Skip to main content
Log in

In situ transmission electron microscopy observation of reversible deformation in nacre organic matrix

  • Published:
Journal of Materials Research Aims and scope Submit manuscript

Abstract

The deformation behavior of the organic polymer matrix of the biocomposite nacre structure in abalone shell was investigated by in situ straining during transmission electron microscopy (TEM). We observed strong adhesion to mineral plates and high ductility of the organic matrix, confirming a crack-bridging toughening mechanism. In addition, direct observation of reversible mechanical behavior was made in the viscoelastic reformation of matrix ligaments after failure. Crystalline β-sheet structures identified through electron diffraction suggested the presence of protein structures similar to spider or cocoon silk, and the reversible mechanism was attributed to hydration-induced unfolding and refolding of domains in these silklike proteins. This work provides further insight into the molecular and nanoscale behavior of nacre organic matrix and its contribution to bulk mechanical performance.

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.

FIG. 1
FIG. 2
FIG. 3
FIG. 4
FIG. 5

Similar content being viewed by others

References

  1. G. Mayer: Rigid biological systems as models for synthetic composites. Science 310, 1144 2005

    Article  CAS  Google Scholar 

  2. M. Sarikaya: An introduction to biomimetics: A structural viewpoint. Microsc. Res. Tech. 27, 360 1994

    Article  CAS  Google Scholar 

  3. A.P. Jackson, J.F.V. Vincent R.M. Tuner: The mechanical design of nacre. Proc. R. Soc. London B Biol. Sci. 234, 415 1988

    Article  Google Scholar 

  4. J.D. Currey: Mechanical properties of mother of pearl in compression. Proc. R. Soc. London B Biol. Sci. 196, 443 1977

    Article  Google Scholar 

  5. R. Menig, M.H. Meyers, M.A. Meyers K.S. Vecchio: Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells. Acta Mater. 48, 2383 2000

    Article  CAS  Google Scholar 

  6. F. Song, A.K. Soh Y.L. Bai: Structural and mechanical properties of the organic matrix layers of nacre. Biomaterials 24, 3623 2003

    Article  CAS  Google Scholar 

  7. R.Z. Wang, Z. Suo, A.G. Evans, N. Yao I.A. Aksay: Deformation mechanisms in nacre. J. Mater. Res. 16, 2485 2001

    Article  CAS  Google Scholar 

  8. R.Z. Wang, H.B. Wen, F.Z. Cui, H.B. Zhang H.D. Li: Observations of damage morphologies in nacre during deformation and fracture. J. Mater. Sci. 30, 2299 1995

    Article  CAS  Google Scholar 

  9. F. Barthelat, C-M. Li, C. Comi H.D. Espinosa: Mechanical properties of nacre constituents and their impact on mechanical performance. J. Mater. Res. 21, 1977 2006

    Article  CAS  Google Scholar 

  10. A.G. Evans, Z. Suo, R.Z. Wang, I.A. Aksay, M.Y. He J.W. Hutchinson: Model for the robust mechanical behaviour of nacre. J. Mater. Res. 16, 2475 2001

    Article  CAS  Google Scholar 

  11. M.A. Meyers, A.Y.-M. Lin, P.-Y. Chen J. Muyco: Mechanical strength of abalone nacre: Role of the soft organic layer. J. Mech. Behavior Biomed. Mater. 1 2008

  12. T.E. Schäffer, C. Ionescu-Zanetti, R. Proksch, M. Fritz, D.A. Walters, N. Almqvist, C.M. Zaremba, A.M. Belcher, B.L. Smith, G.D. Stucky, D.E. Morse P.K. Hansma: Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chem. Mater. 9, 1731 1997

    Article  Google Scholar 

  13. K.S. Katti, D.R. Katti, S.M. Pradhan A. Bhosle: Platelet interlocks are the key to toughness and strength in nacre. J. Mater. Res. 20, 1097 2005

    Article  CAS  Google Scholar 

  14. B.L. Smith, T.E. Schäffer, M. Viani, J.B. Thompson, N.A. Frederick, J. Kindt, A.M. Belcher, G.D. Stucky, D.E. Morse P.K. Hansma: Molecular mechanistic origin of natural adhesives, fibres and composites. Nature 399, 761 1999

    Article  CAS  Google Scholar 

  15. B. Ji H. Gao: Mechanical properties of nanostructure of biological materials. J. Mech. Phys. Solids 52, 1963 2004

    Article  Google Scholar 

  16. P.K.V.V. Nukala S. Simunovic: A continuous damage random thresholds model for simulating the fracture behavior of nacre. Biomaterials 26, 6087 2005

    Article  CAS  Google Scholar 

  17. N.M. Neves J.F. Mano: Structure/mechanical behavior relationships in crossed-lamellar sea shells. Mater. Sci. Eng., C 25, 113 2005

    Article  CAS  Google Scholar 

  18. L. Addadi, D. Joester, F. Nudelman S. Weiner: Mollusk shell formation: A source of new concepts for understanding biomineralization processes. Chem. Eur. J. 12, 980 2006

    Article  CAS  Google Scholar 

  19. G. Bevelander H. Nakahara: An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs. Calcif. Tissue Res. 3, 84 1969

    Article  CAS  Google Scholar 

  20. A. Williams: Growth and structure of the shell of living articulate brachiopods. Nature 211, 1146 1966

    Article  Google Scholar 

  21. A.M. Belcher, X.H. Wu, R.J. Christensen, P.K. Hansma, G.D. Stucky D.E. Morse: Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature 381, 56 1996

    Article  CAS  Google Scholar 

  22. Q.L. Feng, G. Pu, Y. Pei, F.Z. Cui, H.D. Li T.N. Kim: Polymorph and morphology of calcium carbonate crystals induced by proteins extracted from mollusk shell. J. Cryst. Growth 216, 459 2000

    Article  CAS  Google Scholar 

  23. J.B. Thompson, G.T. Paloczi, J.H. Kindt, M. Michenfelder, B.L. Smith, G. Stucky, D.E. Morse P.K. Hansma: Direct observation of the transition from calcite to aragonite growth as induced by abalone shell proteins. Biophys. J. 79(6), 3307 2000

    Article  CAS  Google Scholar 

  24. A.P. Wheeler, J.W. George C.A. Evans: Control of calcium carbonate nucleation and crystal growth by soluble matrix of oyster shell. Science 212, 1397 1981

    Article  CAS  Google Scholar 

  25. S. Weiner W. Traub: Macromolecules in mollusc shells and their functions in biomineralization. Philos. Trans. R. Soc. London B Biol. Sci. 304, 425 1984

    Article  CAS  Google Scholar 

  26. X. Shen, A.M. Belcher, P.K. Hansma, G.D. Stucky D.E. Morse: Molecular cloning and characterization of Lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens. J. Biol. Chem. 272, 32472 1997

    Article  CAS  Google Scholar 

  27. S. Weiner W. Traub: X-ray diffraction study of the insoluble organic matrix of mollusk shells. FEBS Lett. 111, 311 1980

    Article  CAS  Google Scholar 

  28. S. Sudo, T. Fujikawa, T. Nagakura, T. Ohkubo, K. Sakaguchi, M. Tanaka, K. Nakashima T. Takahashi: Structures of mollusc shell framework proteins. Nature 387, 563 1997

    Article  CAS  Google Scholar 

  29. P. Ghosh, D.R. Katti K.S. Katti: Impact of β-sheet conformations on the mechanical response of protein in biocomposites. Mater. Manuf. Process. 21, 676 2006

    Article  CAS  Google Scholar 

  30. P. Ghosh, D.R. Katti K.S. Katti: Mineral proximity influences mechanical response of proteins in biological mineral-protein hybrid systems. Biomacromolecules 8, 851 2007

    Article  CAS  Google Scholar 

  31. E. Bini, D.P. Knight D.L. Kaplan: Mapping domain structures in silks from insects and spiders related to protein assembly. J. Mol. Biol. 335, 27 2004

    Article  CAS  Google Scholar 

  32. C. Dicko, D.P. Knight, J.M. Kennedy F. Vollrath: Conformational polymorphism, stability and aggregation in spider dragline silks proteins. Int. J. Biol. Macromol. 36, 215 2005

    Article  CAS  Google Scholar 

  33. H-J. Jin D.L. Kaplan: Mechanism of silk processing in insects and spiders. Nature 424, 1057 2003

    Article  CAS  Google Scholar 

  34. J.M. Gosline, M.W. Denny M.E. DeMont: Spider silk as rubber. Nature 309, 551 1984

    Article  CAS  Google Scholar 

  35. E. Oroudjev, J. Soares, S. Arcidiacono, J.B. Thompson, S.A. Fossey H.G. Hansma: Segmented nanofibers of spider dragline silk: Atomic force microscopy and single-molecule force microscopy. Proc. Natl. Acad. Sci. USA 99, 6460 2002

    Article  CAS  Google Scholar 

  36. H. Shulha, C.W.P. Foo, D.L. Kaplan V.V. Tsukruk: Unfolding the multi-length scale domain structure of silk fibroin protein. Polymer 47, 5821 2006

    Article  CAS  Google Scholar 

  37. M. Xu R.V. Lewis: Structure of a protein superfiber: Spider dragline silk. Proc. Natl. Acad. Sci. USA 87, 7120 1990

    Article  CAS  Google Scholar 

  38. B. Mohanty, K.S. Katti, D.R. Katti D. Verma: Dynamical nanomechanical response of nacre. J. Mater. Res. 21, 2045 2006

    Article  CAS  Google Scholar 

  39. T. Sumitomo, H. Kakisawa, Y. Owaki Y. Kagawa: Deformation mechanisms of natural nano-laminar composites: Direct TEM observation of organic matrix in nacre in Proceedings of the 31st International Conference on Advanced Ceramics and Composites, edited by J. Salem and D. Zhu John Wiley and Sons Hoboken, NJ 2007

  40. G.E. Fantner, T. Hassenkam, J. Kindt, J.C. Weaver, H. Birkedal, L. Pechnik, G.A.G. Cidade, G.D. Stucky, D.E. Morse P.K. Hansma: Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat. Mater. 4, 612 2005

    Article  CAS  Google Scholar 

  41. J.B. Thompson, J.H. Kindt, B. Drake, H.G. Hansma, D.E. Morse P.K. Hansma: Bone indentation recovery time correlates with bond reforming time. Nature 414, 773 2001

    Article  CAS  Google Scholar 

  42. N. Becker, E. Oroudjev, S. Mutz, J.P. Cleveland, P.K. Hansma, C.Y. Hayashi, D.E. Makarov H.G. Hansma: Molecular nanosprings in spider capture-silk threads. Nat. Mater. 2, 278 2003

    Article  CAS  Google Scholar 

  43. G.E. Fantner, E. Oroudjev, G. Schitter, L.S. Golde, P. Thurner, M.M. Finch, P. Turner, T. Gutsmann, D.E. Morse, H. Hansma P.K. Hansma: Sacrificial bonds and hidden length: Unraveling molecular mesostructures in tough materials. Biophys. J. 90, 1411 2006

    Article  CAS  Google Scholar 

  44. J.D. van Beek, S. Hess, F. Vollrath B.H. Meier: The molecular structure of spider dragline silk: Folding and orientation of the protein backbone. Proc. Natl. Acad. Sci. USA 99(16), 10266 2002

    Article  CAS  Google Scholar 

  45. D.W. Urry: Physical chemistry of biological free energy transduction as demonstrated by elastic protein-based polymers. J. Phys. Chem. 101, 11007 1997

    Article  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (No.16760555).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Taro Sumitomo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sumitomo, T., Kakisawa, H., Owaki, Y. et al. In situ transmission electron microscopy observation of reversible deformation in nacre organic matrix. Journal of Materials Research 23, 1466–1471 (2008). https://doi.org/10.1557/JMR.2008.0184

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1557/JMR.2008.0184

Navigation