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The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems

Author

Listed:
  • Keren Lasker

    (Stanford University School of Medicine
    The Scripps Research Institute)

  • Steven Boeynaems

    (Stanford University School of Medicine)

  • Vinson Lam

    (University of California San Diego)

  • Daniel Scholl

    (The Scripps Research Institute)

  • Emma Stainton

    (Stanford University School of Medicine)

  • Adam Briner

    (The University of Queensland)

  • Maarten Jacquemyn

    (KU Leuven)

  • Dirk Daelemans

    (KU Leuven)

  • Ashok Deniz

    (The Scripps Research Institute)

  • Elizabeth Villa

    (University of California San Diego
    University of California San Diego)

  • Alex S. Holehouse

    (Washington University in St. Louis
    Washington University in St. Louis)

  • Aaron D. Gitler

    (Stanford University School of Medicine)

  • Lucy Shapiro

    (Stanford University School of Medicine)

Abstract

Intracellular phase separation is emerging as a universal principle for organizing biochemical reactions in time and space. It remains incompletely resolved how biological function is encoded in these assemblies and whether this depends on their material state. The conserved intrinsically disordered protein PopZ forms condensates at the poles of the bacterium Caulobacter crescentus, which in turn orchestrate cell-cycle regulating signaling cascades. Here we show that the material properties of these condensates are determined by a balance between attractive and repulsive forces mediated by a helical oligomerization domain and an expanded disordered region, respectively. A series of PopZ mutants disrupting this balance results in condensates that span the material properties spectrum, from liquid to solid. A narrow range of condensate material properties supports proper cell division, linking emergent properties to organismal fitness. We use these insights to repurpose PopZ as a modular platform for generating tunable synthetic condensates in human cells.

Suggested Citation

  • Keren Lasker & Steven Boeynaems & Vinson Lam & Daniel Scholl & Emma Stainton & Adam Briner & Maarten Jacquemyn & Dirk Daelemans & Ashok Deniz & Elizabeth Villa & Alex S. Holehouse & Aaron D. Gitler & , 2022. "The material properties of a bacterial-derived biomolecular condensate tune biological function in natural and synthetic systems," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33221-z
    DOI: 10.1038/s41467-022-33221-z
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    1. Hong Joo Kim & Nam Chul Kim & Yong-Dong Wang & Emily A. Scarborough & Jennifer Moore & Zamia Diaz & Kyle S. MacLea & Brian Freibaum & Songqing Li & Amandine Molliex & Anderson P. Kanagaraj & Robert Ca, 2013. "Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS," Nature, Nature, vol. 495(7442), pages 467-473, March.
    2. Emanuele G. Biondi & Sarah J. Reisinger & Jeffrey M. Skerker & Muhammad Arif & Barrett S. Perchuk & Kathleen R. Ryan & Michael T. Laub, 2006. "Regulation of the bacterial cell cycle by an integrated genetic circuit," Nature, Nature, vol. 444(7121), pages 899-904, December.
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    Cited by:

    1. Viet Sang Doan & Ibraheem Alshareedah & Anurag Singh & Priya R. Banerjee & Sangwoo Shin, 2024. "Diffusiophoresis promotes phase separation and transport of biomolecular condensates," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Saumyak Mukherjee & Lars V. Schäfer, 2023. "Thermodynamic forces from protein and water govern condensate formation of an intrinsically disordered protein domain," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. 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.
    4. Y Hoang & Christopher A. Azaldegui & Rachel E. Dow & Maria Ghalmi & Julie S. Biteen & Anthony G. Vecchiarelli, 2024. "An experimental framework to assess biomolecular condensates in bacteria," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    5. 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.
    6. Maruša Ramšak & Dominique A. Ramirez & Loren E. Hough & Michael R. Shirts & Sara Vidmar & Kristina Eleršič Filipič & Gregor Anderluh & Roman Jerala, 2023. "Programmable de novo designed coiled coil-mediated phase separation in mammalian cells," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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