Skip to main content
Log in

Multiscale mechanics of biological and biologically inspired materials and structures

  • Published:
Acta Mechanica Solida Sinica Aims and scope Submit manuscript

Abstract

The world of natural materials and structures provides an abundance of applications in which mechanics is a critical issue for our understanding of functional material properties. In particular, the mechanical properties of biological materials and structures play an important role in virtually all physiological processes and at all scales, from the molecular and nanoscale to the macroscale, linking research fields as diverse as genetics to structural mechanics in an approach referred to as materiomics. Example cases that illustrate the importance of mechanics in biology include mechanical support provided by materials like bone, the facilitation of locomotion capabilities by muscle and tendon, or the protection against environmental impact by materials as the skin or armors. In this article we review recent progress and case studies, relevant for a variety of applications that range from medicine to civil engineering. We demonstrate the importance of fundamental mechanistic insight at multiple time- and length-scales to arrive at a systematic understanding of materials and structures in biology, in the context of both physiological and disease states and for the development of de novo biomaterials. Three particularly intriguing issues that will be discussed here include: First, the capacity of biological systems to turn weakness to strength through the utilization of multiple structural levels within the universality-diversity paradigm. Second, material breakdown in extreme and disease conditions. And third, we review an example where the hierarchical design paradigm found in natural protein materials has been applied in the development of a novel biomaterial based on amyloid protein.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Alberts, B., Johnson, A., Lewis, J., Raff, M., Roberts, K. and Walter, P., Molecular Biology of the Cell. New York: Taylor & Francis, 2002.

    Google Scholar 

  2. Fratzl, P. and Weinkamer, R., Nature’s hierarchical materials. Progress in Materials Science, 2007, 52: 1263–1334.

    Article  Google Scholar 

  3. Meyers, M.A., Chen, P.Y., Lin, A.Y.M. and Seki, Y., Biological materials: Structure and mechanical properties. Progress in Materials Science, 2008, 53(1): 1–206.

    Article  Google Scholar 

  4. Lakes, R., Materials with structural hierarchy. Nature, 1993, 361(6412): 511–515.

    Article  Google Scholar 

  5. Buehler, M.J., Tu(r)ning weakness to strength. Nano Today, 2010, 5(5): 379–383.

    Article  Google Scholar 

  6. Buehler, M.J. and Yung, Y.C., Deformation and failure of protein materials in physiologically extreme conditions and disease. Nature Materials, 2009, 8(3): 175–188.

    Article  Google Scholar 

  7. Buehler, M.J. and Yung, Y.C., How protein materials balance strength, robustness and adaptability. HFSP Journal, 2010, 4(1): 26–40.

    Article  Google Scholar 

  8. Cranford, S. and Buehler, M.J., Materiomics: biological protein materials, from nano to macro. Journal of Nanotechnology, Science and Applications, 2010, 3: 127–148.

    Google Scholar 

  9. Buehler, M.J., Strength in numbers. Nature Nanotechnology, 2010, 5(3): 172–174.

    Article  Google Scholar 

  10. Paparcone, R., Cranford, S.W. and Buehler, M.J., Self-folding and aggregation of amyloid fibrils. in submission.

  11. Buehler, M.J. and Keten, S., Failure of molecules, bones, and the earth itself. Reviews of Modern Physics, 2010, 82: 1459–1487.

    Article  Google Scholar 

  12. Prockop, D.J. and Kivirikko, K.I., Collagens: molecular biology, diseases, and potentials for therapy. Annual Review of Biochemistry, 1995, 64: 403–434.

    Article  Google Scholar 

  13. Byers, P.H., Wallis, G.A. and Willing, M.C., Osteogenesis imperfecta: translation of mutation to phenotype. Journal of Medical Genetics, 1991, 28(7): 433–442.

    Article  Google Scholar 

  14. Gautieri, A., Vesentini, S., Redaelli, A. and Buehler, M.J., Single molecule effects of osteogenesis imperfecta mutations in tropocollagen protein domains. Protein Science, 2009, 18(1): 161–168.

    Google Scholar 

  15. Gautieri, A., Uzel, S., Vesentini, S., Redaelli, A. and Buehler, M.J., Molecular and mesoscale mechanisms of osteogenesis imperfecta disease in collagen fibrils. Biophysical Journal, 2009, 97(3): 857–865.

    Article  Google Scholar 

  16. Hudson, B.G., Tryggvason, K., Sundaramoorthy, M. and Neilson, E.G., Alport’s syndrome, goodpasture’s syndrome, and type IV collagen. New England Journal of Medicine, 2003, 348(25): 2543–2556.

    Article  Google Scholar 

  17. Godsel, L.M., Hobbs, R.P. and Green, K.J., Intermediate filament assembly: dynamics to disease. Trends in Cell Biology, 2008, 18(1): 28–37.

    Article  Google Scholar 

  18. Buehler, M.J., Atomistic Modeling of Materials Failure. New York: Springer, 2008.

    Book  Google Scholar 

  19. Dahl, K.N., Kahn, S.M., Wilson, K.L. and Discher, D.E., The nuclear envelope lamina network has elasticity and a compressibility limit suggestive of a molecular shock absorber. Journal of Cell Science, 2004, 117(20): 4779–4786.

    Article  Google Scholar 

  20. Gumbsch, P., Riedle, J., Hartmaier, A. and Fischmeister, H.F., Controlling factors for the brittle-to-ductile transition in Tungsten single crystals. Science, 1998, 282(5392): 1293–1295.

    Article  Google Scholar 

  21. Dietz, H. and Rief, M., Elastic bond network model for protein unfolding mechanics. Physical Review Letters, 2008, 100(9): 4.

    Article  Google Scholar 

  22. Rauch, F. and Glorieux, F.H., Osteogenesis imperfecta. Lancet, 2004, 363(9418): 1377–1385.

    Article  Google Scholar 

  23. Miller, E., Delos, D., Baldini, T., Wright, T.M. and Camacho, N.P., Abnormal mineral-matrix interactions are a significant contributor to fragility in oim/oim bone. Calcified Tissue International, 2007, 81(3): 206–214.

    Article  Google Scholar 

  24. Buehler, M.J. and Keten, S., Elasticity, strength and resilience: A comparative study on mechanical signatures of α-helix, β-sheet and tropocollagen domains. Nano Research, 2008, 1(1): 63–71.

    Article  Google Scholar 

  25. Buehler, M.J., Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. Roceedings Of the National Academy of Sciences of the United States of America, 2006, 103(33): 12285–12290.

    Article  Google Scholar 

  26. Gao, H., Ji, B., Jäger, I.L., Arzt, E. and Fratzl, P., Materials become insensitive to flaws at nanoscale: lessons from nature. Roceedings of the National Academy of Sciences of the United States of America, 2003, 100(10): 5597–5600.

    Article  Google Scholar 

  27. Hamm, C.E., Merkel, R., Springer, O., Jurkojc, P., Maier, C., Prechtel, K. and Smetacek, V., Architecture and material properties of diatom shells provide effective mechanical protection. Nature, 2003, 421(6925): 841–843.

    Article  Google Scholar 

  28. Garcia, A.P., Sen, D., and Buehler, M.J., Hierarchical silica nanostructures inspired by diatom algae yield superior deformability, toughness and strength. Metallurgical and Materials Transactions A-Physical Metallurgy and Materials Science, 2010, Doi: 10.1007/s11661-010-0477-y.

    Article  Google Scholar 

  29. Garcia, A.P. and Buehler, M.J., Bioinspired nanoporous silicon provides great toughness at great deformability. Computational Materials Science, 2010, 48(2): 303–309.

    Article  Google Scholar 

  30. Cranford, S. and Buehler, M.J., Mechanomutable carbon nanotube arrays. International Journal of Material and Structural Integrity, 2009, 3(2–3): 161–178.

    Article  Google Scholar 

  31. Trotter, J.A., Tipper, J., Lyons-Levy, G., Chino, K., Heuer, A.H., Liu, Z., Mrksich, M., Hodneland, C., Dillmore, W.S., Koob, T.J., Koob-Emunds, M.M., Kadler, K. and Holmes, D., Towards a fibrous composite with dynamically controlled stiffness: lessons from echinoderms. Biochemistry Society Transactions, 2000, 28(4): 357–362.

    Article  Google Scholar 

  32. Schmidt, D.J., Cebeci, F.C., Kalcioglu, Z.I., Wyman, S.G., Ortiz, C., Van Vliet, K.J. and Hammond, P.T., Electrochemically controlled swelling and mechanical properties of a polymer nanocomposite. ACS Nano, 2009, 3(8): 2207–2216.

    Article  Google Scholar 

  33. Cranford, S., Ortiz, C. and Buehler, M.J., Mechanomutable properties of a PAA/PAH polyelectrolyte complex: rate dependence and ionization effects on tunable adhesion strength. Soft Matter, 2010, 6: 4175–4188.

    Article  Google Scholar 

  34. Vollrath, F. and Porter, D., Spider silk as archetypal protein elastomer. Soft Matter, 2006, 2(5): 377–385.

    Article  Google Scholar 

  35. Rammensee, S., Slotta, U., Scheibel, T. and Bausch, A.R., Assembly mechanism of recombinant spider silk proteins. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(18): 6590–6595.

    Article  Google Scholar 

  36. Keten, S., Xu, Z., Ihle, B. and Buehler, M.J., Nanoconfinement controls stiffness, strength and mechanical toughness of beta-sheet crystals in silk. Nature Materials, 2010, 9(4): 359–367.

    Article  Google Scholar 

  37. Keten, S. and Buehler, M.J., Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale. Nano Letters, 2008, 8(2): 743–748.

    Article  Google Scholar 

  38. Nova, A., Keten, S., Pugno, N.M., Redaelli, A. and Buehler, M.J., Molecular and nanostructural mechanisms of deformation, strength and toughness of spider silk fibrils. Nano Letters, 2010, 10(7): 2626–2634.

    Article  Google Scholar 

  39. Xu, Z. and Buehler, M.J., Mechanical energy transfer and dissipation in fibrous beta-sheet-rich proteins. Physical Review E, 2010, 81: 061910.

    Article  Google Scholar 

  40. Keten, S. and Buehler, M.J., Nanostructure and molecular mechanics of spider dragline silk protein assemblies. Journal of the Royal Society Interface, 2010, 7(53): 1709–1721.

    Article  Google Scholar 

  41. Knowles, T.P.J., Oppenheim, T., Buell, A.K., Chirgadze, D.Y. and Welland, M.E., Nanostructured biofilms from hierarchical self-assembly of amyloidogenic proteins. Nature Nanotechnology, 2010, 5: 204–207.

    Article  Google Scholar 

  42. Chiti, F. and Dobson, C.M., Protein misfolding, functional amyloid, and human disease. Annual Review of Biochemistry, 2006, 75: 333–366.

    Article  Google Scholar 

  43. Mostaert, A.S., Giordani, C., Crockett, R., Karsten, U., Schumann, R. and Jarvis, S.P., Characterisation of amyloid nanostructures in the natural adhesive of unicellular subaerial algae. Journal of Adhesion, 2009, 85(8): 465–483.

    Article  Google Scholar 

  44. Ackbarow, T., Sen, D., Thaulow, C. and Buehler, M.J., Alpha-helical protein networks are self protective and flaw tolerant. PLoS ONE, 2009, 4(6): e6015.

    Article  Google Scholar 

  45. Kamien, R., Music: An Appreciation. McGraw-Hill Humanities/Social Sciences/Languages, 2007.

  46. Dodge, C. and Jerse, T.A., Computer Music: synthesis, Composition, and Performance. Cengage Learning, 1997.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Markus J. Buehler.

Additional information

Project supported by NSF, ARO, AFOSR and ONR. Additional support from DARPA and the MITEI is acknowledged.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buehler, M.J. Multiscale mechanics of biological and biologically inspired materials and structures. Acta Mech. Solida Sin. 23, 471–483 (2010). https://doi.org/10.1016/S0894-9166(11)60001-3

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/S0894-9166(11)60001-3

Key words

Navigation