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Mechanistic insights of evaporation-induced actuation in supramolecular crystals

Nature Materials volume 20, pages 403–409 (2021)Cite this article

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An Author Correction to this article was published on 08 February 2021

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Abstract

Water-responsive materials undergo reversible shape changes upon varying humidity levels. These mechanically robust yet flexible structures can exert substantial forces and hold promise as efficient actuators for energy harvesting, adaptive materials and soft robotics. Here we demonstrate that energy transfer during evaporation-induced actuation of nanoporous tripeptide crystals results from the strengthening of water hydrogen bonding that drives the contraction of the pores. The seamless integration of mobile and structurally bound water inside these pores with a supramolecular network that contains readily deformable aromatic domains translates dehydration-induced mechanical stresses through the crystal lattice, suggesting a general mechanism of efficient water-responsive actuation. The observed strengthening of water bonding complements the accepted understanding of capillary-force-induced reversible contraction for this class of materials. These minimalistic peptide crystals are much simpler in composition compared to natural water-responsive materials, and the insights provided here can be applied more generally for the design of high-energy molecular actuators.

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Fig. 1: Tripeptide crystals exhibit water responsiveness.
Fig. 2: WR properties of micrometre-scale tripeptide crystals.
Fig. 3: Reversible WR deformation of tripeptide crystals at the molecular level.
Fig. 4: Dehydration-induced H-bond strengthening in HYF.

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Data availability

The data supporting the findings of this study are included in the main text and in the Supplementary Information files, and are also available from the corresponding authors upon reasonable request. Crystallographic data of HYF can be found in the CCDC with accession number 1917273. The crystal structures of DYF and YFD reported previously27 can be found in the CCDC with accession numbers 1539905 (DYF) and 1539906 (YFD).

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References

  1. Chen, X. et al. Scaling up nanoscale water-driven energy conversion into evaporation-driven engines and generators. Nat. Commun. 6, 7346 (2015).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Ma, M., Guo, L., Anderson, D. G. & Langer, R. Bio-inspired polymer composite actuator and generator driven by water gradients. Science 339, 186–189 (2013).

    Article  CAS  Google Scholar 

  4. Arazoe, H. et al. An autonomous actuator driven by fluctuations in ambient humidity. Nat. Mater. 15, 1084–1089 (2016).

    Article  CAS  Google Scholar 

  5. Shin, B. et al. Hygrobot: a self-locomotive ratcheted actuator powered by environmental humidity. Sci. Robot. 3, 2629 (2018).

    Article  Google Scholar 

  6. Chen, L. et al. Ultrafast water sensing and thermal imaging by a metal-organic framework with switchable luminescence. Nat. Commun. 8, 15985 (2017).

    Article  CAS  Google Scholar 

  7. Kim, S. H. et al. Bio-inspired, moisture-powered hybrid carbon nanotube yarn muscles. Sci. Rep. 6, 23016 (2016).

    Article  CAS  Google Scholar 

  8. Chen, P. N. et al. Hierarchically arranged helical fibre actuators driven by solvents and vapours. Nat. Nanotechnol. 10, 1077–1083 (2015).

    Google Scholar 

  9. Cheng, H. et al. Moisture-activated torsional graphene-fiber motor. Adv. Mater. 26, 2909–2913 (2014).

    Article  CAS  Google Scholar 

  10. Evershed, R. P. et al. Archaeological frankincense. Nature 390, 667–668 (1997).

    Article  CAS  Google Scholar 

  11. Elbaum, R., Zaltzman, L., Burgert, I. & Fratzl, P. The role of wheat awns in the seed dispersal unit. Science 316, 884–886 (2007).

    Article  CAS  Google Scholar 

  12. Levin, A. et al. Elastic instability-mediated actuation by a supra-molecular polymer. Nat. Phys. 12, 926–930 (2016).

    Article  Google Scholar 

  13. Keten, S., Xu, Z. P., Ihle, B. & Buehler, M. J. Nanoconfinement controls stiffness, strength and mechanical toughness of beta-sheet crystals in silk. Nat. Mater. 9, 359–367 (2010).

    Article  CAS  Google Scholar 

  14. Ling, S., Kaplan, D. L. & Buehler, M. J. Nanofibrils in nature and materials engineering. Nat. Rev. Mater. 3, 18016 (2018).

    Article  CAS  Google Scholar 

  15. Bertinetti, L., Fischer, F. D. & Fratzl, P. Physicochemical basis for water-actuated movement and stress generation in nonliving plant tissues. Phys. Rev. Lett. 111, 238001 (2013).

    Article  CAS  Google Scholar 

  16. van Zee, N. J. et al. Potential enthalpic energy of water in oils exploited to control supramolecular structure. Nature 558, 100–103 (2018).

    Google Scholar 

  17. Aida, T., Meijer, E. W. & Stupp, S. I. Functional supramolecular polymers. Science 335, 813–817 (2012).

    Article  CAS  Google Scholar 

  18. Zhang, S. Fabrication of novel biomaterials through molecular self-assembly. Nat. Biotechnol. 21, 1171–1178 (2003).

    Article  CAS  Google Scholar 

  19. Carter, N. A. & Grove, T. Z. Protein self-assemblies that can generate, hold, and discharge electric potential in response to changes in relative humidity. J. Am. Chem. Soc. 140, 7144–7151 (2018).

    Article  CAS  Google Scholar 

  20. Gorbitz, C. H. Nanotube formation by hydrophobic dipeptides. Chemistry 7, 5153–5159 (2001).

    Article  CAS  Google Scholar 

  21. Katsoulidis, A. P. et al. Chemical control of structure and guest uptake by a conformationally mobile porous material. Nature 565, 213–217 (2019).

    Article  CAS  Google Scholar 

  22. Rabone, J. et al. An adaptable peptide-based porous material. Science 329, 1053–1057 (2010).

    Article  CAS  Google Scholar 

  23. Huang, Z. et al. Pulsating tubules from noncovalent macrocycles. Science 337, 1521–1526 (2012).

    Article  CAS  Google Scholar 

  24. Freeman, R. et al. Reversible self-assembly of superstructured networks. Science 362, 808–813 (2018).

    Article  CAS  Google Scholar 

  25. Suzuki, Y. et al. Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals. Nature 533, 369–373 (2016).

    Article  CAS  Google Scholar 

  26. Ortony, J. H. et al. Internal dynamics of a supramolecular nanofibre. Nat. Mater. 13, 812–816 (2014).

    Article  CAS  Google Scholar 

  27. Lampel, A. et al. Polymeric peptide pigments with sequence-encoded properties. Science 356, 1064–1068 (2017).

    Article  CAS  Google Scholar 

  28. Zhang, L., Bailey, J. B., Subramanian, R. H., Groisman, A. & Tezcan, F. A. Hyperexpandable, self-healing macromolecular crystals with integrated polymer networks. Nature 557, 86–91 (2018).

    Article  CAS  Google Scholar 

  29. Wang, M., Shijie, X., Wu, X. & Chu, P. Effects of water molecules on photoluminescence from hierarchical peptide nanotubes and water probing capability. Small 19, 2801–2807 (2011).

    Article  Google Scholar 

  30. Lampel, A., Ulijn, R. V. & Tuttle, T. Guiding principles for peptide nanotechnology through directed discovery. Chem. Soc. Rev. 47, 3737–3758 (2018).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  32. Frederix, P. W. et al. Exploring the sequence space for (tri-)peptide self-assembly to design and discover new hydrogels. Nat. Chem. 7, 30–37 (2015).

    Article  CAS  Google Scholar 

  33. Park, Y. & Chen, X. Water-responsive materials for sustainable energy applications. J. Mater. Chem. A 8, 15227–15244 (2020).

    Article  CAS  Google Scholar 

  34. Mason, T. O. et al. Expanding the solvent chemical space for self-assembly of dipeptide nanostructures. ACS Nano 8, 1243–1253 (2014).

    Article  CAS  Google Scholar 

  35. Lowell, S. & Lowell, S. Characterization of Porous Solids and Powders: Surface Area, Pore Size and Density 3rd edn (Kluwer Academic Publishers, 2004).

  36. Myshakina, N. S., Ahmed, Z. & Asher, S. A. Dependence of amide vibrations on hydrogen bonding. J. Phys. Chem. B 112, 11873–11877 (2008).

    Article  CAS  Google Scholar 

  37. Socrates, G. Infrared and Raman Characteristic Group Frequencies: Tables and Charts 3rd edn (Wiley, 2001).

  38. Gun’ko, V. M. et al. Unusual properties of water at hydrophilic/hydrophobic interfaces. Adv. Colloid Interface Sci. 118, 125–172 (2005).

    Article  Google Scholar 

  39. Brini, E. et al. How water’s properties are encoded in its molecular structure and energies. Chem. Rev. 117, 12385–12414 (2017).

    Article  CAS  Google Scholar 

  40. Bird, J. Electrical Principles and Technology for Engineering 1st edn, 188–189 (Butterworth-Heinemann, 1995).

Download references

Acknowledgements

This work was supported in part by the Office of Naval Research (ONR; N00014-18-1-2492), the Air Force Office of Scientific Research (AFOSR; FA9550-19-1-0111), the National Science Foundation (NSF; CHE-1808143), the EPSRC-funded ARCHIE-WeSt High Performance Computer (www.archie-west.ac.uk) for computational resources via EPSRC grant no. EP/K000586/1 and the CUNY/Strathclyde partnership. We acknowledge that the powder X-ray diffraction and DVS experiments were carried out in the CMAC National Facility, housed within the University of Strathclyde’s Technology and Innovation Centre, and funded with a UKRPIF (UK Research Partnership Institute Fund) capital award, SFC ref. H13054, from the Higher Education Funding Council for England (HEFCE). C.T.H. acknowledges the support of the National Science Foundation (NSF) Chemistry Research Instrumentation and Facilities Program (CHE-0840277) and Materials Research Science and Engineering Center (MRSEC) Program (DMR-1420073).

Author information

Authors and Affiliations

  1. Advanced Science Research Center (ASRC) at the Graduate Center of the City University of New York, New York, NY, USA

    Roxana Piotrowska, Haozhen Wang, Chunqiu Zhang, Scott A. McPhee, Tong Wang, Yaewon Park, Pulkit Singla, Rein V. Ulijn & Xi Chen

  2. PhD Program in Chemistry, The Graduate Center of the City University of New York, New York, NY, USA

    Roxana Piotrowska, Rein V. Ulijn & Xi Chen

  3. Department of Pure and Applied Chemistry, University of Strathclyde, Glasgow, UK

    Travis Hesketh & Tell Tuttle

  4. PhD Program in Physics, The Graduate Center of the City University of New York, New York, NY, USA

    Haozhen Wang & Xi Chen

  5. EPSRC Continuous Manufacturing and Crystallisation Future Research Hub c/o Strathclyde Institute of Pharmacy and Biomedical Sciences, Technology Innovation Centre, University of Strathclyde, Glasgow, UK

    Alan R. G. Martin, Deborah Bowering, Thomas McGlone & Alastair Florence

  6. Department of Chemistry, New York University, New York, NY, USA

    Chunhua T. Hu

  7. Department of Chemistry and Biochemistry, Hunter College, City University of New York, New York, NY, USA

    Rein V. Ulijn

  8. Department of Chemical Engineering, The City College of New York, New York, NY, USA

    Xi Chen

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  1. Roxana Piotrowska
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Contributions

X.C. and R.V.U. conceived and initiated the project. R.P. grew tripeptide crystals. R.P. and S.A.M. performed FTIR measurements and analysed the data. T.H. and T.T. performed MD simulations. H.W. and R.P. performed AFM measurements and analysed the data. A.R.G.M. and D.B. conducted the powder X-ray diffraction and DVS experiments and data analysis. C.Z. initiated the crystallization of HYF. C.T.H. conducted single-crystal X-ray diffraction experiments and solved single-crystal structures. T.W. and X.C. characterized crystal morphologies. All authors contributed to data analysis and discussed the results. R.P., T.T., R.V.U. and X.C. wrote the paper. T.T., R.V.U. and X.C. supervised the project.

Corresponding authors

Correspondence to Tell Tuttle, Rein V. Ulijn or Xi Chen.

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Extended data

Extended Data Fig. 1 Tripeptides crystallization.

Tripeptides (a) HYF, (b) DYF and (c) YFD crystallize in phosphate buffer at pH 8, scale bar 2 cm. Optical microscopy images of (d) HYF, (e) DYF, and (f) YFD crystals; scale bar 100 μm.

Extended Data Fig. 2 DYF and YFD molecular structure.

Top (a) and side (b) view of structure of monoclinic DYF crystal with blue colored nanopores. The volume of the solvent accessible area in DYF is 355 Å3 (14.1%) per unit cell. (c) and (d) show the cross-sectional view of (a). Top view of an individual void (e). There are two voids per unit cell, each occupying 7%. Each void has dimensions of ~13.4 Å x 6.1 Å. Top (f) and side (g) view of structure of monoclinic YFD crystal with blue coloured water voids. The volume of the solvent accessible area in YFD is 78 Å3 (3.4%) per unit cell. (h) and (i) show the cross-sectional view of (g). Top view of an individual void (j). These crystal structures were previously published in27; the representation used here emphasizes the water voids in these structures.

Extended Data Fig. 3 Water responsiveness of DYF and YFD.

(a) AFM topography image of DYF at 10% RH. Scale bar, 1 μm. Crystals change their dimensions in height (b) vs. % RH. (c) Volume vs. % RH of DYF. (d) DVS water sorption of DYF at varying RH levels. (e) % Mass change obtained by DVS showing hysteresis between 20% - 40% during hydration/dehydration cycles. (f) AFM topography image of YFD at 10% RH. Scale bar, 2 μm. (g) Crystals only change its dimension in height vs. % RH. (h) Volume vs. % RH of YFD. (i) DVS water sorption of YFD at varying RH levels. (j)% Mass change obtained by DVS showing hysteresis between 20% - 40% during hydration/dehydration cycles. Error bars represent standard deviations calculated from three measurements.

Extended Data Fig. 4 The lattice parameter changes of DYF.

Comparisons of the lattice parameter changes of DYF in (a) c, derived from the Pawley refinement and a, derived from the Pawley refinement with MD simulated illustrated distance, and (b) b, derived from the Pawley refinement with MD simulated backbone–backbone distance (illustrated in inset) in response to RH/R. Hyd. changes. Error bars represent standard deviations calculated from three measurements.

Extended Data Fig. 5

Top view MD simulated void structures of HYF indicating decrease of water molecules (red dots) and collapse during dehydration processes.

Extended Data Fig. 6 Top view MD simulated void structures of DYF.

Water molecules are shown as red dots.

Supplementary information

Supplementary Information

Supplementary Notes 1–8, Video legends, Figs. 1–20, Tables 1 and 2 and references.

Supplementary Video 1

Bending of the polyimide film with deposited crystals in response to decrease in RH from 90% to 10%.

Supplementary Video 2

Microscopy video showing HYF crystal (left) and weakening of second harmonic signal (right) in response to RH decrease from 90% to 10%.

Supplementary Video 3

HYF unit cell rotation.

Supplementary Video 4

DYF unit cell rotation.

Supplementary Video 5

YFD unit cell rotation.

Supplementary Video 6

Simulation of pore shrinking and side view of the simulated HYF crystal structure in response to decrease in R. Hyd. from 100% to 10%.

Supplementary Video 7

Simulation of pore shrinking and side view of the simulated DYF crystal structure in response to decrease in R. Hyd. from 100% to 10%.

Supplementary Video 8

Testing bonding strength between HYF/adhesive composites and polyimide films.

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Piotrowska, R., Hesketh, T., Wang, H. et al. Mechanistic insights of evaporation-induced actuation in supramolecular crystals. Nat. Mater. 20, 403–409 (2021). https://doi.org/10.1038/s41563-020-0799-0

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