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Nanoscale chemical tomography of buried organic–inorganic interfaces in the chiton tooth

Nature volume 469, pages 194–197 (2011)Cite this article

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Abstract

Biological organisms possess an unparalleled ability to control the structure and properties of mineralized tissues. They are able, for example, to guide the formation of smoothly curving single crystals or tough, lightweight, self-repairing skeletal elements1. In many biominerals, an organic matrix interacts with the mineral as it forms, controls its morphology and polymorph, and is occluded during mineralization2,3,4. The remarkable functional properties of the resulting composites—such as outstanding fracture toughness and wear resistance—can be attributed to buried organic–inorganic interfaces at multiple hierarchical levels5. Analysing and controlling such interfaces at the nanometre length scale is critical also in emerging organic electronic and photovoltaic hybrid materials6. However, elucidating the structural and chemical complexity of buried organic–inorganic interfaces presents a challenge to state-of-the-art imaging techniques. Here we show that pulsed-laser atom-probe tomography reveals three-dimensional chemical maps of organic fibres with a diameter of 5–10 nm in the surrounding nano-crystalline magnetite (Fe3O4) mineral in the tooth of a marine mollusc, the chiton Chaetopleura apiculata. Remarkably, most fibres co-localize with either sodium or magnesium. Furthermore, clustering of these cations in the fibre indicates a structural level of hierarchy previously undetected. Our results demonstrate that in the chiton tooth, individual organic fibres have different chemical compositions, and therefore probably different functional roles in controlling fibre formation and matrix–mineral interactions. Atom-probe tomography is able to detect this chemical/structural heterogeneity by virtue of its high three-dimensional spatial resolution and sensitivity across the periodic table. We anticipate that the quantitative analysis and visualization of nanometre-scale interfaces by laser-pulsed atom-probe tomography will contribute greatly to our understanding not only of biominerals (such as bone, dentine and enamel), but also of synthetic organic–inorganic composites.

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Figure 1: Chiton radula and tooth structure.
Figure 2: Chiton tooth magnetite and occluded organic fibres.
Figure 3: APT time-of-flight m/z spectra.
Figure 4: Three-dimensional reconstructions and proxigrams.
Figure 5: Model of a chiton tooth organic fibre.

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Acknowledgements

This work was supported in part by the Canadian National Sciences and Engineering Research Council and the US National Science Foundation (DMR-0805313). FIB, SEM and (S)TEM work was performed in the Northwestern University Atomic and Nanoscale Characterization and Experimental Center (NUANCE) supported by NSF-NSEC, NSF-MRSEC, the Keck Foundation, the State of Illinois, and Northwestern University. APT measurements were performed at the Northwestern University Center for Atom Probe Tomography (NUCAPT) supported by NSF-MRI (DMR-0420532) and ONR-DURIP (N00014-0400798, N00014-0610539, N00014-0910781). We thank A. Tayi for help in preparing chitin thin film samples; B. Myers (NUANCE) for help with FIB; D. Isheim (NUCAPT), and D. Lawrence, R. Ulfig, T. Prosa and M. Greene (Cameca) for their assistance with APT; and D. Seidman for discussions.

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Authors and Affiliations

  1. Department of Materials Science and Engineering, Northwestern University, 2220 Campus Drive, Evanston, 60208, Illinois, USA

    Lyle M. Gordon & Derk Joester

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  1. Lyle M. Gordon
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Contributions

L.M.G. and D.J. designed the experiments, analysed the data and prepared the manuscript. L.M.G. performed the experiments.

Corresponding author

Correspondence to Derk Joester.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Information

The file contains Supplementary Figures 1-7 with legends and Supplementary Notes on Isotopic Analysis. (PDF 1002 kb)

Supplementary Movie 1

This movie shows a three-dimensional reconstruction of a region of the chiton tooth containing organic fibres that bind sodium ions (Fig. 4A). Clear co-localization of the sodium ions within the organic fibre is visible. Sodium and carbon are rendered as red and grey spheres, respectively. Oxygen and iron are rendered as light blue and pink points, respectively. For clarity, only ~5% of the Fe/O are rendered. (MPG 9706 kb)

Supplementary Movie 2

This movie shows a three-dimensional reconstruction of region of the chiton tooth where multiple fibers are bundled together. In this bundle there are fibres which bind either sodium or magnesium resulting in the co-localization of both sodium and magnesium ions around the closely bundle fibres. Similar bundles are visible in the STEM images. Sodium, magnesium and carbon are rendered as red, blue and grey spheres, respectively. Oxygen and iron are rendered as light blue and pink points, respectively. A cross-section through the fibre bundle is shown in supplementary figure 6. For clarity, only ~5% of the Fe/O are rendered. (MPG 19020 kb)

Supplementary Movie 3

This movie shows a three-dimensional reconstruction of a region of the chiton tooth containing organic fibres that bind only magnesium ions (Fig. 4D). Clear co-localization of the magnesium ions within the organic fibre is visible. Magnesium and carbon are rendered as blue and grey spheres, respectively. Oxygen and iron are rendered as light blue and pink points, respectively. For clarity, only ~5% of the Fe/O are rendered. (MPG 11118 kb)

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Gordon, L., Joester, D. Nanoscale chemical tomography of buried organic–inorganic interfaces in the chiton tooth. Nature 469, 194–197 (2011). https://doi.org/10.1038/nature09686

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