems)

  • Rebecca M. Voorhees

    (California Institute of Technology)

  • Joseph E. Chambers

    (Cambridge Institute for Medical Research)

  • Qing-Jun Meng

    (University of Manchester)

  • John S. O’Neill

    (MRC Laboratory of Molecular Biology)

  • Rachel S. Edgar

    (Imperial College London)

  • Emmanuel Derivery

    (MRC Laboratory of Molecular Biology)

Abstract

Optimum protein function and biochemical activity critically depends on water availability because solvent thermodynamics drive protein folding and macromolecular interactions1. Reciprocally, macromolecules restrict the movement of ‘structured’ water molecules within their hydration layers, reducing the available ‘free’ bulk solvent and therefore the total thermodynamic potential energy of water, or water potential. Here, within concentrated macromolecular solutions such as the cytosol, we found that modest changes in temperature greatly affect the water potential, and are counteracted by opposing changes in osmotic strength. This duality of temperature and osmotic strength enables simple manipulations of solvent thermodynamics to prevent cell death after extreme cold or heat shock. Physiologically, cells must sustain their activity against fluctuating temperature, pressure and osmotic strength, which impact water availability within seconds. Yet, established mechanisms of water homeostasis act over much slower timescales2,3; we therefore postulated the existence of a rapid compensatory response. We find that this function is performed by water potential-driven changes in macromolecular assembly, particularly biomolecular condensation of intrinsically disordered proteins. The formation and dissolution of biomolecular condensates liberates and captures free water, respectively, quickly counteracting thermal or osmotic perturbations of water potential, which is consequently robustly buffered in the cytoplasm. Our results indicate that biomolecular condensation constitutes an intrinsic biophysical feedback response that rapidly compensates for intracellular osmotic and thermal fluctuations. We suggest that preserving water availability within the concentrated cytosol is an overlooked evolutionary driver of protein (dis)order and function.

Suggested Citation

  • Joseph L. Watson & Estere Seinkmane & Christine T. Styles & Andrei Mihut & Lara K. Krüger & Kerrie E. McNally & Vicente Jose Planelles-Herrero & Michal Dudek & Patrick M. McCall & Silvia Barbiero & Mi, 2023. "Macromolecular condensation buffers intracellular water potential," Nature, Nature, vol. 623(7988), pages 842-852, November.
  • Handle: RePEc:nat:nature:v:623:y:2023:i:7988:d:10.1038_s41586-023-06626-z
    DOI: 10.1038/s41586-023-06626-z
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    Cited by:

    1. György Abrusán & Aleksej Zelezniak, 2024. "Cellular location shapes quaternary structure of enzymes," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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