Skip to main content
SpringerLink
Log in

Unraveling the internal microstructure of biogenic and bioinspired calcite single crystals

  • Biomineralization
  • Published:
MRS Bulletin Aims and scope Submit manuscript

Abstract

Modern materials design is largely based on composite structures aimed at a synergistic integration of multiple components with a diverse range of properties. Biologically grown minerals provide an intriguing example of sophisticated organic–inorganic nanocomposite structures resulting in excellent mechanical characteristics. Among the mineral phases utilized by living organisms to generate hard tissues, calcium carbonate—especially the calcite polymorph—is ubiquitous and has been studied intensively. Biogenic calcite crystals often show hierarchical organization spanning multiple length scales, and the occluded organic phases are now known to be intimately associated with the mineral host. Here, we discuss the internal micro- and nanostructure of two selected types of calcite biominerals—the sea urchin spine and prismatic single crystals extracted from mollusk shells. This article highlights recent advances in translating the key principles of biological mineralization into design strategies for synthetic materials and presents analogies between biogenic and synthetic calcite single crystals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. H.A. Lowenstam, S. Weiner, On Biomineralization ( Oxford University Press, New York, 1989 ).

  2. L. Brecevic, D. Kralj, Croat. Chem. Acta 80, 467 ( 2007 ).

    CAS  Google Scholar 

  3. T.P. Scoffin, An Introduction to Carbonate Sediments and Rocks ( Blackie, Glasgow, London, 1987 ).

  4. L. Addadi, S. Weiner, Phys. Scr. 89, 098003 ( 2014 ).

    Article  CAS  Google Scholar 

  5. D. Vielzeuf, N. Floquet, D. Chatain, F. Bonnete, D. Ferry, J. Garrabou, E.M. Stolper, Am. Mineral. 95, 242 ( 2010 ).

    Article  CAS  Google Scholar 

  6. J. Seto, Y.R. Ma, S.A. Davis, F. Meldrum, A. Gourrier, Y.Y. Kim, U. Schilde, M. Sztucki, M. Burghammer, S. Maltsev, C. Jäger, H. Cölfen, Proc. Natl. Acad. Sci. U.S.A. 109, 3699 ( 2012 ).

    Article  CAS  Google Scholar 

  7. F. Nudelman, H.H. Chen, H.A. Goldberg, S. Weiner, L. Addadi, Faraday Discuss. 136, 9 ( 2007 ).

    Article  CAS  Google Scholar 

  8. L. Addadi, D. Joester, F. Nudelman, S. Weiner, Chem. Eur. J. 12, 981 ( 2006 ).

    Article  Google Scholar 

  9. R van de Locht, T.J.A. Slater, A. Verch, J.R. Young, S.J. Haigh, R. Kröger, Cryst. Growth Des. 14, 1710 ( 2014 ).

    Article  Google Scholar 

  10. J. Aizenberg, A. Tkachenko, S. Weiner, L. Addadi, G. Hendler, Nature 412, 819 ( 2001 ).

    Article  CAS  Google Scholar 

  11. P. Fratzl, R. Weinkamer, Prog. Mater. Sci. 52, 1263 ( 2007 ).

    Article  CAS  Google Scholar 

  12. S. Albeck, J. Aizenberg, L. Addadi, J. Am. Chem. Soc. 135 ( 1993 ).

  13. F. Nudelman, B.A. Gotliv, L. Addadi, S. Weiner, J. Struct. Biol. 153, 176 ( 2006).

    Article  CAS  Google Scholar 

  14. B. Pokroy, A.N. Fitch, F. Marin, M. Kapon, N. Adir, E. Zolotoyabko, J. Struct. Biol. 155, 96 ( 2006 ).

    Article  CAS  Google Scholar 

  15. M.E. Kunitake, L.M. Mangano, J.M. Peloquin, S.P. Baker, L.A. Estroff, Acta Biomater. 9, 5353 ( 2013 ).

    Article  CAS  Google Scholar 

  16. L. Li, S. Kolle, J.C. Weaver, C. Ortiz, J. Aizenberg, M. Kolle, Nat. Commun. 6, 6322 ( 2015 ).

    Article  CAS  Google Scholar 

  17. G. Falini, S. Albeck, S. Weiner, L. Addadi, Science 271, 67 ( 1996 ).

    Article  Google Scholar 

  18. J.Y. Sun, B. Bhushan, RSC Adv. 2, 7617 ( 2012 ).

    Article  CAS  Google Scholar 

  19. I.C. Olson, R.A. Metzler, N. Tamura, M. Kunz, C.E. Killian, P.U.P.A. Gilbert, J. Struct. Biol. 183, 180 ( 2013 ).

    Article  CAS  Google Scholar 

  20. A. Berman, J. Hanson, L. Leiserowitz, T.F. Koetzle, S. Weiner, L. Addadi, Science 259, 776 ( 1993 ).

    Article  CAS  Google Scholar 

  21. B. Bayerlein, P. Zaslansky, Y. Dauphin, A. Rack, P. Fratzl, I. Zlotnikov, Nat. Mater. 13, 1102 ( 2014 ).

    Article  CAS  Google Scholar 

  22. C. Gilow, E. Zolotoyabko, O. Paris, P. Fratzl, B. Aichmayer, Cryst. Growth Des. 11, 2054 ( 2011 ).

    Article  CAS  Google Scholar 

  23. S.E. Wolf, I. Lieberwirth, F. Natalio, J.F. Bardeau, N. Delorme, F. Emmerling, R. Barrea, M. Kappl, F. Marin, Faraday Discuss. 159, 433 ( 2012 ).

    Article  CAS  Google Scholar 

  24. T.H. Metzger, Y. Politi, G. Carbone, B. Bayerlein, I. Zlotnikov, E. Zolotoyabko, P. Fratzl, Cryst. Growth Des. 14, 5275 ( 2014 ).

    Article  CAS  Google Scholar 

  25. Y. Dauphin, J.P. Cuif, J. Doucet, M. Salome, J. Susini, C.T. Williams, Mar. Biol. 142, 299 ( 2003 ).

    Article  Google Scholar 

  26. Y. Dauphin, J.P. Cuif, J. Doucet, M. Salome, J. Susini, C.T. Willams, J. Struct. Biol. 142, 272 ( 2003 ).

    Article  CAS  Google Scholar 

  27. H. Li, H.L. Xin, M.E. Kunitake, E.C. Keene, D.A. Muller, L.A. Estroff, Adv. Funct. Mater. 21, 2028 ( 2011 ).

    Article  Google Scholar 

  28. E. Zolotoyabko, E.N. Caspi, J.S. Fieramosca, R.B. Von Dreele, F. Marin, G. Mor, L. Addadi, S. Weiner, Y. Politi, Cryst. Growth Des. 10, 1207 ( 2010 ).

    Article  CAS  Google Scholar 

  29. J.S. Evans, Chem. Rev. 108, 4455 ( 2008 ).

    Article  CAS  Google Scholar 

  30. F. Marin, R. Amons, N. Guichard, M. Stigter, A. Hecker, G. Luquet, P. Layrolle, G. Alcaraz, C. Riondet, P. Westbroek, J. Biol. Chem. 280, 33895 ( 2005 ).

    Article  CAS  Google Scholar 

  31. B.-A. Gotliv, N. Kessler, J.L. Sumerel, D.E. Morse, N. Tuross, L. Addadi, S. Weiner, Chembiochem 6, 304 ( 2005 ).

    Article  CAS  Google Scholar 

  32. K.M. Towe, Science 157, 1048 ( 1967 ).

    Article  CAS  Google Scholar 

  33. B. Borzecka-Prokop, A. Weselucha-Birczynska, E. Koszowska, J. Mol. Struct. 828, 80 ( 2007 ).

    Article  CAS  Google Scholar 

  34. A. Berman, L. Addadi, S. Weiner, Nature 331, 546 ( 1988 ).

    Article  CAS  Google Scholar 

  35. A. Berman, L. Addadi, A. Kvick, L. Leiserowitz, M. Nelson, S. Weiner, Science 250, 664 ( 1990 ).

    Article  CAS  Google Scholar 

  36. U. Magdans, H. Gies, Eur. J. Mineral. 16, 261 ( 2004 ).

    Article  CAS  Google Scholar 

  37. J. Aizenberg, J. Hanson, T.F. Koetzle, S. Weiner, L. Addadi, J. Am. Chem. Soc. 119, 881 ( 1997 ).

    Article  CAS  Google Scholar 

  38. M.E. Kunitake, S.P. Baker, L.A. Estroff, MRS Commun. 2, 113 ( 2012 ).

    Article  CAS  Google Scholar 

  39. S. Weiner, L. Addadi, J. Mater. Chem. 7, 689 ( 1997 ).

    Article  CAS  Google Scholar 

  40. Y. Politi, T. Arad, E. Klein, S. Weiner, L. Addadi, Science 306, 1161 ( 2004 ).

    Article  CAS  Google Scholar 

  41. K.J. Davis, P.M. Dove, L.E. Wasylenki, J.J. De Yoreo, Am. Mineral. 89, 714 ( 2004 ).

    Article  CAS  Google Scholar 

  42. A. Mucci, J.W. Morse, Geochim. Cosmochim. Acta 47, 217 ( 1983 ).

    Article  CAS  Google Scholar 

  43. S. Borukhin, L. Bloch, T. Radlauer, A.H. Hill, A.N. Fitch, B. Pokroy, Adv. Funct. Mater. 22, 4216 ( 2012 ).

    Article  CAS  Google Scholar 

  44. T. Wang, H. Cölfen, M. Antonietti, J. Am. Chem. Soc. 127, 3246 ( 2005 ).

    Article  CAS  Google Scholar 

  45. Y.Y. Kim, A.S. Schenk, J. Ihli, A.N. Kulak, N.B.J. Hetherington, C.C. Tang, W.W. Schmahl, E. Griesshaber, G. Hyett, F.C. Meldrum, Nat. Commun. 5, 4341 ( 2014 ).

    Article  CAS  Google Scholar 

  46. Y.Y. Kim, K. Ganesan, P.C. Yang, A.N. Kulak, S. Borukhin, S. Pechook, L. Ribeiro, R. Kroger, S.J. Eichhorn, S.P. Armes, B. Pokroy, F.C. Meldrum, Nat. Mater. 10, 890 ( 2011 ).

    Article  CAS  Google Scholar 

  47. E. Asenath-Smith, H. Li, E.C. Keene, Z.W. Seh, L.A. Estroff, Adv. Funct. Mater. 22, 2891 ( 2012 ).

    Article  CAS  Google Scholar 

  48. H.Y. Li, H.L. Xin, D.A. Muller, L.A. Estroff, Science 326, 1244 ( 2009 ).

    Article  CAS  Google Scholar 

  49. A.N. Kulak, P.C. Yang, Y.Y. Kim, S.P. Armes, F.C. Meldrum, Chem. Commun. 50, 67 ( 2014 ).

    Article  CAS  Google Scholar 

  50. A.N. Kulak, M. Semsarilar, Y.Y. Kim, J. Ihli, L.A. Fielding, O. Cespedes, S.P. Armes, F.C. Meldrum, Chem. Sci. 5, 738 ( 2014 ).

    Article  CAS  Google Scholar 

  51. Y.Y. Kim, L. Ribeiro, F. Maillot, O. Ward, S.J. Eichhorn, F.C. Meldrum, Adv. Mater. 22, 2082 ( 2010 ).

    Article  CAS  Google Scholar 

  52. S.-H. Yu, H. Cölfen, J. Mater. Chem. 14, 2124 ( 2004 ).

    Article  CAS  Google Scholar 

  53. L.B. Gower, Chem. Rev. 108, 4551 ( 2008 ).

    Article  CAS  Google Scholar 

  54. F.C. Meldrum, H. Cölfen, Chem. Rev. 108, 4332 ( 2008 ).

    Article  CAS  Google Scholar 

  55. D.B. DeOliveira, R.A. Laursen, J. Am. Chem. Soc. 119, 10627 ( 1997 ).

    Article  CAS  Google Scholar 

  56. A.S. Schenk, B. Cantaert, Y.Y. Kim, Y.T. Li, E.S. Read, M. Semsarilar, S.P. Armes, F.C. Meldrum, Chem. Mater. 26, 2703 ( 2014 ).

    Article  CAS  Google Scholar 

  57. B. Cantaert, Y.Y. Kim, H. Ludwig, F. Nudelman, N.A.J.M. Sommerdijk, F.C. Meldrum, Adv. Funct. Mater. 22, 907 ( 2012 ).

    Article  CAS  Google Scholar 

  58. C.L. Chen, J.H. Qi, J.H. Tao, R.N. Zuckermann, J.J. De Yoreo, Sci. Rep. 4, 6266 ( 2014 ).

    Article  CAS  Google Scholar 

  59. A. Verch, D. Gebauer, M. Antonietti, H. Cölfen, Phys. Chem. Chem. Phys. 13, 16811 ( 2011 ).

    Article  CAS  Google Scholar 

  60. D. Gebauer, H. Cölfen, A. Verch, M. Antonietti, Adv. Mater. 21, 435 ( 2009 ).

    Article  CAS  Google Scholar 

  61. A.S. Schenk, I. Zlotnikov, B. Pokroy, N. Gierlinger, A. Masic, P. Zaslansky, A.N. Fitch, O. Paris, T.H. Metzger, H. Cölfen, P. Fratzl, B. Aichmayer, Adv. Funct. Mater. 22, 4668 ( 2012 ).

    Article  CAS  Google Scholar 

  62. R.A. Metzler, G.A. Tribello, M. Parrinello, P. Gilbert, J. Am. Chem. Soc. 132, 11585 ( 2010 ).

    Article  CAS  Google Scholar 

  63. U. Lins, M. Farina, M. Kurc, G. Riordan, R. Thalmann, I. Thalmann, B. Kachar, J. Struct. Biol. 131, 67 ( 2000 ).

    Article  CAS  Google Scholar 

  64. F. Nindiyasari, L. Fernandez-Diaz, E. Griesshaber, J.M. Astilleros, N. Sanchez-Pastor, W.W. Schmahl, Cryst. Growth Des. 14, 1531 ( 2014 ).

    Article  CAS  Google Scholar 

  65. F. Nindiyasari, E. Griesshaber, L. Fernandez-Diaz, J.M. Astilleros, N. Sanchez-Pastor, A. Ziegler, W.W. Schmahl, Cryst. Growth Des. 14, 4790 ( 2014 ).

    Article  CAS  Google Scholar 

  66. L. Fernandez-Diaz, J.M. Astilleros, C.M. Pina, Chem. Geol. 225, 314 ( 2006 ).

    Article  CAS  Google Scholar 

  67. O. Grassmann, P. Löbmann, Chem. Eur. J. 9, 1310 ( 2003 ).

    Article  CAS  Google Scholar 

  68. Y.Y. Kim, A.S. Schenk, D. Walsh, A.N. Kulak, O. Cespedes, F.C. Meldrum, Nanoscale 6, 852 ( 2014 ).

    Article  CAS  Google Scholar 

  69. H.Y. Li, L.A. Estroff, J. Am. Chem. Soc. 129, 5480 ( 2007 ).

    Article  CAS  Google Scholar 

  70. T. Okumura, M. Suzuki, H. Nagasawa, T. Kogure, J. Cryst. Growth 381, 114 ( 2013 ).

    Article  CAS  Google Scholar 

  71. F. Natalio, T.P. Corrales, M. Panthöfer, D. Schollmeyer, I. Lieberwirth, W.E.G. Müller, M. Kappl, H.J. Butt, W. Tremel, Science 339, 1298 ( 2013 ).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Engineering and Physical Sciences Research Council via grants EP/J018589/1and EP/ H005374/1 (YYK), and Programme Grant ASS EP/I001514/1 which funds the Materials Interface with Biology Consortium. A.S.S. further acknowledges financial support from the Deutsche Forschungsgemein-Schaft. The authors would like to thank Fiona Meldrum and Sabine Ludwigs for valuable advice and inspiring discussions. The authors are grateful to Alex N. Kulak for recording SEM images of Atrina rigida prisms and sea urchin skeletal elements. Andreas Verch is acknowledged for kindly providing an electron micrograph of a coccosphere.

Author information

Authors and Affiliations

  1. Institute of Polymer Chemistry, University of Stuttgart, Germany

    Anna S. Schenk

  2. School of Chemistry, University of Leeds, UK

    Yi-Yeoun Kim

Authors
  1. Anna S. Schenk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yi-Yeoun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anna S. Schenk.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Schenk, A.S., Kim, YY. Unraveling the internal microstructure of biogenic and bioinspired calcite single crystals. MRS Bulletin 40, 499–508 (2015). https://doi.org/10.1557/mrs.2015.100

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1557/mrs.2015.100

Search

Navigation