Letter | Published:

Self-assembly of coherently dynamic, auxetic, two-dimensional protein crystals

Nature volume 533, pages 369373 (19 May 2016) | Download Citation

Abstract

Two-dimensional (2D) crystalline materials possess unique structural, mechanical and electronic properties1,2 that make them highly attractive in many applications3,4,5. Although there have been advances in preparing 2D materials that consist of one or a few atomic or molecular layers6,7, bottom-up assembly of 2D crystalline materials remains a challenge and an active area of development8,9,10. More challenging is the design of dynamic 2D lattices that can undergo large-scale motions without loss of crystallinity. Dynamic behaviour in porous three-dimensional (3D) crystalline solids has been exploited for stimuli-responsive functions and adaptive behaviour11,12,13. As in such 3D materials, integrating flexibility and adaptiveness into crystalline 2D lattices would greatly broaden the functional scope of 2D materials. Here we report the self-assembly of unsupported, 2D protein lattices with precise spatial arrangements and patterns using a readily accessible design strategy. Three single- or double-point mutants of the C4-symmetric protein RhuA were designed to assemble via different modes of intermolecular interactions (single-disulfide, double-disulfide and metal-coordination) into crystalline 2D arrays. Owing to the flexibility of the single-disulfide interactions, the lattices of one of the variants (C98RhuA) are essentially defect-free and undergo substantial, but fully correlated, changes in molecular arrangement, yielding coherently dynamic 2D molecular lattices. C98RhuA lattices display a Poisson’s ratio of −1—the lowest thermodynamically possible value for an isotropic material—making them auxetic.

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Acknowledgements

We thank M. Sailor, H. Gray, R. Alberstein and F. Paesani for discussions, N. Olson and J. Bouwer for assistance with TEM measurements, and N. Gianneschi for the use of AFM and DLS instrumentation. This work was primarily supported by the US Department of Energy (DOE) (Division of Materials Sciences, Office of Basic Energy Sciences, Award DE-FG02-10ER46677 to F.A.T.). Y.S. and F.A.T. were partially supported (for EM measurements) by a grant from the Air Force Office of Scientific Research (AFOSR, BRI FA9550-12-1-0414). The EM facilities used in this work are supported by funding to T.S.B. from the NIH (1S10 RR-020016 and GM-033050), the Agouron Foundation and UCSD.

Author information

Affiliations

  1. Department of Chemistry and Biochemistry, University of California, San Diego, La Jolla, California 92093, USA

    • Yuta Suzuki
    • , Giovanni Cardone
    • , Timothy S. Baker
    •  & F. Akif Tezcan
  2. School of Civil Engineering, Purdue University, West Lafayette, Indiana 47907-2051, USA

    • David Restrepo
    •  & Pablo D. Zavattieri
  3. Division of Biological Sciences, University of California, San Diego, La Jolla, California 92093, USA

    • Timothy S. Baker

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Contributions

Y.S. and F.A.T. conceived the work and designed the experiments. Y.S. carried out all experimental work and EM measurements. G.C. and Y.S. performed, and T.S.B. oversaw, EM data analysis. D.R. and P.D.Z. performed digital image-correlation analysis. F.A.T. and Y.S. wrote the manuscript with contributions from G.C., T.S.B., D.R. and P.D.Z.

Competing interests

F.A.T. and Y.S. are inventors on two provisional patent applications based on the described work.

Corresponding author

Correspondence to F. Akif Tezcan.

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    Supplementary Information

    This file contains Supplementary Figures 1-3 and Supplementary Tables 1-4.

Videos

  1. 1.

    Illustrates the dynamics of 2D C98RhuA crystals starting from the TEM snapshots of the seven conformational states (I–VII; Fig. 3a).

    All projected density images were rescaled to include the same field of view (bint and bimg from Bsoft). Twenty-four intermediate image frames were created between each pair in the sequence by pseudo-morphing, using the program convert from the software suite ImageMagick.

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DOI

https://doi.org/10.1038/nature17633

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