Abstract
Significant progress has been made in understanding the interaction between mineral precursors and organic components leading to material formation and structuring in biomineralizing systems1,2,3,4,5. The mesostructure of biological materials, such as the outer calcitic shell of molluscs, is characterized by many parameters and the question arises as to what extent they all are, or need to be, controlled biologically. Here, we analyse the three-dimensional structure of the calcite-based prismatic layer of Pinna nobilis6,7,8, the giant Mediterranean fan mussel, using high-resolution synchrotron-based microtomography. We show that the evolution of the layer is statistically self-similar and, remarkably, its morphology and mesostructure can be fully predicted using classical materials science theories for normal grain growth9,10,11,12,13,14,15,16. These findings are a fundamental step in understanding the constraints that dictate the shape of these biogenic minerals and shed light on how biological organisms make use of thermodynamics to generate complex morphologies.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$259.00 per year
only $21.58 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Weiner, S. & Addadi, L. Crystallization pathways in biomineralization. Annu. Rev. Mater. Res. 41, 21–40 (2011).
Nudelman, F. & Sommerdijk, N. Biomineralization as an inspiration for materials chemistry. Angew. Chem. Int. Ed. 51, 6582–6596 (2012).
Schenk, A. S. et al. Systematic study of the effects of polyamines on calcium carbonate precipitation. Chem. Mater. 26, 2703–2711 (2014).
Gower, L. B. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem. Rev. 108, 4551–4627 (2008).
Schenk, A. S. et al. Hierarchical calcite crystals with occlusions of a simple polyelectrolyte mimic complex biomineral structures. Adv. Funct. Mater. 22, 4668–4676 (2012).
Marin, F., Narayanappa, P. & Motreuil, S. in Molecular Biomineralization Vol. 52 (ed. Müller, W. E. G.) Ch. 13, 353–395 (Springer, 2011).
Taylor, J. & Layman, M. The mechanical properties of bivalve (Mollusca) shell structures. Palaeontology 15, 73–87 (1972).
Marin, F. & Luquet, G. Molluscan biomineralization: The proteinaceous shell constituents of Pinna nobilis L. Mater. Sci. Eng. C 25, 105–111 (2005).
Atkinson, H. V. Theories of normal grain growth in pure single phase systems. Acta Metall. 36, 469–491 (1988).
Hillert, M. On the theory of normal and abnormal grain growth. Acta Metall. 13, 227–238 (1965).
Mullins, W. W. Two-dimensional motion of idealized grain boundaries. J. Appl. Phys. 27, 900–904 (1956).
Von Neumann, J. in Metal Interfaces (ed Herring, C.) 108–110 (American Society of Metals, 1952).
Burke, J. & Turnbull, D. Recrystallization and grain growth. Prog. Met. Phys. 3, 220–244 (1952).
Srolovitz, D. J., Anderson, M. P., Crest, G. S. & Sahni, P. S. Computer simulation of grain growth-II. Grain size distribution, topology, and local dynamics. Acta Metall. 32, 793–802 (1984).
Smith, C. S. Some elementary principles of polycrystalline microstructure. Metall. Rev. 9, 1–48 (1964).
Smith, C. S. Structure, substructure, and superstructure. Rev. Mod. Phys. 36, 524–532 (1964).
Fratzl, P. & Weinkamer, R. Nature’s hierarchical materials. Prog. Mater. Sci. 52, 1263–1334 (2007).
Dauphin, Y. et al. In situ mapping of growth lines in the calcitic prismatic layers of mollusc shells using X-ray absorption near-edge structure (XANES) spectroscopy at the sulphur K-edge. Mar. Biol. 142, 299–304 (2003).
Pokroy, B., Fitch, A. & Zolotoyabko, E. The microstructure of biogenic calcite: A view by high-resolution synchrotron powder diffraction. Adv. Mater. 18, 2363–2368 (2006).
Dauphin, Y. Comparison of the soluble matrices of the calcitic prismatic layer of Pinnanobilis (Mollusca, Bivalvia, Pteriomorpha). Comp. Biochem. Physiol. A 132, 577–590 (2002).
Olson, I. C. et al. Crystal nucleation and near-epitaxial growth in nacre. J. Struct. Biol. 184, 454–463 (2013).
Checa, A. G., Rodríguez-Navarro, A. B. & Esteban-Delgado, F. J. The nature and formation of calcitic columnar prismatic shell layers in pteriomorphian bivalves. Biomaterials 26, 6404–6414 (2005).
Thompson, C. V. Grain growth in thin films. Annu. Rev. Mater. Sci. 20, 245–268 (1990).
Barmak, K. et al. Grain growth and the puzzle of its stagnation in thin films: The curious tale of a tail and an ear. Prog. Mater. Sci. 58, 987–1055 (2013).
Beck, P. Annealing of cold worked metals. Adv. Phys. 3, 245–324 (1954).
Mullins, W. W. The statistical self-similarity hypothesis in grain growth and particle coarsening. J. Appl. Phys. 59, 1341–1349 (1986).
Elsey, M., Esedoglu, S. & Smereka, P. Large-scale simulation of normal grain growth via diffusion-generated motion. Proc. R. Soc. A 467, 381–401 (2010).
Fayad, W., Thompson, C. V. & Frost, H. J. Steady-state grain-size distributions resulting from grain growth in two dimensions. Scripta Mater. 40, 1199–1204 (1999).
Zöllner, D. & Rios, P. R. Investigating the von Neumann–Mullins relation under triple junction dragging. Acta Mater. 70, 290–297 (2014).
Weitkamp, T., Haas, D., Wegrzynek, D. & Rack, A. ANKAphase: Software for single-distance phase retrieval from inline X-ray phase-contrast radiographs. J. Synchrotron Radiat. 18, 617–629 (2011).
Schneider, C. A, Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675 (2012).
Acknowledgements
We acknowledge the European Synchrotron Radiation Facility for provision of synchrotron radiation facilities on ID19. Project supported in part by the German Science Foundation DFG, project FR 2190/4-1 (Leibniz Prize to P.F.).
Author information
Authors and Affiliations
Contributions
B.B. prepared the samples for the tomography experiments. B.B., I.Z., P.Z. and A.R. performed the synchrotron-based microtomography experiments. P.Z. and A.R. performed the data processing. B.B., P.F. and I.Z. performed image and data analysis. Y.D. supplied the samples. B.B., P.F. and I.Z. wrote the manuscript. I.Z. conceived the project. All authors commented on the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Information
Supplementary Movie S1 (AVI 4759 kb)
Rights and permissions
About this article
Cite this article
Bayerlein, B., Zaslansky, P., Dauphin, Y. et al. Self-similar mesostructure evolution of the growing mollusc shell reminiscent of thermodynamically driven grain growth. Nature Mater 13, 1102–1107 (2014). https://doi.org/10.1038/nmat4110
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nmat4110
This article is cited by
-
Strategies for simultaneous strengthening and toughening via nanoscopic intracrystalline defects in a biogenic ceramic
Nature Communications (2020)
-
Intermolecular channels direct crystal orientation in mineralized collagen
Nature Communications (2020)
-
From spinodal decomposition to alternating layered structure within single crystals of biogenic magnesium calcite
Nature Communications (2019)
-
Correlation between three-dimensional and cross-sectional characteristics of ideal grain growth: large-scale phase-field simulation study
Journal of Materials Science (2018)
-
Total morphosynthesis of biomimetic prismatic-type CaCO3 thin films
Nature Communications (2017)