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Dissipative adaptation in driven self-assembly leading to self-dividing fibrils

Nature Nanotechnology volume 13, pages 849–855 (2018)Cite this article

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Abstract

Out-of-equilibrium self-assembly of proteins such as actin and tubulin is a key regulatory process controlling cell shape, motion and division. The design of functional nanosystems based on dissipative self-assembly has proven to be remarkably difficult due to a complete lack of control over the spatial and temporal characteristics of the assembly process. Here, we show the dissipative self-assembly of FtsZ protein (a bacterial homologue of tubulin) within coacervate droplets. More specifically, we show how such barrier-free compartments govern the local availability of the energy-rich building block guanosine triphosphate, yielding highly dynamic fibrils. The increased flux of FtsZ monomers at the tips of the fibrils results in localized FtsZ assembly, elongation of the coacervate compartments, followed by division of the fibrils into two. We rationalize the directional growth and division of the fibrils using dissipative reaction–diffusion kinetics and capillary action of the filaments as main inputs. The principle presented here, in which open compartments are used to modulate the rates of dissipative self-assembly by restricting the absorption of energy from the environment, may provide a general route to dissipatively adapting nanosystems exhibiting life-like behaviour.

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Fig. 1: A combination of FtsZ dissipative self-assembly and compartmentalization in coacervate droplets can lead to dissipative adaptation.
Fig. 2: FtsZ filaments form bundles that can deform coacervate droplets.
Fig. 3: Shape of the compartmentalized FtsZ assemblies depends on the available drive.
Fig. 4: Fibrils are dynamic, self-dividing structures of FtsZ bundles with a coacervate layer.
Fig. 5: Division of fibrils can be modelled using a combination of reaction–diffusion kinetics and capillary action.

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Acknowledgements

This work was supported by the Netherlands Organization for Scientific Research (NWO, VICI grant 700.10.44 and ECHO-STIP grant 717.012.001) and funding from the Dutch Ministry of Education, Culture and Science (Gravity program 024.001.035). G.R. is supported by the Spanish Government through grant BFU2016-75471-C2-1-P. A.H. is grateful for financial support from the European Commission through an ERC Advanced Grant (SUPRABIOTICS, no. 694610). The authors thank K.A. Brakke (Susquehanna University) for help with Surface Evolver modelling.

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Authors and Affiliations

  1. Institute for Molecules and Materials, Radboud University, Nijmegen, The Netherlands

    Esra te Brinke, Joost Groen, Hans A. Heus, Evan Spruijt & Wilhelm T. S. Huck

  2. DWI Leibniz Institute for Interactive Materials, Aachen, Germany

    Andreas Herrmann

  3. Institute of Technical and Macromolecular Chemistry, RWTH Aachen University, Aachen, Germany

    Andreas Herrmann

  4. Systems Biochemistry Lab, Centro de Investigaciones Biológicas, CSIC, Madrid, Spain

    Germán Rivas

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Contributions

E.t.B., J.G. and E.S. carried out all experiments. A.H. and G.R. contributed materials (GFP-K72 and FtsZ/Alex647-FtsZ, respectively). Modelling was performed by E.S. All authors discussed the results. E.S. and W.T.S.H. wrote the manuscript.

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Correspondence to Evan Spruijt or Wilhelm T. S. Huck.

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Supplementary information

Supplementary Information

Supplementary Video 1

Time evolution of FtsZ (1.0 g l–1 overall concentration) filaments bundled inside torula yeast RNA/GFP-K72 coacervates upon exposure to a slowly increasing concentration of GTP.

Supplementary Video 2

Dynamic fibrils of FtsZ filaments bundled inside torula yeast RNA/GFP-K72 coacervates, displaying bending, motion, growth, splitting and fusion at 1.0 g l–1 FtsZ and an initial GTP concentration of 10 mM.

Supplementary Video 3

Fibrils of FtsZ filaments bundled inside torula yeast RNA/GFP-K72 coacervates in the presence of the slowly hydrolysable GTP analogue GMPCPP, displaying no dynamic behaviour.

Supplementary Video 4

Dynamics of elongated coacervate droplets of torula yeast RNA/GFP-K72 at 1.0 g l–1 FtsZ and an initial GTP concentration of 5 mM.

Supplementary Video 5

Initial dynamics of very long fibrils of FtsZ filaments bundled inside torula yeast RNA/GFP-K72 coacervates at 1.0 g l–1 FtsZ and 10.2 mM GTP.

Supplementary Video 6

A droplet held between five parallel filaments is forced to stretch and split by capillary action caused by four additional filaments touching both ends of the initial droplet.

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te Brinke, E., Groen, J., Herrmann, A. et al. Dissipative adaptation in driven self-assembly leading to self-dividing fibrils. Nature Nanotech 13, 849–855 (2018). https://doi.org/10.1038/s41565-018-0192-1

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