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ACKNOWLEDGMENTS
We thank the staff at the University of California (UC), Berkeley,
Electron Microscopy Lab for advice in electron microscopy sample
preparation and data collection. We thank P. Risch and M. Sanjaya
for providing reference samples. We thank A. Warmbold for the
thermogravimetric analysis measurement. We thank S. Kumar’s lab
at UC Berkeley for allowing use of the rheometer. We would like
to thank the anonymous reviewers for their time and valuable critique.
Funding:This work was funded by the National Science Foundation
under cooperative agreement no. EEC-1160494 (J.T.T., C.C.L., H.K.T.);
the European Research Council (ERC) under the European Union’s
Horizon 2020 Research and Innovation Programme (grant agreement
nos. 816006 to M.L. and 825521 to S.J.); the Carl Zeiss Foundation
as a part of the Research Cluster“Interactive and Programmable
Materials (IPROM)”; the German Research Foundation (Deutsche
Forschungsgemeinschaft, DFG) through the Centre for Excellence
livMatS Exec 2193/1–project number 390951807 (B.E.R.); the German
Research Foundation (Deutsche Forschungsgemeinschaft, DFG)
project number 455798326 (F.K.-H.); and the Lawrence Livermore
National Laboratory Directed Research and Development program.
The work was performed under the auspices of the US Department
of Energy by Lawrence Livermore National Laboratory under
contract DE-AC52-07NA27344 (LLNL-JRNL-826682) (C.C.C.).
Author contributions:Conceptualization: J.T.T., F.K.-H., H.K.T.;
Methodology: J.T.T., M.L., F.K.-H.; Investigation: J.T.T., M.L., C.C.C.,
S.J., C.C.L.; Visualization: J.T.T.; Funding acquisition: H.K.T.,
F.K.-H., B.E.R.; Project administration: H.K.T., F.K.-H., J.T.T.;
Supervision: F.K.-H., H.K.T., B.E.R.; Writing–original draft: J.T.T.;Writing–review and editing: All authors.Competing interests:
H.K.T. holds US patent 10,647,061 relating to computed axial
lithography. B.E.R. and F.K.-H. hold US patent 10,954,155 B2 relating
to the silica nanocomposite material described in this paper.
F.K.-H. and B.E.R. are co-founders of, and have an equity interest in,
Glassomer GmbH. The authors declare that they have no other
competing interests.Data and materials availability:All data are
available in the main text or the supplementary materials. Code
used to analyze and visualize data is available upon request.SUPPLEMENTARY MATERIALS
science.org/doi/10.1126/science.abm6459
Materials and Methods
Supplementary Text
Figs. S1 to S23
Tables S1 to S9
References ( 33 – 46 )
30 September 2021; accepted 23 February 2022
10.1126/science.abm6459MATERIALS SCIENCE
Complex morphologies of biogenic crystals emerge
from anisotropic growth of symmetry-related facets
Emanuel M. Avrahami^1 , Lothar Houben^2 , Lior Aram^1 , Assaf Gal^1 *
Directing crystal growth into complex morphologies is challenging, as crystals tend to adopt
thermodynamically stable morphologies. However, many organisms form crystals with intricate
morphologies, as exemplified by coccoliths, microscopic calcite crystal arrays produced by unicellular
algae. The complex morphologies of the coccolith crystals were hypothesized to materialize from
numerous crystallographic facets, stabilized by fine-tuned interactions between organic molecules and
the growing crystals. Using electron tomography, we examined multiple stages of coccolith development
in three dimensions. We found that the crystals express only one set of symmetry-related
crystallographic facets, which grow differentially to yield highly anisotropic shapes. Morphological
chirality arises from positioning the crystals along specific edges of these same facets. Our findings
suggest that growth rate manipulations are sufficient to yield complex crystalline morphologies.
C
ontrol over nanoscale morphologies of
crystalline materials is connected to
their physical properties and thus their
potential applications ( 1 – 3 ). However,
the inherent thermodynamic properties
of the crystalline lattice dictate a strong ten-
dency toward specific low-energy facets, re-
sulting in characteristic shapes (habits) ( 4 ). In
contrast, many organisms evolved the ability
to form intricate crystalline structures with
hierarchical organization, out of very simple
materials and under ambient conditions. In
such biomineralization processes, the poly-
morph of the crystal, its nucleation site, orien-
tation, and eventual morphology, are all under
strict control ( 5 – 7 ).
Coccoliths—micrometer-sized calcite (calcium
carbonate) scales formed by unicellular algae
called coccolithophores—are a prime example
of biological control over crystal morphogen-
esis. Each coccolith is composed of crystalline
subunits and has intricate species-specific
morphology ( 8 , 9 ). Coccoliths are made intra-
cellularly within a specialized vesicle known as
the coccolith vesicle, into which calcium and
carbonate ions are delivered ( 10 , 11 ). Inside the
coccolith vesicle, crystals nucleate and grow
around the rim of an organic base plate ( 8 , 12 ).
A common feature of coccolith architectures
is an alternating arrangement of crystal units,
as identified in the V/R model ( 13 ). Accord-
ing to the model, two unit types make up a
coccolith—a V-unit and an R-unit—possessing
either a vertical or a radial orientation of the
calcitecaxis relative to the base plate. The
units initially possess a pseudo-rhombohedral
morphology that closely resembles the thermo-
dynamically stable {104} calcite rhombohedron
( 14 , 15 ). Nonetheless, upon completion, their
morphology is highly convoluted, displaying
various surfaces that deviate markedly from
the simple rhombohedral habit ( 8 , 14 ).
The consensus view on coccolith morpho-
genesis is reliant on biomolecules as the
“sculptor’s toolkit.”The rationale is that
specific stereochemical interactions with the
growing crystals allow such biomoleculesto funnel the process away from the stable
thermodynamic path, and into local kinetic
minima, giving rise to potentially unlimited
morphologies ( 6 , 16 – 21 ). Presumably, crystal
nucleation is the result of epitaxy from the
base plate, and crystal growth produces various
types of crystallographic facets stabilized by
“tailored”biomolecules. It has also been sug-
gested that stereospecific interactions with
chiral organic modifiers induce chirality to
the habit of calcite ( 21 – 23 ).
To elucidate the morphological develop-
ment of coccolith crystals, we investigated
the large coccoliths ofCalcidiscus leptoporus,
which have a characteristic double-shield ultra-
structure (Fig. 1A). To create a timeline of
coccolith growth, we established a procedure
for extracting intracellular coccoliths (ICCs).
First, extracellular coccoliths of actively calci-
fying cells were removed with a short acid
exposure. Next, a hypotonic solution was used
to burst the cells, thus releasing their ICCs. By
tuning the pH and chemistry of the hypotonic
solution, we ensured that crystal morpholo-
gies were unaffected (figs. S1 to S3 and sup-
plementary text). Therefore, the ICCs serve
as“snapshots in time”of the dynamic devel-
opment of the crystals.
Scanning electron microscopy (SEM) images
of the extracted ICCs (Fig. 1) show a sequence
of evolving intermediate morphologies from
small, 100- to 200-nm rhombohedra to fully
formed chiral coccoliths (see also fig. S4). The
overall chirality of the structure is evident even
in the arrangement of the initial units, which
resembles the isotropic rhombohedral habit of
calcite (Fig. 1, E and I). Two distinct surface
types of the crystals were observed: (i) flat
facets with straight edges, characterizing
the distal sides of both shields (Fig. 1, purple
arrowheads), and (ii) curved and smooth
surfaces, characterizing the proximal sides of
the two shields and stem region (Fig. 1, green
arrowheads).
We used high-resolution electron tomogra-
phy to investigate crystal morphologies of312 15 APRIL 2022•VOL 376 ISSUE 6590 science.orgSCIENCE
(^1) Department of Plant and Environmental Sciences, Weizmann
Institute of Science, Rehovot, Israel.^2 Department of
Chemical Research Support, Weizmann Institute of Science,
Rehovot, Israel.
*Corresponding author. Email: [email protected]
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