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Phase-separated droplets swim to their dissolution

Author

Listed:
  • Etienne Jambon-Puillet

    (ETH Zürich
    Institut Polytechnique de Paris)

  • Andrea Testa

    (ETH Zürich)

  • Charlotta Lorenz

    (ETH Zürich
    Cornell University)

  • Robert W. Style

    (ETH Zürich)

  • Aleksander A. Rebane

    (ETH Zürich
    New York University Abu Dhabi)

  • Eric R. Dufresne

    (ETH Zürich
    Cornell University)

Abstract

Biological macromolecules can condense into liquid domains. In cells, these condensates form membraneless organelles that can organize chemical reactions. However, little is known about the physical consequences of chemical activity in and around condensates. Working with model bovine serum albumin (BSA) condensates, we show that droplets swim along chemical gradients. Active BSA droplets loaded with urease swim toward each other. Passive BSA droplets show diverse responses to externally applied gradients of the enzyme’s substrate and products. In all these cases, droplets swim toward solvent conditions that favor their dissolution. We call this behavior “dialytaxis”, and expect it to be generic, as conditions which favor dissolution typically reduce interfacial tension, whose gradients are well-known to drive droplet motion through the Marangoni effect. These results could potentially suggest alternative physical mechanisms for active transport in living cells, and may enable the design of fluid micro-robots.

Suggested Citation

  • Etienne Jambon-Puillet & Andrea Testa & Charlotta Lorenz & Robert W. Style & Aleksander A. Rebane & Eric R. Dufresne, 2024. "Phase-separated droplets swim to their dissolution," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47889-y
    DOI: 10.1038/s41467-024-47889-y
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    1. William E. Arter & Runzhang Qi & Nadia A. Erkamp & Georg Krainer & Kieran Didi & Timothy J. Welsh & Julia Acker & Jonathan Nixon-Abell & Seema Qamar & Jordina Guillén-Boixet & Titus M. Franzmann & Dav, 2022. "Biomolecular condensate phase diagrams with a combinatorial microdroplet platform," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Karina K. Nakashima & Merlijn H. I. Haren & Alain A. M. André & Irina Robu & Evan Spruijt, 2021. "Active coacervate droplets are protocells that grow and resist Ostwald ripening," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    3. Carsten Donau & Fabian Späth & Marilyne Sosson & Brigitte A. K. Kriebisch & Fabian Schnitter & Marta Tena-Solsona & Hyun-Seo Kang & Elia Salibi & Michael Sattler & Hannes Mutschler & Job Boekhoven, 2020. "Active coacervate droplets as a model for membraneless organelles and protocells," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    4. Miriam Linsenmeier & Maria Hondele & Fulvio Grigolato & Eleonora Secchi & Karsten Weis & Paolo Arosio, 2022. "Dynamic arrest and aging of biomolecular condensates are modulated by low-complexity domains, RNA and biochemical activity," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Christine K. Schmidt & Mariana Medina-Sánchez & Richard J. Edmondson & Oliver G. Schmidt, 2020. "Engineering microrobots for targeted cancer therapies from a medical perspective," Nature Communications, Nature, vol. 11(1), pages 1-18, December.
    6. Pilong Li & Sudeep Banjade & Hui-Chun Cheng & Soyeon Kim & Baoyu Chen & Liang Guo & Marc Llaguno & Javoris V. Hollingsworth & David S. King & Salman F. Banani & Paul S. Russo & Qiu-Xing Jiang & B. Tra, 2012. "Phase transitions in the assembly of multivalent signalling proteins," Nature, Nature, vol. 483(7389), pages 336-340, March.
    7. Michel Fruchart & Ryo Hanai & Peter B. Littlewood & Vincenzo Vitelli, 2021. "Non-reciprocal phase transitions," Nature, Nature, vol. 592(7854), pages 363-369, April.
    8. 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.
    9. N. J. Cira & A. Benusiglio & M. Prakash, 2015. "Vapour-mediated sensing and motility in two-component droplets," Nature, Nature, vol. 519(7544), pages 446-450, March.
    10. Maria Hondele & Ruchika Sachdev & Stephanie Heinrich & Juan Wang & Pascal Vallotton & Beatriz M. A. Fontoura & Karsten Weis, 2019. "DEAD-box ATPases are global regulators of phase-separated organelles," Nature, Nature, vol. 573(7772), pages 144-148, September.
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