news & views

the Department of Electrical and Computer References 6. Sharvin, Y. V. Sov. Phys. JETP 21, 655–656 (1965).
Engineering, and Department of Materials Science 1. Radisavlejevic, B., Radenovic, A., Brivio, J., Giacometti, V. & 7. Datta, S., Assad, F. & Lundstrom, M. S. Superlattices Microstructures
Kis, A. Nature Nanotech. 6, 147–150 (2011). 23, 771–780 (1998).
& Engineering, Cornell University, New York 14853, 2. Kappera, R. et al. Nature Mater. 13, 1128–1134 (2014). 8. Van Wees, B. et al. Phys. Rev. Lett. 60, 848–850 (1988).
USA. Kaustav Banerjee is in the Department of 3. Lin, Y.‑C., Dumnenco, D. O., Huang, Y.‑S. & Suenaga, K. 9. Maassen, J., Jeong, C., Baraskar, A., Rodwell, M. & Lundstrom, M.
Electrical and Computer Engineering, University of Nature Nanotech. 9, 391–396 (2014). Appl. Phys. Lett. 102, 111605 (2013).
4. Maxwell, J. C. A Treatise on Electricity and Magnetism 10. Yang, L. et al. VLSI Technol. Digest of Tech. Papers, 2014
California, Santa Barbara, California 93106, USA. (Clarendon, 1904). Symposium on, 238–239 (2014); http:dx.doi.org/10.1109/
e-mail: djena@nd.edu 5. Landauer, R. IBM J. Res. Dev. 1, 223–231 (1957). VLSIT.2014.6894432

BIOMINERALIZATION

Crystals competing for space

Analysis of the growth patterns of calcitic prisms within the shell of the fan mollusc Pinna nobilis shows that growth
can be predicted using grain theory and that the organic casings of the prisms set the thermodynamic boundaries.

Nico A. J. M. Sommerdijk and Maggie Cusack

B
iominerals, such as bone, teeth and structure, size and morphology of the evolution of calcite prisms in a mollusc,
shells, are organic–inorganic composite resulting material2. Moreover, through these and show that the prismatic structure
materials with often amazingly interactions the structure and properties and morphology can be predicted by
complex shapes and structures. Biology of the biological hybrids are precisely classical thermodynamic theories3. Using
uses a variety of minerals to form these tuned towards their specific functions: for synchrotron-based microtomography, they
structures — most commonly, calcium example, navigation, mechanical support, analyse the mesostructure of the prisms
carbonate (CaCO3) and calcium phosphate, photonics and protection against predation, forming the calcitic outer layer of the giant
which are used by marine invertebrates often producing physical structures that Mediterranean fan mollusc Pinna nobilis
and vertebrates, respectively, as well as iron surpass those of synthetic analogues. and conclude that only a minimal amount
oxides and silica1. Growth of biominerals is However, the extent to which the growth of biological control is used to create the
thought to be controlled by their interaction of biominerals is controlled by their well-organized prismatic crystals. Indeed,
with a complex organic macromolecular interaction with these organic matrices, other than setting the boundary conditions
matrix that consists of a specialized and whether there is also control through of the thermodynamics involved in the
dynamic assembly of (glyco)proteins and classical thermodynamic parameters, process, the findings of Zlotnikov and
carbohydrate polymers. As a consequence remains unclear. colleagues suggest that the biological
of these interactions, a high level of Writing in Nature Materials, Zlotnikov organism has little involvement in the
control is achieved over the composition, and colleagues now shed light on the shape formation of the finer structural detail of the
outer layer of its shell.
a b Biomineralization has intrigued
scientists for many decades and serves as
a constant source of inspiration for the
development of new materials with highly
controllable and specialized properties4.
Also, because biological materials are
normally synthesized in aqueous media
and at ambient temperatures — conditions
that are prerequisites for the synthesis of
green materials — a richer understanding
of the biomineralization process may open
new sustainable pathways to materials
with advanced functional and structural
properties. Moreover, the findings reported
by Zlotnikov and colleagues point towards
the simpler nature of the factors that
control this particular biomineralization
process, and if similar strategies could
be exploited by synthetic chemists the
Figure 1 | Secondary electron images of the calcite prisms and organic casings of the shell of the fan accessibility of green synthesis routes could
mollusc, Atrina vexillum. a, Fracture section of the shell of A. vexillum showing the oriented calcite crystals be greatly improved.
in the prismatic layer of the shell. Scale bar, 250 μm. b, The organic casings in which the prisms grow. As a result of their abundance in
The prisms were dissolved by incubation in acetic acid (1 M) for 24 h. Scale bar, 50 μm. Images courtesy nature, biological materials composed of
of Peter Chung (a,b) and Maggie Cusack (b), University of Glasgow. CaCO3, for example mollusc shells, are the

1078 NATURE MATERIALS | VOL 13 | DECEMBER 2014 | www.nature.com/naturematerials

© 2014 Macmillan Publishers Limited. All rights reserved

 news & views

focus of many biomineralization studies5.

Shells of marine bivalve molluscs, such as
Pinna nobilis, comprise two mineral layers,
each of a different CaCO3 polymorph: an
outer calcite layer and an inner aragonite Growth
nacre layer. During growth of this
bimineralic shell the mollusc produces, in
tandem, each of these polymorphs. The
inner smooth layer of nacre is formed by G1
stacked oriented aragonite tablets organized
in a brick-wall-like structure that we know
G4
as Mother of Pearl, whereas the outside
consists of a layer of oriented calcite prisms G3
forming a palisade-like arrangement. The
formation of the calcite prisms begins G2 G5 G1
with the laying down of an organic matrix,
which is thought to determine the size,
G4
shape, orientation, polymorph and the
spatial arrangement of the crystals. In vitro G3
experiments have shown that organic
molecules can indeed direct the orientation G5
G2
and determine polymorph selection of
CaCO3 crystals6. Growing these crystals
in the confines of a bio-matrix leads to the
production of single crystals with intriguing,
non-equilibrium shapes7 as seen in Fig. 1 Figure 2 | A schematic representation showing the evolution of prism diameter during the growth of
for another fan mussel, Atrina vexillum. The calcitic prisms in Pinna nobilis. The cross-sections on the left- and right-hand sides show the prisms at
organic matrices within which these types of early and late growth stages, respectively. At the early stages of growth (left-hand side) the prisms with
crystal grow, consist of complex assemblies cross-sectional surfaces larger than the average (pink, G1–G5) are growing, whereas the ones with cross-
of insoluble biopolymers and a variety of sections smaller than the average (blue) are shrinking and will eventually disappear (right-hand side).
associated biomacromolecules8 that are Figure adapted from ref. 3, 2014 Nature Publishing Group.
thought to play different, complementary
roles in controlling crystal growth9. Looking
at the precisely organized structure of the neighbour or being out-competed. Thus, this design and synthesize advanced materials
mollusc shell one is inclined to believe analysis not only presents a thermodynamic without trying to achieve growth control
that the organism does indeed control explanation for growth of the calcite prisms by mimicking a complex multicomponent
the formation of these crystals both at the but also highlights the often ignored matrix, but by relying on the competition
macro- and nanoscale in fine detail. But is dynamic interplay of organic and mineral between domains driven by the
this really the case? components in biomineral formation. minimization of interfacial energy. ❐
Zlotnikov and colleagues reconstruct It would be interesting to assess such
the three-dimensional organization of the a thermodynamic model in other shell Nico A. J. M. Sommerdijk is in the Laboratory of
crystal assembly within the calcite outer structures such as the aragonite nacreous Materials and Interface Chemistry & Soft Matter
layer of the Pinna nobilis shell (Fig. 2). By inner layer of Pinna nobilis. Other common CryoTEM Research Unit, of the Department of
considering that the length of the crystals calcite biomineral structures are brachiopod Chemical Engineering and Chemistry, and in
is directly proportional to their growth fibres, which are analogous to molluscan the Institute for Complex Molecular Systems, at
time, Zlotnikov and colleagues demonstrate prisms in that they are encased in an organic Eindhoven University of Technology, 5600 MB
that during their development the prisms sheath, but in this case the fibres run Eindhoven, The Netherlands. Maggie Cusack is in
that have larger diameters than the average parallel with the shell outer surface so the the School of Geographical and Earth Science at the
will grow at the expense of those that have same space competition does not apply 7. It University of Glasgow, Glasgow G12 8QQ, UK.
smaller diameters. They analysed this would be worthwhile to probe whether or e-mail: n.sommerdijk@tue.nl;
evolution and concluded that the pattern not biology sets different thermodynamic Maggie.Cusack@glasgow.ac.uk
of growth of these prisms can be predicted boundary conditions for a structure that
References
using theories of grain growth in, for is completely different. If biology is able to 1. Lowenstam, H. A. & Weiner, S. On Biomineralization
example, metals, where the prisms are the do so, the implications for growth rate and (Oxford Univ. Press, 1989).
equivalent of grains. Prism growth where metabolic efficiencies in various biomineral 2. Weiner, S. & Addadi, L. J. Mater. Chem.
7, 689–702 (1997).
one prism out-competes another can be ultrastructures, not just prisms, would be 3. Bayerlein, B. et al. Nature Mater. 13, 1102–1107 (2014).
explained by the interplay between energetic important factors to consider. 4. Nudelman, F. & Sommerdijk, N. A. J. M. Angew. Chem. Int. Ed.
equilibrium and topological requirements From this study, biology shows us a 51, 6582–6596 (2012).
5. Cusack, M. & Freer, A. Chem. Rev. 108, 4433–4454 (2008).
for space filling. By depositing the organic minimalistic approach to the formation 6. Pouget, E. M. et al. Science 323, 1455–1458 (2009).
matrix first, before mineral formation, of highly ordered assemblies of crystals 7. Cusack, M., Dauphin, Y., Chung, P., Perez-Huerta, A. &
biology sets the thermodynamic boundary with near uniform sizes, shapes and Cuif, J. P. J. Struct. Biol. 164, 96–100 (2008).
conditions. As prism growth proceeds, the orientation by crystallization from solution. 8. Marin, F., Narayanappa, P. & Motreuil, S. Prog. Mol. Subcell. Biol.
52, 353–395 (2011).
dimensions of the organic casing responds What remains to be seen is whether we 9. Nudelman, F., Chen, H. H., Goldberg, H. A., Weiner, S. &
to whether a prism is out-competing a can apply these insights to materials Addadi, L. Farad. Discuss. 136, 9–25 (2007).

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