Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T14:54:36.103Z Has data issue: false hasContentIssue false
  • English
  • Français

Matrix-Mediated Biomineralization in Marine Mollusks: A Combined Transmission Electron Microscopy and Focused Ion Beam Approach

Published online by Cambridge University Press:  04 March 2011

Martin Saunders ,
Charlie Kong ,
Jeremy A. Shaw  and
Peta L. Clode
Martin Saunders*
Affiliation:
Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Crawley, Perth, WA 6009, Australia
Charlie Kong
Affiliation:
Electron Microscopy Unit, University of New South Wales, Sydney, NSW 2052, Australia
Jeremy A. Shaw
Affiliation:
Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Crawley, Perth, WA 6009, Australia
Peta L. Clode
Affiliation:
Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, Crawley, Perth, WA 6009, Australia
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

The teeth of the marine mollusk Acanthopleura hirtosa are an excellent example of a complex, organic, matrix-mediated biomineral, with the fully mineralized teeth comprising layers of iron oxide and iron oxyhydroxide minerals around a calcium apatite core. To investigate the relationship between the various mineral layers and the organic matrix fibers on which they grew, sections have been prepared from specific features in the teeth at controlled orientations using focused ion beam processing. Compositional and microstructural details of heterophase interfaces, and the fate of the organic matrix fibers within the mineral layers, can then be analyzed by a range of transmission electron microscopy (TEM) techniques. Energy-filtered TEM highlights the interlocking nature of the various mineral phases, while high-angle annular dark-field scanning TEM imaging demonstrates that the organic matrix continues to exist in the fully mineralized teeth. These new insights into the structure of this complex biomaterial are an important step in understanding the relationship between its structural and physical properties and may help explain its high strength and crack-resistance behavior.

Keywords

FIBSTEMEFTEMchitonteethmagnetitegoethitelepidocrociteapatiteinterface
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 17 , Issue 2 , April 2011 , pp. 220 - 225
Copyright
Copyright © Microscopy Society of America 2011

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

Addadi, L., Joester, D., Nudelman, F. & Weiner, S. (2006). Mollusk shell formation: A source of new concepts for understanding biomineralization processes. Chem Europ J 12, 980–987.CrossRefGoogle ScholarPubMed
Birchall, J.D. (1989). The importance of the study of biominerals to materials technology. In Biomineralization: Chemical and Biochemical Perspectives, Mann, S., Webb, J. & Williams, R.J.P. (Eds.), pp. 491–509. Weinheim, Germany: VCH Verlagsgesellschaft.Google Scholar
Evans, L.A., Macey, D.J. & Webb, J. (1990). Characterization and structural organization of the organic matrix of the radula teeth of the chiton Acanthopleura hirtosa. Philos Trans R Soc Lond B Biol Sci 329, 87–96.Google Scholar
Evans, L.A., Macey, D.J. & Webb, J. (1994). Matrix heterogeneity in the radular teeth of the chiton Acanthopleura hirtosa. Acta Zool 75(1), 75–79.CrossRefGoogle Scholar
Fratzl, P. (2007). Biomimetic materials research: What can we really learn from nature's structural materials? J R Soc Interface 4, 637–642.CrossRefGoogle ScholarPubMed
Huebsch, N. & Mooney, D.J. (2009). Inspiration and application in the evolution of biomaterials. Nature 462(7272), 426–432.CrossRefGoogle ScholarPubMed
Kim, K.S., Macey, D.J., Webb, J. & Mann, S. (1989). Iron mineralization in the radula teeth of the chiton Acanthopleura hirtosa. Proc R Soc Lond B Biol Sci B237, 335–346.Google Scholar
Lee, A.P., Webb, J., Macey, D.J., van Bronswijk, W., Savarese, A. & De Witt, C. (1998). In situ Raman spectroscopic studies of the teeth of the chiton Acanthopleura hirtosa. J Biol Inorg Chem 3, 614–619.CrossRefGoogle Scholar
Lowenstam, H.A. (1967). Lepidocrocite, an apatite mineral, and magnetite in teeth of chitons (Polyplacophora). Science 156(3780), 1373–1375.CrossRefGoogle ScholarPubMed
Lowenstam, H.A. & Weiner, S. (1989). On Biomineralization. Oxford, UK: Oxford University Press.CrossRefGoogle Scholar
Macey, D.J., Webb, J. & Brooker, L.R. (1994). The structure and synthesis of biominerals in chiton teeth. Bull Inst Oceanog 14(1), 191–197.Google Scholar
Mann, S. (2001). Biomineralization, Principals and Concepts in Bioinorganic Materials Chemistry. Oxford, UK: Oxford University Press.CrossRefGoogle Scholar
Mann, S. & Ozin, G.A. (1996). Synthesis of inorganic materials with complex form. Nature 382, 313–318.CrossRefGoogle Scholar
Nesson, M.H. & Lowenstam, H.A. (1985). Biomineralization processes of the radula teeth of chitons. In Magnetite Biomineralization and Magnetoreception in Organisms, Kirshvink, J.L., Jones, D.S. & MacFadden, B.J. (Eds.), pp. 333–361. New York: Plenum Press.CrossRefGoogle Scholar
Saunders, M., Kong, C., Shaw, J.A., Macey, D.J. & Clode, P.L. (2009). Characterization of biominerals in the radula teeth of the chiton, Acanthopleura hirtosa. J Struct Biol 167(1), 55–61.CrossRefGoogle ScholarPubMed
Saunders, M., Shaw, J.A., Clode, P.L., Kong, C. & Macey, D.J. (2010). Fine-scale analysis of biomineralized mollusc teeth using FIB and TEM. Microsc Today 18(1), 24–28.CrossRefGoogle Scholar
Shaw, J.A., Macey, D.J. & Brooker, L.R. (2008). Radula synthesis by three species of iron mineralizing molluscs: Production rate and elemental demand. J Mar Biol Assoc UK 88(3), 597–601.CrossRefGoogle Scholar
Shaw, J.A., Macey, D.J., Brooker, L.R. & Clode, P.L. (2010). Tooth use and wear in three iron-biomineralizing mollusc species. Biol Bull 218, 132–144.CrossRefGoogle ScholarPubMed
Shaw, J.A., Macey, D.J., Brooker, L.R., Stockdale, E.J., Saunders, M. & Clode, P.L. (2009a). The chiton stylus canal: An element delivery pathway for tooth cusp biomineralization. J Morphol 270(5), 588–600.CrossRefGoogle ScholarPubMed
Shaw, J.A., Macey, D.J., Brooker, L.R., Stockdale, E.J., Saunders, M. & Clode, P.L. (2009b). Ultrastructure of the epithelial cells associated with tooth biomineralization in the chiton Acanthopleura hirtosa. Microsc Microanal 15(2), 154–165.CrossRefGoogle ScholarPubMed
Sone, E.D., Weiner, S. & Addadi, L. (2007). Biomineralization of limpet teeth: A cryo-TEM study of the organic matrix and the onset of mineral deposition. J Struct Biol 158, 428–444.CrossRefGoogle ScholarPubMed
van der Wal, P., Giesen, H. & Videler, J. (2000). Radular teeth as models for the improvement of industrial cutting devices. Mater Sci Eng C 7(2), 129–142.CrossRefGoogle Scholar
van der Wal, P., Videler, J.J., Havinga, P. & Pel, R. (1989). Architecture and chemical composition of the magnetite-bearing layer in the radula teeth of Chiton olivaceus (Polyplacophora). In Origin, Evolution, and Modern Aspects of Biomineralization in Plants and Animals, Crick, R.E. (Ed.), pp. 153–166. New York: Plenum Press.CrossRefGoogle Scholar
Wealthall, R.J., Brooker, L.R., Macey, D.J. & Griffin, B.J. (2005). Fine structure of the mineralized teeth of the chiton Acanthopleura echinata (Mollusca: Polyplacophora). J Morphol 265(2), 165–175.CrossRefGoogle ScholarPubMed
Weaver, J.C., Wang, Q., Miserez, A., Tantuccio, A., Stromberg, R., Bozhilov, K.N., Maxwell, P., Nay, R., Heier, S.T., DiMasi, E. & Kisailus, D. (2010). Analysis of an ultra hard magnetic biomineral in chiton radular teeth. Mater Today 13(1-2), 42–52.CrossRefGoogle Scholar
Weiner, S. (2008). Biomineralization: A structural perspective. J Struct Biol 163(3), 229–234.CrossRefGoogle ScholarPubMed
Weiner, S. & Addadi, L. (2002). At the cutting edge. Science 298(5592), 375–376.CrossRefGoogle ScholarPubMed
Weiner, S., Sagi, I. & Addadi, L. (2005). Choosing the crystallization path less traveled. Science 309, 1027–1028.CrossRefGoogle ScholarPubMed