Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-17T18:21:34.240Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  31 January 2011

Taro Sumitomo*
Affiliation:
National Institute for Materials Science, Tsukuba, Ibaraki 305-0047, Japan
Hideki Kakisawa
Affiliation:
National Institute for Materials Science, Tsukuba, Ibaraki 305-0047, Japan
Yusuke Owaki
Affiliation:
Research Center for Advanced Science and Technology, University of Tokyo, Meguro, Tokyo 153-8904, Japan
Yutaka Kagawa
Affiliation:
Research Center for Advanced Science and Technology, University of Tokyo, Meguro, Tokyo 153-8904, Japan
*
a)Address all correspondence to this author. e-mail: [email protected]
Get access

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.

Type
Articles
Copyright
Copyright © Materials Research Society 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

1Mayer, G.: Rigid biological systems as models for synthetic composites. Science 310, 1144 2005CrossRefGoogle ScholarPubMed
2Sarikaya, M.: An introduction to biomimetics: A structural viewpoint. Microsc. Res. Tech. 27, 360 1994CrossRefGoogle ScholarPubMed
3Jackson, A.P., Vincent, J.F.V.Tuner, R.M.: The mechanical design of nacre. Proc. R. Soc. London B Biol. Sci. 234, 415 1988Google Scholar
4Currey, J.D.: Mechanical properties of mother of pearl in compression. Proc. R. Soc. London B Biol. Sci. 196, 443 1977Google Scholar
5Menig, R., Meyers, M.H., Meyers, M.A.Vecchio, K.S.: Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells. Acta Mater. 48, 2383 2000CrossRefGoogle Scholar
6Song, F., Soh, A.K.Bai, Y.L.: Structural and mechanical properties of the organic matrix layers of nacre. Biomaterials 24, 3623 2003CrossRefGoogle ScholarPubMed
7Wang, R.Z., Suo, Z., Evans, A.G., Yao, N.Aksay, I.A.: Deformation mechanisms in nacre. J. Mater. Res. 16, 2485 2001CrossRefGoogle Scholar
8Wang, R.Z., Wen, H.B., Cui, F.Z., Zhang, H.B.Li, H.D.: Observations of damage morphologies in nacre during deformation and fracture. J. Mater. Sci. 30, 2299 1995CrossRefGoogle Scholar
9Barthelat, F., Li, C-M., Comi, C.Espinosa, H.D.: Mechanical properties of nacre constituents and their impact on mechanical performance. J. Mater. Res. 21, 1977 2006CrossRefGoogle Scholar
10Evans, A.G., Suo, Z., Wang, R.Z., Aksay, I.A., He, M.Y.Hutchinson, J.W.: Model for the robust mechanical behaviour of nacre. J. Mater. Res. 16, 2475 2001CrossRefGoogle Scholar
11Meyers, M.A., Lin, A.Y.-M., Chen, P.-Y.Muyco, J.: Mechanical strength of abalone nacre: Role of the soft organic layer. J. Mech. Behavior Biomed. Mater. 1 2008CrossRefGoogle ScholarPubMed
12Schäffer, T.E., Ionescu-Zanetti, C., Proksch, R., Fritz, M., Walters, D.A., Almqvist, N., Zaremba, C.M., Belcher, A.M., Smith, B.L., Stucky, G.D., Morse, D.E.Hansma, P.K.: Does abalone nacre form by heteroepitaxial nucleation or by growth through mineral bridges? Chem. Mater. 9, 1731 1997CrossRefGoogle Scholar
13Katti, K.S., Katti, D.R., Pradhan, S.M.Bhosle, A.: Platelet interlocks are the key to toughness and strength in nacre. J. Mater. Res. 20, 1097 2005CrossRefGoogle Scholar
14Smith, B.L., Schäffer, T.E., Viani, M., Thompson, J.B., Frederick, N.A., Kindt, J., Belcher, A.M., Stucky, G.D., Morse, D.E.Hansma, P.K.: Molecular mechanistic origin of natural adhesives, fibres and composites. Nature 399, 761 1999CrossRefGoogle Scholar
15Ji, B.Gao, H.: Mechanical properties of nanostructure of biological materials. J. Mech. Phys. Solids 52, 1963 2004CrossRefGoogle Scholar
16Nukala, P.K.V.V.Simunovic, S.: A continuous damage random thresholds model for simulating the fracture behavior of nacre. Biomaterials 26, 6087 2005CrossRefGoogle ScholarPubMed
17Neves, N.M.Mano, J.F.: Structure/mechanical behavior relationships in crossed-lamellar sea shells. Mater. Sci. Eng., C 25, 113 2005CrossRefGoogle Scholar
18Addadi, L., Joester, D., Nudelman, F.Weiner, S.: Mollusk shell formation: A source of new concepts for understanding biomineralization processes. Chem. Eur. J. 12, 980 2006CrossRefGoogle ScholarPubMed
19Bevelander, G.Nakahara, H.: An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs. Calcif. Tissue Res. 3, 84 1969CrossRefGoogle ScholarPubMed
20Williams, A.: Growth and structure of the shell of living articulate brachiopods. Nature 211, 1146 1966CrossRefGoogle Scholar
21Belcher, A.M., Wu, X.H., Christensen, R.J., Hansma, P.K., Stucky, G.D.Morse, D.E.: Control of crystal phase switching and orientation by soluble mollusc-shell proteins. Nature 381, 56 1996CrossRefGoogle Scholar
22Feng, Q.L., Pu, G., Pei, Y., Cui, F.Z., Li, H.D.Kim, T.N.: Polymorph and morphology of calcium carbonate crystals induced by proteins extracted from mollusk shell. J. Cryst. Growth 216, 459 2000CrossRefGoogle Scholar
23Thompson, J.B., Paloczi, G.T., Kindt, J.H., Michenfelder, M., Smith, B.L., Stucky, G., Morse, D.E.Hansma, P.K.: Direct observation of the transition from calcite to aragonite growth as induced by abalone shell proteins. Biophys. J. 79(6), 3307 2000CrossRefGoogle ScholarPubMed
24Wheeler, A.P., George, J.W.Evans, C.A.: Control of calcium carbonate nucleation and crystal growth by soluble matrix of oyster shell. Science 212, 1397 1981CrossRefGoogle ScholarPubMed
25Weiner, S.Traub, W.: Macromolecules in mollusc shells and their functions in biomineralization. Philos. Trans. R. Soc. London B Biol. Sci. 304, 425 1984Google Scholar
26Shen, X., Belcher, A.M., Hansma, P.K., Stucky, G.D.Morse, D.E.: Molecular cloning and characterization of Lustrin A, a matrix protein from shell and pearl nacre of Haliotis rufescens. J. Biol. Chem. 272, 32472 1997CrossRefGoogle ScholarPubMed
27Weiner, S.Traub, W.: X-ray diffraction study of the insoluble organic matrix of mollusk shells. FEBS Lett. 111, 311 1980CrossRefGoogle Scholar
28Sudo, S., Fujikawa, T., Nagakura, T., Ohkubo, T., Sakaguchi, K., Tanaka, M., Nakashima, K.Takahashi, T.: Structures of mollusc shell framework proteins. Nature 387, 563 1997CrossRefGoogle ScholarPubMed
29Ghosh, P., Katti, D.R.Katti, K.S.: Impact of β-sheet conformations on the mechanical response of protein in biocomposites. Mater. Manuf. Process. 21, 676 2006CrossRefGoogle Scholar
30Ghosh, P., Katti, D.R.Katti, K.S.: Mineral proximity influences mechanical response of proteins in biological mineral-protein hybrid systems. Biomacromolecules 8, 851 2007CrossRefGoogle ScholarPubMed
31Bini, E., Knight, D.P.Kaplan, D.L.: Mapping domain structures in silks from insects and spiders related to protein assembly. J. Mol. Biol. 335, 27 2004CrossRefGoogle ScholarPubMed
32Dicko, C., Knight, D.P., Kennedy, J.M.Vollrath, F.: Conformational polymorphism, stability and aggregation in spider dragline silks proteins. Int. J. Biol. Macromol. 36, 215 2005CrossRefGoogle ScholarPubMed
33Jin, H-J.Kaplan, D.L.: Mechanism of silk processing in insects and spiders. Nature 424, 1057 2003CrossRefGoogle ScholarPubMed
34Gosline, J.M., Denny, M.W.DeMont, M.E.: Spider silk as rubber. Nature 309, 551 1984CrossRefGoogle Scholar
35Oroudjev, E., Soares, J., Arcidiacono, S., Thompson, J.B., Fossey, S.A.Hansma, H.G.: Segmented nanofibers of spider dragline silk: Atomic force microscopy and single-molecule force microscopy. Proc. Natl. Acad. Sci. USA 99, 6460 2002CrossRefGoogle Scholar
36Shulha, H., Foo, C.W.P., Kaplan, D.L.Tsukruk, V.V.: Unfolding the multi-length scale domain structure of silk fibroin protein. Polymer 47, 5821 2006CrossRefGoogle Scholar
37Xu, M.Lewis, R.V.: Structure of a protein superfiber: Spider dragline silk. Proc. Natl. Acad. Sci. USA 87, 7120 1990CrossRefGoogle ScholarPubMed
38Mohanty, B., Katti, K.S., Katti, D.R.Verma, D.: Dynamical nanomechanical response of nacre. J. Mater. Res. 21, 2045 2006CrossRefGoogle Scholar
39Sumitomo, T., Kakisawa, H., Owaki, Y.Kagawa, Y.: 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 2007Google Scholar
40Fantner, G.E., Hassenkam, T., Kindt, J., Weaver, J.C., Birkedal, H., Pechnik, L., Cidade, G.A.G., Stucky, G.D., Morse, D.E.Hansma, P.K.: Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat. Mater. 4, 612 2005CrossRefGoogle ScholarPubMed
41Thompson, J.B., Kindt, J.H., Drake, B., Hansma, H.G., Morse, D.E.Hansma, P.K.: Bone indentation recovery time correlates with bond reforming time. Nature 414, 773 2001CrossRefGoogle ScholarPubMed
42Becker, N., Oroudjev, E., Mutz, S., Cleveland, J.P., Hansma, P.K., Hayashi, C.Y., Makarov, D.E.Hansma, H.G.: Molecular nanosprings in spider capture-silk threads. Nat. Mater. 2, 278 2003CrossRefGoogle ScholarPubMed
43Fantner, G.E., Oroudjev, E., Schitter, G., Golde, L.S., Thurner, P., Finch, M.M., Turner, P., Gutsmann, T., Morse, D.E., Hansma, H.Hansma, P.K.: Sacrificial bonds and hidden length: Unraveling molecular mesostructures in tough materials. Biophys. J. 90, 1411 2006CrossRefGoogle ScholarPubMed
44van 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(16), 10266 2002CrossRefGoogle ScholarPubMed
45Urry, D.W.: Physical chemistry of biological free energy transduction as demonstrated by elastic protein-based polymers. J. Phys. Chem. 101, 11007 1997CrossRefGoogle Scholar