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

Many biomineralized tissues, such as teeth and bone, are hybrid inorganic–organic materials whose properties are determined by their convoluted internal structures. Lyle Gordon and Derk Joester now show how the internal structural and chemical complexity of such biomaterials and their synthetic analogues can be elucidated using pulsed-laser atom-probe tomography (APT), an established technique in metallurgical and semiconductor research. The model for the study was a tooth from a marine mollusc, the Eastern beaded chiton. The resulting high-resolution three-dimensional chemical maps reveal individual organic fibres within the tooth that have different compositions, and therefore probably different functional roles in controlling the interactions between the organic matrix and inorganic mineral phases. As well as revealing the nature of naturally occurring materials, the use of APT in this field should provide useful data for the design of bio-inspired composites for medical and industrial applications. Many biomineralized tissues (such as teeth and bone) are hybrid inorganic–organic materials whose properties are determined by their convoluted internal structures. Now, using a chiton tooth as an example, this study shows how the internal structural and chemical complexity of such biomaterials and their synthetic analogues can be elucidated using pulsed-laser atom-probe tomography. 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.