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Tuning hardness in calcite by incorporation of amino acids

Nature Materials volume 15, pages 903–910 (2016)Cite this article

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Abstract

Structural biominerals are inorganic/organic composites that exhibit remarkable mechanical properties. However, the structure–property relationships of even the simplest building unit—mineral single crystals containing embedded macromolecules—remain poorly understood. Here, by means of a model biomineral made from calcite single crystals containing glycine (0–7 mol%) or aspartic acid (0–4 mol%), we elucidate the origin of the superior hardness of biogenic calcite. We analysed lattice distortions in these model crystals by using X-ray diffraction and molecular dynamics simulations, and by means of solid-state nuclear magnetic resonance show that the amino acids are incorporated as individual molecules. We also demonstrate that nanoindentation hardness increased with amino acid content, reaching values equivalent to their biogenic counterparts. A dislocation pinning model reveals that the enhanced hardness is determined by the force required to cut covalent bonds in the molecules.

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Figure 1: Crystal morphologies.
Figure 2: Occlusion of aspartic acid and glycine in calcite.
Figure 3: High-resolution PXRD analysis.
Figure 4: Solid-state NMR analysis.
Figure 5: Molecular dynamics simulations.
Figure 6: Mechanical properties.

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Acknowledgements

This work was supported by an Engineering and Physical Sciences Research Council (EPSRC) Leadership Fellowship (F.C.M. and Y.-Y.K., EP/H005374/1), by an EPSRC Materials World Network grant (EP/J018589/1, F.C.M. and Y.-Y.K.) and an EPSRC Programme Grant (grant EP/I001514/1) which funds the Materials Interface with Biology (MIB) consortium (F.C.M., J.H.H. and D.S.). We acknowledge Diamond Light Source for time on beamline I11 under commissioning time and proposal EE10137. L.A.E., J.D.C., M.E.K. and S.P.B. were supported by the US National Science Foundation (NSF) via a Materials World Network grant (DMR-1210304). B.P. acknowledges support from the European Research Council under the European Union’s Seventh Framework Program (FP/2007–2013)/ERC Grant Agreement no [336077]. B.D. and K.P. were supported by the Leverhulme Trust and the EU reintegration grant (PERG07-GA-2010-268429, FP7), project ‘mAARiTIME’. Ashely Coutu and Sheila Taylor are thanked for technical help for RP-HPLC analysis. This work made use of the Cornell Center for Materials Research Shared Facilities, which are supported through the NSF MRSEC Program (DMR-1120296). The authors also thank Matthew Collins for his intellectual contribution to the development of the study and for helpful discussions throughout.

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Authors and Affiliations

  1. School of Chemistry, University of Leeds, Woodhouse Lane, Leeds LS2 9JT, UK

    Yi-Yeoun Kim & Fiona C. Meldrum

  2. Department of Materials Science and Engineering, 214 Bard Hall, Cornell University, Ithaca, New York 14853, USA

    Joseph D. Carloni, Miki E. Kunitake, Lara A. Estroff & Shefford P. Baker

  3. Departments of Chemistry and Archaeology, BioArCh, University of York, York YO10 5DD, UK

    Beatrice Demarchi & Kirsty Penkman

  4. Department of Materials Science and Engineering, University of Sheffield, Mappin Street, Sheffield S1 3JD, UK

    David Sparks, Colin L. Freeman & John H. Harding

  5. Department of Chemistry, University of Cambridge, Lensfield Road, Cambridge CB2 1EW, UK

    David G. Reid & Melinda J. Duer

  6. Diamond Light Source, Harwell Science and Innovation Campus, Didcot OX11 0DE, UK

    Chiu C. Tang

  7. Department of Materials Science and Engineering and the Russell Berrie Nanotechnology Institute, Technion Israel Institute of Technology, Haifa 32000, Israel

    Boaz Pokroy

  8. Kavli Institute at Cornell for Nanoscale Science, 420 Physical Sciences Building, Ithaca, New York 14853, USA

    Lara A. Estroff

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Contributions

Y.-Y.K. led the experimental work, preparing samples and carrying out EM and XRD, and analysing the data; B.D. and K.P. performed HPLC measurements and analysed the occlusion data; J.D.C. and M.E.K. carried out nanoindentation measurements, J.D.C., S.P.B. and L.A.E. analysed and modelled mechanical data; S.P.B. and L.A.E. co-supervised J.D.C. and M.E.K.; D.S. carried out molecular dynamic simulations work and C.L.F. and J.H.H. supervised D.S. and analysed simulation data; C.C.T. assisted with the PXRD experiments; B.P. assisted with analysis and discussion of the PXRD data; D.G.R. and M.J.D. performed the NMR studies and analyses; F.C.M. originated and supervised the project. All authors contributed to the preparation of the manuscript.

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Correspondence to Yi-Yeoun Kim, Shefford P. Baker or Fiona C. Meldrum.

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Kim, YY., Carloni, J., Demarchi, B. et al. Tuning hardness in calcite by incorporation of amino acids. Nature Mater 15, 903–910 (2016). https://doi.org/10.1038/nmat4631

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