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Nanoconfinement controls stiffness, strength and mechanical toughness of β-sheet crystals in silk

Nature Materials volume 9, pages 359–367 (2010)Cite this article

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Abstract

Silk features exceptional mechanical properties such as high tensile strength and great extensibility, making it one of the toughest materials known. The exceptional strength of silkworm and spider silks, exceeding that of steel, arises from β-sheet nanocrystals that universally consist of highly conserved poly-(Gly-Ala) and poly-Ala domains. This is counterintuitive because the key molecular interactions in β-sheet nanocrystals are hydrogen bonds, one of the weakest chemical bonds known. Here we report a series of large-scale molecular dynamics simulations, revealing that β-sheet nanocrystals confined to a few nanometres achieve higher stiffness, strength and mechanical toughness than larger nanocrystals. We illustrate that through nanoconfinement, a combination of uniform shear deformation that makes most efficient use of hydrogen bonds and the emergence of dissipative molecular stick–slip deformation leads to significantly enhanced mechanical properties. Our findings explain how size effects can be exploited to create bioinspired materials with superior mechanical properties in spite of relying on mechanically inferior, weak hydrogen bonds.

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Figure 1: Hierarchical structure of spider silk, simulation set-up and theoretical considerations.
Figure 2: Snapshots of deformation profiles and failure mechanisms of silk β-sheet nanocrystals at different sizes.
Figure 3: Size dependence of the stiffness, and bending versus shear contributions as a function of β-sheet nanocrystal size.
Figure 4: Strength, toughness, resilience and strain distribution in β-sheet nanocrystals as a function of crystal size.
Figure 5: Hierarchical effects in the architecture of spider silk nanocrystals.

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References

  1. Becker, N. et al. Molecular nanosprings in spider capture-silk threads. Nature Mater. 2, 278–283 (2003).

    Article  CAS  Google Scholar 

  2. Shao, Z. Z. & Vollrath, F. Materials: Surprising strength of silkworm silk. Nature 418, 741–741 (2002).

    Article  CAS  Google Scholar 

  3. Vollrath, F. & Knight, D. P. Liquid crystalline spinning of spider silk. Nature 410, 541–548 (2001).

    Article  CAS  Google Scholar 

  4. Vepari, C. & Kaplan, D. L. Silk as a biomaterial. Prog. Polymer Sci. 32, 991–1007 (2007).

    Article  CAS  Google Scholar 

  5. Termonia, Y. Molecular modeling of spider silk elasticity. Macromolecules 27, 7378–7381 (1994).

    Article  CAS  Google Scholar 

  6. Du, N. et al. Design of superior spider silk: From nanostructure to mechanical properties. Biophys. J. 91, 4528–4535 (2006).

    Article  CAS  Google Scholar 

  7. Lee, S. M. et al. Greatly increased toughness of infiltrated spider silk. Science 324, 488–492 (2009).

    Article  CAS  Google Scholar 

  8. Rammensee, S., Slotta, U., Scheibel, T. & Bausch, A. R. Assembly mechanism of recombinant spider silk proteins. Proc. Natl Acad. Sci. USA 105, 6590–6595 (2008).

    Article  CAS  Google Scholar 

  9. Hayashi, C. Y., Shipley, N. H. & Lewis, R. V. Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. Int. J. Biol. Macromol. 24, 271–275 (1999).

    Article  CAS  Google Scholar 

  10. Lefevre, T., Rousseau, M. E. & Pezolet, M. Protein secondary structure and orientation in silk as revealed by Raman spectromicroscopy. Biophys. J. 92, 2885–2895 (2007).

    Article  CAS  Google Scholar 

  11. van Beek, J. D., Hess, S., Vollrath, F. & Meier, B. H. The molecular structure of spider dragline silk: Folding and orientation of the protein backbone. Proc. Natl Acad. Sci. USA 99, 10266–10271 (2002).

    Article  CAS  Google Scholar 

  12. Thiel, B. L., Guess, K. B. & Viney, C. Non-periodic lattice crystals in the hierarchical microstructure of spider (major ampullate) silk. Biopolymers 41, 703–719 (1997).

    Article  CAS  Google Scholar 

  13. Keten, S. & Buehler, M. J. Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale. Nano Lett. 8, 743–748 (2008).

    Article  CAS  Google Scholar 

  14. Keten, S. & Buehler, M. J. Asymptotic strength limit of hydrogen bond assemblies in proteins at vanishing pulling rates. Phys. Rev. Lett. 100, 198301 (2008).

    Article  Google Scholar 

  15. Rousseau, M. E., Lefevre, T., Beaulieu, L., Asakura, T. & Pezolet, M. Study of protein conformation and orientation in silkworm and spider silk fibers using Raman microspectroscopy. Biomacromolecules 5, 2247–2257 (2004).

    Article  CAS  Google Scholar 

  16. Grubb, D. T. & Jelinski, L. W. Fiber morphology of spider silk: The effects of tensile deformation. Macromolecules 30, 2860–2867 (1997).

    Article  CAS  Google Scholar 

  17. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M. & Gaub, H.E. Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276, 1109–1112 (1997).

    Article  CAS  Google Scholar 

  18. Lee, E. H., Gao, M., Pinotsis, N., Wilmanns, M. & Schulten, K. Mechanical strength of the titin Z1Z2-telethonin complex. Structure 14, 497–509 (2006).

    Article  CAS  Google Scholar 

  19. Marszalek, P. E. et al. Mechanical unfolding intermediates in titin modules. Nature 402, 100–103 (1999).

    Article  CAS  Google Scholar 

  20. Brockwell, D. J. et al. Pulling geometry defines the mechanical resistance of a beta-sheet protein. Nature Struct. Biol. 10, 731–737 (2003).

    Article  CAS  Google Scholar 

  21. Eom, K., Li, P. C., Makarov, D. E. & Rodin, G. J. Relationship between the mechanical properties and topology of cross-linked polymer molecules: Parallel strands maximize the strength of model polymers and protein domains. J. Phys. Chem. B 107, 8730–8733 (2003).

    Article  CAS  Google Scholar 

  22. Sulkowska, J. I. & Cieplak, M. Mechanical stretching of proteins—a theoretical survey of the Protein Data Bank. J. Phys. Condens. Matter 19, 283201 (2007).

    Article  Google Scholar 

  23. Buehler, M. J. & Yung, Y. C. Deformation and failure of protein materials in physiologically extreme conditions and disease. Nature Mater. 8, 175–188 (2009).

    Article  CAS  Google Scholar 

  24. Schwaiger, I., Sattler, C., Hostetter, D. R. & Rief, M. The myosin coiled-coil is a truly elastic protein structure. Nature Mater. 1, 232–235 (2002).

    Article  CAS  Google Scholar 

  25. Sotomayor, M. & Schulten, K. Single-molecule experiments in vitro and in silico. Science 316, 1144–1148 (2007).

    Article  CAS  Google Scholar 

  26. Ma, B. & Nussinov, R. Molecular dynamics simulations of the unfolding of beta(2)-microglobulin and its variants. Protein Eng. 16, 561–575 (2003).

    Article  CAS  Google Scholar 

  27. Brooks, C. L. Methodological advances in molecular-dynamics simulations of biological-systems. Curr. Opin. Struct. Biol. 5, 211–215 (1995).

    Article  CAS  Google Scholar 

  28. Fossey, S. A., Nemethy, G., Gibson, K. D. & Scheraga, H. A. Conformational energy studies of beta-sheets of model silk fibroin peptides 1. Sheets of poly(Ala–Gly) chains. Biopolymers 31, 1529–1541 (1991).

    Article  CAS  Google Scholar 

  29. Shao, Z. Z. & Vollrath, F. The effect of solvents on the contraction and mechanical properties of spider silk. Polymer 40, 1799–1806 (1999).

    Article  CAS  Google Scholar 

  30. Oroudjev, E. et al. Segmented nanofibers of spider dragline silk: Atomic force microscopy and single-molecule force spectroscopy. Proc. Natl Acad. Sci. USA 99, 6460–6465 (2002).

    Article  CAS  Google Scholar 

  31. Sirichaisit, J., Brookes, V. L., Young, R. J. & Vollrath, F. Analysis of structure/property relationships in silkworm (Bombyx mori) and spider dragline (Nephila edulis) silks using Raman spectroscopy. Biomacromolecules 4, 387–394 (2003).

    Article  CAS  Google Scholar 

  32. Pampaloni, F. et al. Thermal fluctuations of grafted microtubules provide evidence of a length-dependent persistence length. Proc. Natl Acad. Sci. USA 103, 10248–10253 (2006).

    Article  CAS  Google Scholar 

  33. Knowles, T. P. et al. Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318, 1900–1903 (2007).

    Article  CAS  Google Scholar 

  34. Connor, J. J. MIT-Prentice Hall Series on Civil, Environmental, and Systems Engineering xiv 53–56 (Prentice Hall Pearson Education, 2003).

    Google Scholar 

  35. Krasnov, I. et al. Mechanical properties of silk: Interplay of deformation on macroscopic and molecular length scales. Phys. Rev. Lett. 100, 048104 (2008).

    Article  Google Scholar 

  36. Philip, M. C. et al. Mechanical and thermal properties of dragline silk from the spider Nephila clavipes. Polym. Adv. Technol. 5, 401–410 (1994).

    Article  Google Scholar 

  37. Ko, F. K. & Jovicic, J. Modeling of mechanical properties and structural design of spider web. Biomacromolecules 5, 780–785 (2004).

    Article  CAS  Google Scholar 

  38. Keten, S. & Buehler, M. J. Strength limit of entropic elasticity in beta-sheet protein domains. Phys. Rev. E 78, 061913 (2008).

    Article  Google Scholar 

  39. Fratzl, P. & Weinkamer, R. Nature’s hierarchical materials. Prog. Mater. Sci. 52, 1263–1334 (2007).

    Article  CAS  Google Scholar 

  40. Hartmann, M. A. & Fratzl, P. Sacrificial ionic bonds need to be randomly distributed to provide shear deformability. Nano Lett. 9, 3603–3607 (2009).

    Article  CAS  Google Scholar 

  41. Keckes, J. et al. Cell-wall recovery after irreversible deformation of wood. Nature Mater. 2, 810–814 (2003).

    Article  CAS  Google Scholar 

  42. LeDuc, P. R. & Robinson, D. N. Using lessons from cellular and molecular structures for future materials. Adv. Mater. 19, 3761–3770 (2007).

    Article  CAS  Google Scholar 

  43. Gao, H. J., Ji, B. H., Jager, I. L., Arzt, E. & Fratzl, P. Materials become insensitive to flaws at nanoscale: Lessons from nature. Proc. Natl Acad. Sci. USA 100, 5597–5600 (2003).

    Article  CAS  Google Scholar 

  44. Porter, D. & Vollrath, F. The role of kinetics of water and amide bonding in protein stability. Soft Matter. 4, 328–336 (2008).

    Article  CAS  Google Scholar 

  45. Claessens, M. M. A. E., Bathe, M., Frey, E. & Bausch, A. R. Actin-binding proteins sensitively mediate F-actin bundle stiffness. Nature Mater. 5, 748–753 (2006).

    Article  CAS  Google Scholar 

  46. Xiao, S. B., Stacklies, W., Cetinkaya, M., Markert, B. & Grater, F. Mechanical response of silk crystalline units from force-distribution analysis. Biophys. J. 96, 3997–4005 (2009).

    Article  CAS  Google Scholar 

  47. Nelson, M. T. et al. NAMD: A parallel, object oriented molecular dynamics program. Int. J. Supercomputer Appl. High Performance Comput. 10, 251–268 (1996).

    Google Scholar 

  48. MacKerell, A. D. et al. All-atom empirical potential for molecular modelling and dynamics studies of proteins. J. Phys. Chem. B 102, 3586–3616 (1998).

    Article  CAS  Google Scholar 

  49. Perdew, J. P., Burke, K. & Ernzerhof, M. Generalized gradient approximation made simple. Phys. Rev. Lett. 77, 3865–3868 (1996).

    Article  CAS  Google Scholar 

  50. Soler, J. M. et al. The SIESTA method for ab initio order-N materials simulation. J. Phys. Condens. Matter 14, 2745–2779 (2002).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Office of Naval Research (N00014-08-1-00844). Further support from the National Science Foundation (CMMI-0642545 and MRSEC DMR-0819762), the Army Research Office (W911NF-06-1-0291), DARPA (HR0011-08-1-0067) and the MIT Energy Initiative is acknowledged. B.I. acknowledges support from MIT’s UROP and the MISTI-Germany programme. This research was supported by an allocation of advanced computing resources supported by the National Science Foundation (TeraGrid, grant no. TG-MSS080030). Further simulations have been carried out at MIT’s Laboratory for Atomistic and Molecular Mechanics. The authors thank J. J. Connor and T. Radford at MIT for fruitful discussions.

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Authors and Affiliations

  1. Department of Civil and Environmental Engineering, Laboratory for Atomistic and Molecular Mechanics, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Room 1-235A&B, Cambridge, Massachusetts 02139, USA

    Sinan Keten, Zhiping Xu, Britni Ihle & Markus J. Buehler

  2. Center for Materials Science and Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139, USA

    Zhiping Xu & Markus J. Buehler

  3. Center for Computational Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, Massachusetts 02139, USA

    Markus J. Buehler

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  1. Sinan Keten
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Contributions

S.K. and M.J.B. designed the research and analysed the results. S.K., Z.X. and B.I. carried out atomistic and molecular simulations. S.K., Z.X. and M.J.B. wrote the paper.

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Correspondence to Markus J. Buehler.

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Keten, S., Xu, Z., Ihle, B. et al. Nanoconfinement controls stiffness, strength and mechanical toughness of β-sheet crystals in silk. Nature Mater 9, 359–367 (2010). https://doi.org/10.1038/nmat2704

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