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Biomolecular condensates modulate membrane lipid packing and hydration

Author

Listed:
  • Agustín Mangiarotti

    (Science Park Golm)

  • Macarena Siri

    (Science Park Golm)

  • Nicky W. Tam

    (Science Park Golm)

  • Ziliang Zhao

    (Science Park Golm
    Leibniz Institute of Photonic Technology e.V.
    Friedrich-Schiller-University Jena)

  • Leonel Malacrida

    (Universidad de la República
    Institut Pasteur of Montevideo and Universidad de la República)

  • Rumiana Dimova

    (Science Park Golm)

Abstract

Membrane wetting by biomolecular condensates recently emerged as a key phenomenon in cell biology, playing an important role in a diverse range of processes across different organisms. However, an understanding of the molecular mechanisms behind condensate formation and interaction with lipid membranes is still missing. To study this, we exploited the properties of the dyes ACDAN and LAURDAN as nano-environmental sensors in combination with phasor analysis of hyperspectral and lifetime imaging microscopy. Using glycinin as a model condensate-forming protein and giant vesicles as model membranes, we obtained vital information on the process of condensate formation and membrane wetting. Our results reveal that glycinin condensates display differences in water dynamics when changing the salinity of the medium as a consequence of rearrangements in the secondary structure of the protein. Remarkably, analysis of membrane-condensates interaction with protein as well as polymer condensates indicated a correlation between increased wetting affinity and enhanced lipid packing. This is demonstrated by a decrease in the dipolar relaxation of water across all membrane-condensate systems, suggesting a general mechanism to tune membrane packing by condensate wetting.

Suggested Citation

  • Agustín Mangiarotti & Macarena Siri & Nicky W. Tam & Ziliang Zhao & Leonel Malacrida & Rumiana Dimova, 2023. "Biomolecular condensates modulate membrane lipid packing and hydration," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41709-5
    DOI: 10.1038/s41467-023-41709-5
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    References listed on IDEAS

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    1. Nadia A. Erkamp & Tomas Sneideris & Hannes Ausserwöger & Daoyuan Qian & Seema Qamar & Jonathon Nixon-Abell & Peter George-Hyslop & Jeremy D. Schmit & David A. Weitz & Tuomas P. J. Knowles, 2023. "Spatially non-uniform condensates emerge from dynamically arrested phase separation," Nature Communications, Nature, vol. 14(1), pages 1-8, December.
    2. Agustín Mangiarotti & Nannan Chen & Ziliang Zhao & Reinhard Lipowsky & Rumiana Dimova, 2023. "Wetting and complex remodeling of membranes by biomolecular condensates," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Anamika Avni & Ashish Joshi & Anuja Walimbe & Swastik G. Pattanashetty & Samrat Mukhopadhyay, 2022. "Single-droplet surface-enhanced Raman scattering decodes the molecular determinants of liquid-liquid phase separation," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Ibraheem Alshareedah & Mahdi Muhammad Moosa & Matthew Pham & Davit A. Potoyan & Priya R. Banerjee, 2021. "Programmable viscoelasticity in protein-RNA condensates with disordered sticker-spacer polypeptides," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    5. Bernardo Gouveia & Yoonji Kim & Joshua W. Shaevitz & Sabine Petry & Howard A. Stone & Clifford P. Brangwynne, 2022. "Capillary forces generated by biomolecular condensates," Nature, Nature, vol. 609(7926), pages 255-264, September.
    6. Aishwarya Agarwal & Lisha Arora & Sandeep K. Rai & Anamika Avni & Samrat Mukhopadhyay, 2022. "Spatiotemporal modulations in heterotypic condensates of prion and α-synuclein control phase transitions and amyloid conversion," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    7. Jaime Agudo-Canalejo & Sebastian W. Schultz & Haruka Chino & Simona M. Migliano & Chieko Saito & Ikuko Koyama-Honda & Harald Stenmark & Andreas Brech & Alexander I. May & Noboru Mizushima & Roland L. , 2021. "Wetting regulates autophagy of phase-separated compartments and the cytosol," Nature, Nature, vol. 591(7848), pages 142-146, March.
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    Cited by:

    1. Yohan Lee & Sujin Park & Feng Yuan & Carl C. Hayden & Liping Wang & Eileen M. Lafer & Siyoung Q. Choi & Jeanne C. Stachowiak, 2023. "Transmembrane coupling of liquid-like protein condensates," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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