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Programmable viscoelasticity in protein-RNA condensates with disordered sticker-spacer polypeptides

Author

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  • Ibraheem Alshareedah

    (University at Buffalo)

  • Mahdi Muhammad Moosa

    (University at Buffalo)

  • Matthew Pham

    (Iowa State University)

  • Davit A. Potoyan

    (Iowa State University)

  • Priya R. Banerjee

    (University at Buffalo)

Abstract

Liquid-liquid phase separation of multivalent proteins and RNAs drives the formation of biomolecular condensates that facilitate membrane-free compartmentalization of subcellular processes. With recent advances, it is becoming increasingly clear that biomolecular condensates are network fluids with time-dependent material properties. Here, employing microrheology with optical tweezers, we reveal molecular determinants that govern the viscoelastic behavior of condensates formed by multivalent Arg/Gly-rich sticker-spacer polypeptides and RNA. These condensates behave as Maxwell fluids with an elastically-dominant rheological response at shorter timescales and a liquid-like behavior at longer timescales. The viscous and elastic regimes of these condensates can be tuned by the polypeptide and RNA sequences as well as their mixture compositions. Our results establish a quantitative link between the sequence- and structure-encoded biomolecular interactions at the microscopic scale and the rheological properties of the resulting condensates at the mesoscale, enabling a route to systematically probe and rationally engineer biomolecular condensates with programmable mechanics.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26733-7
    DOI: 10.1038/s41467-021-26733-7
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    References listed on IDEAS

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    3. Mina Farag & Samuel R. Cohen & Wade M. Borcherds & Anne Bremer & Tanja Mittag & Rohit V. Pappu, 2022. "Condensates formed by prion-like low-complexity domains have small-world network structures and interfaces defined by expanded conformations," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Andres R. Tejedor & Ignacio Sanchez-Burgos & Maria Estevez-Espinosa & Adiran Garaizar & Rosana Collepardo-Guevara & Jorge Ramirez & Jorge R. Espinosa, 2022. "Protein structural transitions critically transform the network connectivity and viscoelasticity of RNA-binding protein condensates but RNA can prevent it," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    5. Min Lee & Hyungseok C. Moon & Hyeonjeong Jeong & Dong Wook Kim & Hye Yoon Park & Yongdae Shin, 2024. "Optogenetic control of mRNA condensation reveals an intimate link between condensate material properties and functions," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    6. 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.
    7. Mrityunjoy Kar & Laura T. Vogel & Gaurav Chauhan & Suren Felekyan & Hannes Ausserwöger & Timothy J. Welsh & Furqan Dar & Anjana R. Kamath & Tuomas P. J. Knowles & Anthony A. Hyman & Claus A. M. Seidel, 2024. "Solutes unmask differences in clustering versus phase separation of FET proteins," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    8. Dinesh Sundaravadivelu Devarajan & Jiahui Wang & Beata Szała-Mendyk & Shiv Rekhi & Arash Nikoubashman & Young C. Kim & Jeetain Mittal, 2024. "Sequence-dependent material properties of biomolecular condensates and their relation to dilute phase conformations," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. 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.
    10. Merlijn H. I. Haren & Brent S. Visser & Evan Spruijt, 2024. "Probing the surface charge of condensates using microelectrophoresis," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
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