Mechanistic insights of evaporation-induced actuation in supramolecular crystals

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.

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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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

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Authors

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 or 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, 500 nm. (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. (2020). https://doi.org/10.1038/s41563-020-0799-0

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