Biologically Inspired Engineering, National Institutes of Health
National Center for Advancing Translational Sciences grant
UH3TR000522, and National Science Foundation Materials
Research Science and Engineering Center grant DMR-1420570.
K.K.P. was sponsored by National Institutes of Health National Center
for Advancing Translational Sciences grant 1-UG3-HL-141798-01.
S.-J.P. was funded by the Georgia Institute of Technology and
Emory University School of Medicine. G.V.L. was funded by
the Office of Naval Research (T. McKenna, Program Manager,
ONR 341), grant N00014-15-1-2234, and the National Science
Foundation, grant 1830881. H.A.M.A. would like to thank the
American Chemical Society for their generous support through the
Irving S. Sigal Postdoctoral Fellowship. The views and conclusions
contained in this document are those of the authors and should
not be interpreted as representing the official policies, either expressed
or implied, of the National Institutes of Health, the National Science
Foundation, or the US Government. This work was performed in part at
the Harvard Center for Nanoscale Systems, a member of the National
Nanotechnology Infrastructure Network, which is supported by the
National Science Foundation under award ECS-0335765. The Center
for Nanoscale Systems is part of Harvard University.Author
contributions:K.Y.L. and S.-J.P. conceived and designed the study,
developed a geometrically insulated cardiac tissue node-integrated
muscular bilayer construct, designed and performed performance
experiments, analyzed data, organized figures, and wrote the paper.
K.K.P. conceived and designed the study, developed the idea of a
geometrically insulated cardiac tissue node and muscular bilayer, and
supervised the project. A.G.K. and G.V.L. contributed to the concept of
a geometrically insulated cardiac tissue node and muscular bilayer,
respectively. D.M. and G.V.L. contributed to the PIV experiments of both
biohybrid and wild-type fish. S.L.K. designed optogenetic tools and
edited the manuscript. C.M. assisted the fabrication of the biohybrid
fish. S.L.K., J.Z., and H.A.M.A. performed primary neonatal rat ventricular
harvest for the biohybrid fish optimization. All authors contributed to
the preparation of the manuscript;Competing interests:K.Y.L., S.-J.P.,
A.G.K., V.T., and K.K.P. are inventors on a patent filed by HarvardUniversity, U.S. Provisional Patent Application No. 63/299,920, based
on the results described in this manuscript. The remaining authors
declare no competing interests.Data and materials availability:All
data are available in the main text or the supplementary materials.
Code and scripts are available at Zenodo ( 24 )SUPPLEMENTARY MATERIALS
science.org/doi/10.1126/science.abh0474
Materials and Methods
Figs. S1 to S19
References ( 46 – 48 )
MDAR Reproducibility Checklist
Movies S1 to S2516 February 2021; accepted 14 January 2022
10.1126/science.abh0474REPORTS
◥MATERIALS SCIENCE
A damage-tolerant, dual-scale, single-crystalline
microlattice in the knobby starfish,
Protoreasternodosus
Ting Yang^1 †, Hongshun Chen^1 †, Zian Jia^1 , Zhifei Deng^1 , Liuni Chen^1 , Emily M. Peterman^2 ,
James C. Weaver^3 , Ling Li^1 *
Cellular solids (e.g., foams and honeycombs) are widely found in natural and engineering systems
because of their high mechanical efficiency and tailorable properties. While these materials are often
based on polycrystalline or amorphous constituents, here we report an unusual dual-scale, single-
crystalline microlattice found in the biomineralized skeleton of the knobby starfish,Protoreaster
nodosus. This structure has a diamond-triply periodic minimal surface geometry (lattice constant,
approximately 30 micrometers), the [111] direction of which is aligned with thec-axis of the constituent
calcite at the atomic scale. This dual-scale crystallographically coaligned microlattice, which exhibits
lattice-level structural gradients and dislocations, combined with the atomic-level conchoidal fracture
behavior of biogenic calcite, substantially enhances the damage tolerance of this hierarchical biological
microlattice, thus providing important insights for designing synthetic architected cellular solids.
W
eight reduction is often considered a
primary goal when developing struc-
tural materials, which in turn reduces
material usage, energy consumption,
and environmental impact. One effec-
tive solution is through the introduction of
porosity to create cellular solids ( 1 ). Conven-
tional cellular solids include honeycombs and
open- and closed-cell foams with three-dimensional
(3D) stochastic porosities ( 1 ). Recently, archi-
tected cellular materials, enabled by develop-
ments in computational design and additive
manufacturing, further extend the mechanical
property space of conventional cellular solids
while enabling unusual physical properties such
as negative Poisson’s ratio and negative stiffness
( 2 ). Current synthetic architected cellular struc-
tures are exclusively based on either polycrystal-
line or amorphous materials at the atomic scale
( 2 ). These synthetic architected lattice materials
often exhibit catastrophic failure, especially for
those with ceramic and glassy constituents. To
address some of these performance limitations,
and by leveraging the advantages of size effects
and hierarchical design strategies, recent studies
have demonstrated that ceramic nanolattices
can exhibit high energy absorption capabilities
( 2 – 5 ). The strength of these materials, however,
is usually limited by their feature sizes, such as
the wall thickness in hollow nanolattices, which
is maintained in the sub-100-nm range to
achieve high relative strength and recover-
ability ( 2 – 5 ).Widely found in the shallow waters of
the tropical Indo-Pacific, the knobby starfish,
Protoreaster nodosus, is characterized by its
hard, pointy protrusions or“knobs”arranged
radially along its aboral (dorsal) surface (Fig. 1,
A to C). Upon removal of the overlying soft
tissue, a well-organized assembly of the cal-
careous skeletal elements (ossicles) can be re-
vealed with optical microscopy (Fig. 1B and
fig. S1) or microcomputed tomography (m-CT;
Fig. 1C, figs. S2 and S3, and movie S1). Scan-
ning electron microscopy (SEM) reveals that
these millimeter-sized ossicles exhibit a porous
lattice-like structure (Fig. 1, D and E), which
is so ordered that atomic terrace-like mor-
phologies can be observed on the ossicle sur-
faces (yellow arrows, Fig. 1E). Furthermore,
imaging of the fractured surfaces demon-
strates that the periodic microlattice struc-
ture fully extends into the ossicle interiors
(Fig. 1F and fig. S4).
To determine the lattice structure and sym-
metry, we performed quantitative 3D analysis
on a representative high-resolutionm-CT vol-
ume (243 × 243 × 243mm^3 ) extracted from a
single ossicle (Fig. 1G and movie S2). The
skeletonized lattice network demonstrates the
periodic arrangement of the tetrahedron units
withabranchlength(l)of15.5±2.5mm (5499
measurements in total) (Fig. 1H, fig. S5, movie
S3, and materials and methods). The corre-
sponding 3D fast Fourier transform (3D-FFT)
reveals that the most intense reflections result
from the cubic“Fd 3 m”symmetry, such as the
{111} and {220} families, confirming the diamond
microlattice structure in these ossicles (Fig. 1I,
figs. S6 to S8, and movie S4) ( 6 ). Measurement of
the reciprocal lattice constants from the 3D-FFT
data reveals a lattice constant (a)of34.0±5.9mm,
which is in excellent correspondence with the
real-space measurements (a=4l/ffiffiffi
3p
for a
diamond lattice). In addition to the standard
“Fd 3 m”reflections,“symmetry-forbidden”
intensity spots corresponding to the {HKL}
planes withH+K+L=4n+2(wherenis
an integer) were also observed, for example,
the {002} family (circled in green, Fig. 1I andSCIENCEscience.org 11 FEBRUARY 2022•VOL 375 ISSUE 6581 647
(^1) Department of Mechanical Engineering, Virginia Polytechnic
Institute and State University, Blacksburg, VA 24061, USA.
(^2) Earth and Oceanographic Science, Bowdoin College,
Brunswick, ME 04011, USA.^3 Wyss Institute for Biologically
Inspired Engineering, Harvard University, Cambridge, MA
02138, USA.
*Corresponding author. Email: [email protected]
†These authors contributed equally to this work.
RESEARCH