Frontiers of Materials Science

, Volume 11, Issue 1, pp 1–12 | Cite as

Multi-scale simulations of apatite–collagen composites: from molecules to materials

  • Dirk Zahn
Review Article


We review scale-bridging simulation studies for the exploration of atomicto-meso scale processes that account for the unique structure and mechanic properties of apatite-protein composites. As the atomic structure and composition of such complex biocomposites only partially is known, the first part (i) of our modelling studies is dedicated to realistic crystal nucleation scenarios of inorganic-organic composites. Starting from the association of single ions, recent insights range from the mechanisms of motif formation, ripening reactions and the self-organization of nanocrystals, including their interplay with growth-controlling molecular moieties. On this basis, (ii) reliable building rules for unprejudiced scale-up models can be derived to model bulk materials. This is exemplified for (enamel-like) apatite-protein composites, encompassing up to 106 atom models to provide a realistic account of the 10 nm length scale, whilst model coarsening is used to reach μm length scales. On this basis, a series of deformation and fracture simulation studies were performed and helped to rationalize biocomposite hardness, plasticity, toughness, self-healing and fracture mechanisms. Complementing experimental work, these modelling studies provide particularly detailed insights into the relation of hierarchical composite structure and favorable mechanical properties.


biocomposites deformation fracture molecular simulation 


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The author thanks P. Duchstein and R. Kniep for many fruitful discussions. This work was supported by the Deutsche Forschungsgemeinschaft via grants ZA 420/7, 420/8 and EXC315.


  1. [1]
    Fratzl P, Weinkamer R. Natures hierarchical materials. Progress in Materials Science, 2007, 52(8): 1263–1334CrossRefGoogle Scholar
  2. [2]
    Weiner S, Wagner H D. The material bone: structure–mechanical function relations. Annual Review of Materials Science, 1998, 28 (1): 271–298CrossRefGoogle Scholar
  3. [3]
    Fratzl P, Gupta H S, Paschalis E P, et al. Structure and mechanical quality of the collagen–mineral nano-composite in bone. Journal of Materials Chemistry, 2004, 14(14): 2115–2123CrossRefGoogle Scholar
  4. [4]
    Fratzl P, ed. Collagen: Structure and Mechanics. Springer, 2008Google Scholar
  5. [5]
    He L H, Swain M V. Enamel — a “metallic-like” deformable biocomposite. Journal of Dentistry, 2007, 35(5): 431–437CrossRefGoogle Scholar
  6. [6]
    He L H, Swain M V. Contact induced deformation of enamel. Applied Physics Letters, 2007, 90(17): 171916 (3 pages)CrossRefGoogle Scholar
  7. [7]
    He L H, Swain M V. Nanoindentation creep behavior of human enamel. Journal of Biomedical Materials Research Part A, 2009, 91(2): 352–359CrossRefGoogle Scholar
  8. [8]
    Fantner G E, Hassenkam T, Kindt J H, et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Materials, 2005, 4(8): 612–616CrossRefGoogle Scholar
  9. [9]
    Buehler M J. Nature designs tough collagen: explaining the nanostructure of collagen fibrils. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103 (33): 12285–12290CrossRefGoogle Scholar
  10. [10]
    Kniep R, Simon P. Fluorapatite–gelatine-nanocomposites: selforganized morphogenesis, real structure and relations to natural hard materials. Topics in Current Chemistry, 2006, 270: 73–125CrossRefGoogle Scholar
  11. [11]
    Simon P, Rosseeva E, Buder J, et al. Embryonic states of fluorapatite–gelatine nanocomposites and their intrinsic electricfield- driven morphogenesis: the missing link on the way from atomistic simulations to pattern formation on the mesoscale. Advanced Functional Materials, 2009, 19(22): 3596–3603CrossRefGoogle Scholar
  12. [12]
    Kawska A, Hochrein O, Brickmann J, et al. The nucleation mechanism of fluorapatite–collagen composites: ion association and motif control by collagen proteins. Angewandte Chemie International Edition, 2008, 47(27): 4982–4985CrossRefGoogle Scholar
  13. [13]
    Zahn D, Hochrein O, Kawska A, et al. Towards an atomistic understanding of apatite–collagen biomaterials: linking molecular simulation studies of complex-, crystal- and composite-formation to experimental findings. Journal of Materials Science, 2007, 42 (21): 8966–8973CrossRefGoogle Scholar
  14. [14]
    Zahn D, Hochrein O. Computational study of interfaces between hydroxyapatite and water. Physical Chemistry Chemical Physics, 2003, 5(18): 4004–4007CrossRefGoogle Scholar
  15. [15]
    de Leeuw N H. Resisting the onset of hydroxyapatite dissolution through the incorporation of fluoride. The Journal of Physical Chemistry B, 2004, 108(6): 1809–1811CrossRefGoogle Scholar
  16. [16]
    Zahn D. A molecular rationale of shock absorption and selfhealing in a biomimetic apatite–collagen composite under mechanical load. Angewandte Chemie International Edition, 2010, 49(49): 9405–9407CrossRefGoogle Scholar
  17. [17]
    Duchstein P, Zahn D. Atomistic modeling of apatite–collagen composites from molecular dynamics simulations extended to hyperspace. Journal of Molecular Modeling, 2011, 17(1): 73–79CrossRefGoogle Scholar
  18. [18]
    Zahn D, Bitzek E. Shearing in a biomimetic apatite–protein composite: molecular dynamics of slip zone formation, plastic flow and backcreep mechanisms. PLoS One, 2014, 9(4): e93309CrossRefGoogle Scholar
  19. [19]
    Zahn D, Duchstein P. Multi-scale modelling of deformation and fracture in a biomimetic apatite–protein composite: molecularscale processes lead to resilience at the μm-scale. PLoS One, 2016, 11(6): e0157241CrossRefGoogle Scholar
  20. [20]
    Simon P, Zahn D, Lichte H, et al. Intrinsic electric dipole fields and the induction of hierarchical form developments in fluorapatite–gelatine nanocomposites: a general principle for morphogenesis of biominerals? Angewandte Chemie International Edition, 2006, 45(12): 1911–1915CrossRefGoogle Scholar
  21. [21]
    Hauptmann S, Dufner H, Brickmann J, et al. Potential energy function for apatites. Physical Chemistry Chemical Physics, 2003, 5(3): 635–639CrossRefGoogle Scholar
  22. [22]
    de Leeuw N H. A computer modelling study of the uptake and segregation of fluoride ions at the hydrated hydroxyapatite (0001) surface: introducing a Ca10(PO4)6(OH)2 potential model. Physical Chemistry Chemical Physics, 2004, 6(8): 1860–1866CrossRefGoogle Scholar
  23. [23]
    Bhowmik R, Katti K S, Katti D. Molecular dynamics simulation of hydroxyapatite–polyacrylic acid interface. Polymer, 2007, 48 (2): 664–674CrossRefGoogle Scholar
  24. [24]
    Meißner R H, Wei G, Ciacchi L C. Estimation of the free energy of adsorption of a polypeptide on amorphous SiO2 from molecular dynamics simulations and force spectroscopy experiments. Soft Matter, 2015, 11(31): 6254–6265CrossRefGoogle Scholar
  25. [25]
    Larrucea J, Lid S, Ciacchi L C. Parametrization of a classical force field for iron oxyhydroxide/water interfaces based on Density Functional Theory calculations. Computational Materials Science, 2014, 92: 343–352CrossRefGoogle Scholar
  26. [26]
    Almora-Barrios N, De Leeuw N H. Molecular dynamics simulation of the early stages of nucleation of hydroxyapatite at a collagen template. Crystal Growth & Design, 2012, 12(2): 756–763CrossRefGoogle Scholar
  27. [27]
    Milek T, Zahn D. Molecular modeling of (1010) and (0001) zinc oxide surface growth from solution: islands, ridges and growthcontrolling additives. CrystEngComm, 2015, 17(36): 6890–6894CrossRefGoogle Scholar
  28. [28]
    Kawska A, Duchstein P, Hochrein O, et al. Atomistic mechanisms of ZnO aggregation from ethanolic solution: ion association, proton transfer, and self-organization. Nano Letters, 2008, 8(8): 2336–2340CrossRefGoogle Scholar
  29. [29]
    Helminger M, Wu B, Kollmann T, et al. Synthesis and characterization of gelatin-based magnetic hydrogels. Advanced Functional Materials, 2014, 24(21): 3187–3196CrossRefGoogle Scholar
  30. [30]
    Tommaso D D, de Leeuw N H. The onset of calcium carbonate nucleation: a density functional theory molecular dynamics and hybrid microsolvation/continuum study. The Journal of Physical Chemistry B, 2008, 112(23): 6965–6975CrossRefGoogle Scholar
  31. [31]
    Zahn D. Mechanisms of calcium and phosphate ion association in aqueous solution. Zeitschrift fur Anorganische und Allgemeine Chemie, 2004, 630(10): 1507–1511CrossRefGoogle Scholar
  32. [32]
    Wallace A F, Hedges L O, Fernandez-Martinez A, et al. Microscopic evidence for liquid–liquid separation in supersaturated CaCO3 solutions. Science, 2013, 341(6148): 885–889CrossRefGoogle Scholar
  33. [33]
    Duchstein P, Kniep R, Zahn D. On the function of saccharides during the nucleation of calcium carbonate–protein biocomposites. Crystal Growth & Design, 2013, 13(11): 4885–4889CrossRefGoogle Scholar
  34. [34]
    Hochrein O, Zahn D. On the molecular mechanisms of the acidinduced dissociation of hydroxy-apatite in water. Journal of Molecular Modeling, 2011, 17(6): 1525–1528CrossRefGoogle Scholar
  35. [35]
    Damkier H H, Josephsen K, Takano Y, et al. Fluctuations in surface pH of maturing rat incisor enamel are a result of cycles of H+-secretion by ameloblasts and variations in enamel buffer characteristics. Bone, 2014, 60(3): 227–234CrossRefGoogle Scholar
  36. [36]
    Anwar J, Zahn D. Uncovering molecular processes in crystal nucleation and growth by using molecular simulation. Angewandte Chemie International Edition, 2011, 50(9): 1996–2013CrossRefGoogle Scholar
  37. [37]
    Rosseeva E V, Buder J, Simon P, et al. Synthesis, characterization, and morphogenesis of carbonated fluorapatite–gelatine nanocomposites: A complex biomimetic approach toward the mineralization of hard tissues. Chemistry of Materials, 2008, 20(19): 6003–6013CrossRefGoogle Scholar
  38. [38]
    Bos K J, Rucklidge G J, Dunbar B, et al. Primary structure of the helical domain of porcine collagen X. Matrix Biology, 1999, 18 (2): 149–153CrossRefGoogle Scholar
  39. [39]
    Nair A K, Gautieri A, Chang S W, et al. Molecular mechanics of mineralized collagen fibrils in bone. Nature Communications, 2013, 4: 1724CrossRefGoogle Scholar
  40. [40]
    Grenoble D E, Katz J L, Dunn K L, et al. The elastic properties of hard tissues and apatites. Journal of Biomedical Materials Research, 1972, 6(3): 221–233CrossRefGoogle Scholar
  41. [41]
    Maas M C, Dumont E R. Built to last: The structure, function, and evolution of primate dental enamel. Evolutionary Anthropology: Issues, News and Reviews, 1999, 8(4): 133–152CrossRefGoogle Scholar
  42. [42]
    Pomes R, Eisenmesser E, Post C B, et al. Calculating excess chemical potentials using dynamic simulations in the fourth dimension. The Journal of Chemical Physics, 1999, 111(8): 3387–3395CrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Lehrstuhl für Theoretische Chemie/Computer Chemie CentrumFriedrich-Alexander Universität Erlangen-NürnbergErlangenGermany

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