Elastic instability-mediated actuation by a supra-molecular polymer

Abstract

In nature, fast, high-power-density actuation can be achieved through the release of stored elastic energy by exploiting mechanical instabilities in systems including the closure of the Venus flytrap1 and the dispersal of plant or fungal spores2. Here, we use droplet microfluidics to tailor the geometry of a nanoscale self-assembling supra-molecular polymer to create a mechanical instability. We show that this strategy allows the build-up of elastic energy as a result of peptide self-assembly, and its release within milliseconds when the buckled geometry of the nanotube confined within microdroplets becomes unstable with respect to the straight form. These results overcome the inherent limitations of self-assembly for generating large-scale actuation on the sub-second timescale and illuminate the possibilities and performance limits of irreversible actuation by supra-molecular polymers.

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Figure 1: FF tubes are able to pierce through water-in-oil double layer interfaces.
Figure 2: Tailoring the geometry of FF self-assembly to create a mechanical instability.
Figure 3: Control of FF nanotube unbuckling by external stimuli and generation of external work.
Figure 4: Comparison of energy and power generation by biological and synthetic systems.

References

  1. 1

    Forterre, Y., Skotheim, J. M., Dumais, J. & Mahadevan, L. How the Venus flytrap snaps. Nature 433, 421–425 (2005).

  2. 2

    Noblin, X. et al. The fern sporangium: a unique catapult. Science 335, 1322 (2012).

  3. 3

    Ideses, Y., Sonn-Segev, A., Roichman, Y. & Bernheim-Groswasser, A. Myosin II does it all: assembly, remodeling, and disassembly of actin networks are governed by myosin II activity. Soft Matter 9, 7127–7137 (2013).

  4. 4

    Higa, T., Suetsugu, N., Kong, S.-G. & Wada, M. Actin-dependent plastid movement is required for motive force generation in directional nuclear movement in plants. Proc. Natl Acad. Sci. USA 111, 4327–4331 (2014).

  5. 5

    Schliwa, M. & Woehlke, G. Molecular motors. Nature 422, 759–765 (2003).

  6. 6

    Brunsveld, L., Folmer, B., Meijer, E. & Sijbesma, R. Supramolecular polymers. Chem. Rev. 101, 4071–4097 (2001).

  7. 7

    Lehn, J. M. Perspectives in supramolecular chemistry- from molecular recognition towards molecular information processing and self-organization. Angew. Chem. Int. Ed. Engl. 29, 1304–1319 (1990).

  8. 8

    Burnworth, M. et al. Optically healable supramolecular polymers. Nature 472, 334–338 (2011).

  9. 9

    Ananthakrishnan, R. & Ehrlicher, A. The forces behind cell movement. Int. J. Biol. Sci. 3, 303–317 (2007).

  10. 10

    Aratyn-Schaus, Y., Oakes, P. W. & Gardel, M. L. Dynamic and structural signatures of lamellar actomyosin force generation. Mol. Biol. Cell 22, 1330–1339 (2011).

  11. 11

    Tan, J. L. et al. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl Acad. Sci. USA 100, 1484–1489 (2003).

  12. 12

    Roberts, A. J., Kon, T., Knight, P. J., Sutoh, K. & Burgess, S. A. Functions and mechanics of dynein motor proteins. Nature Rev. Mol. Cell Biol. 14, 713–726 (2013).

  13. 13

    Granger, E., McNee, G., Allan, V. & Woodman, P. The role of the cytoskeleton and molecular motors in endosomal dynamics. Semin. Cell. Dev. Biol. 31, 20–29 (2014).

  14. 14

    Mahadevan, L. & Matsudaira, P. Motility powered by supramolecular springs and ratchets. Science 288, 95–99 (2000).

  15. 15

    Krause, M. & Gautreau, A. Steering cell migration: lamellipodium dynamics and the regulation of directional persistence. Nature Rev. Mol. Cell Biol. 15, 577–590 (2014).

  16. 16

    Amari, K., Di Donato, M., Dolja, V. V. & Heinlein, M. Myosins VIII and XI play distinct roles in reproduction and transport of tobacco mosaic virus. PLoS Pathogens 10, e1004448 (2014).

  17. 17

    Utada, A. S. et al. Vibrio cholerae use pili and flagella synergistically to effect motility switching and conditional surface attachment. Nature Commun. 5, 4913 (2014).

  18. 18

    Chen, X., Mahadevan, L., Driks, A. & Sahin, O. Bacillus spores as building blocks for stimuli-responsive materials and nanogenerators. Nature Nanotech. 9, 137–141 (2014).

  19. 19

    Sedman, V. L., Adler-Abramovich, L., Allen, S., Gazit, E. & Tendler, S. J. B. Direct observation of the release of phenylalanine from diphenylalanine nanotubes. J. Am. Chem. Soc. 128, 6903–6908 (2006).

  20. 20

    Hendler, N. et al. Formation of well-organized self-assembled films from peptide nanotubes. Adv. Mater. 19, 1485–1488 (2007).

  21. 21

    Guo, C., Luo, Y., Zhou, R. & Wei, G. Probing the self-assembly mechanism of diphenylalanine-based peptide nanovesicles and nanotubes. ACS Nano 6, 3907–3918 (2012).

  22. 22

    Kim, J. et al. Role of water in directing diphenylalanine assembly into nanotubes and nanowires. Adv. Mater. 22, 583–587 (2010).

  23. 23

    Ikezoe, Y., Washino, G., Uemura, T., Kitagawa, S. & Matsui, H. Autonomous motors of a metalorganic framework powered by reorganization of self-assembled peptides at interfaces. Nature Mater. 11, 1081–1085 (2012).

  24. 24

    Hofrichter, J., Ross, P. D. & Eaton, W. A. Kinetics and mechanism of deoxyhemoglobin S gelation: a new approach to understanding sickle cell disease. Proc. Natl Acad. Sci. USA 71, 4864–4868 (1974).

  25. 25

    Kashchiev, D. Nucleation: Basic Theory with Applications (Oxford Univ. Press, 2000).

  26. 26

    Cohen, A. E. & Mahadevan, L. Kinks, rings, and rackets in filamentous structures. Proc. Natl Acad. Sci. USA 100, 12141–12146 (2003).

  27. 27

    Kol, N. et al. Self-assembled peptide nanostructures are uniquely rigid bioinspired supramolecular structures. Nano Lett. 5, 1343–1346 (2005).

  28. 28

    Hunter, I. & Lafontaine, S. A comparison of muscle with artificial actuators Tech. Dig. IEEE Solid-State Sensor Actuator Workshop Hilton Head, South Carolina 178–185 (1992).

  29. 29

    Reches, M. & Gazit, E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300, 625–627 (2003).

  30. 30

    Adler-Abramovich, L. et al. Thermal and chemical stability of diphenylalanine peptide nanotubes: implications for nanotechnological applications. Langmuir 22, 1313–1320 (2006).

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Acknowledgements

This work was supported by a short-term fellowship from EMBO and from FEBS (A.L.), the Newman Foundation (A.L., T.O.M., T.P.J.K.), the Tel Aviv University Center for Nanoscience and Nanotechnology (A.L.), St John’s College Cambridge (T.C.T.M.), the Israeli National Nanotechnology Initiative and Helmsley Charitable Trust (E.G.), Elan Pharmaceuticals (T.O.M.), the UK BBSRC (T.P.J.K.) and the ERC (T.P.J.K., T.C.T.M.). We thank P. Marcu and Z. Arnon for their assistance with the high-resolution scanning electron microscopy imaging, and members of the Gazit and Knowles groups for helpful discussion.

Author information

A.L., T.C.T.M., L.M., E.G. and T.P.J.K. conceived and designed the experiments. A.L., T.O.M., B.Z. and T.C.T.M. planned and performed the experiments. T.C.T.M., L.M. and T.P.J.K. developed the theory and analysed the experimental data. T.M. provided the fast camera set-up. A.L., T.C.T.M., L.A.-A., T.O.M., T.M., L.M., E.G. and T.P.J.K. wrote the manuscript. All authors discussed the results, provided intellectual input and critical feedback and commented on the manuscript.

Correspondence to Ehud Gazit or Tuomas P. J. Knowles.

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The authors declare no competing financial interests.

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Levin, A., Michaels, T., Adler-Abramovich, L. et al. Elastic instability-mediated actuation by a supra-molecular polymer. Nature Phys 12, 926–930 (2016). https://doi.org/10.1038/nphys3808

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