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Article
Biomimetic discontinuous Bouligand
structural design enables high-performance
nanocomposites
Si-Ming Chen, KaiJin Wu,
Huai-Ling Gao, ..., HengAn Wu,
Yong Ni, Shu-Hong Yu

ghuailing@ustc.edu.cn (H.-L.G.)
shyu@ustc.edu.cn (S.-H.Y.)

Highlights
Introduction of discontinuous
structural characteristics into
Bouligand structures

Programmable and universal

nanofiber assembly strategy is
developed

Construction of biomimetic
discontinuous Bouligand
structural nanocomposites

Synergistic toughening
mechanisms via crack twisting and
fiber bridging

Nanofiber-based composites with biomimetic discontinuous Bouligand structures

are successfully prepared. The combination of discontinuous structure with small-
angle twisted Bouligand structure here is demonstrated to achieve synergistically
improved mechanical properties. The resultant nanocomposites can be in the form
of thin film or thick bulk, according to different application requirements. The
proposed discontinuous Bouligand structural design will promote the
development of fiber-reinforced composites for structural applications.

Chen et al., Matter 5, 1–15

May 4, 2022 ª 2022 Elsevier Inc.
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Article
Biomimetic discontinuous Bouligand structural
design enables high-performance nanocomposites
Si-Ming Chen,1 KaiJin Wu,2 Huai-Ling Gao,1,* XiaoHao Sun,3 Si-Chao Zhang,1 Xin-Yu Li,1
Zhen-Bang Zhang,1 Shao-Meng Wen,1 YinBo Zhu,2 HengAn Wu,2 Yong Ni,2 and Shu-Hong Yu1,2,4,*

SUMMARY Progress and potential

Bouligand structures across several species invariably hold the me- In natural bio-composites,
chanical foundation for the survival of living organisms. Transcribing Bouligand structures with rotated
them into synthetic analogues will promote the development of struc- nanofiber arrangements are
tural materials. Although superior nanofibers emerge continuously, important for mechanical
arranging them into structurally and mechanically optimized biomi- protection. Creatively
metic assemblies remains challenging. Here, we propose a program- constructing biomimetic
mable assembly strategy and construct discontinuous Bouligand Bouligand structural
structural nanocomposites with eco-friendly, silicon-based nanofibers nanocomposites is meaningful for
and biopolymer. Unique helicoidal organization and discontinuity the advancement of structural
enable the resultant nanocomposites’ synergetic toughening via materials but remains challenging
crack twisting and fiber bridging. The optimal nanocomposite ex- due to limited nanofiber assembly
hibits superior tensile strength (356.1 MPa), energy absorption techniques. Here, we propose a
(28.8 MJ m
3), and fatigue durability (more than 30,000 bending cy- conception of discontinuous
cles), outperforming many natural and synthetic Bouligand structural Bouligand structure, develop a
analogues. They hold potential as sustainable materials for mechani- programmable nanofiber
cal protection or tissue engineering. The discontinuous Bouligand assembly system, and ultimately
structural design proposed here, combining the programmable nano- construct biomimetic
fiber assembly strategies, will drive innovation of traditional contin- discontinuous Bouligand
uous macrofiber-reinforced plastics and help creation of advanced structural nanocomposites. Under
nanofibrous composites. external loads, synergistic
toughening via crack twisting and
fiber bridging largely determines
INTRODUCTION the superior mechanical
Bouligand structure is composed of unidirectional nanofiber lamellae that are heli- performance of the
coidally stacked.1 This structural organization is widely found in natural biological nanocomposites, demonstrating
materials.2–4 Periodic Bouligand spiral zone of the hammer of mantis shrimp can the merits of bringing
facilitate energy absorption and inhibit crack when rapidly striking prey.5 Bouligand discontinuous characteristics into
arrangement of collagenous lamellae in fish scale highlights armor’s role against the Bouligand structures. The
fierce attack from piranha.4 Cylindrical Bouligand structural osteon endows bone discontinuous Bouligand
with excellent fracture resistance.2 Although existing in different species, it demon- structural design combined with
strates invariable mechanical functions through remarkable interlayer coupling, the proposed nanofiber assembly
effective stress transfer, and twisted crack propagation. strategy is expected to lead the
development of advanced
These natural nanocomposites strongly illustrate that excellent mechanical proper- biomimetic nanofibrous
ties are tightly correlated with ordered arrangements of their nanofiber building composites for structural
blocks.6–8 Compared with nature, engineering fibrous composites, such as contin- applications.
uous macrofiber-reinforced plastics, look less impressive, whether in structural
hierarchy, accuracy, or even in performance.9–11 Nacre is another natural model
for mechanical study; the staggered arrangement of discontinuous microplatelets
that feature pull out and slippage for toughening attracts considerable atten-
tion.2,12–16 Overall, natural materials maximize their hierarchies and accuracies

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that cannot be reached by existing engineering materials, and they are inspiring
extensive bionics studies for high-performance nanocomposites.

In the past, considerable progress has been made in the fabrication of biomimetic
Bouligand structural nanocomposites and nacre-inspired nanocomposites.7,17
Langmuir-Schaefer strategy was developed in constructing beetle-cuticle-inspired
Bouligand structural NiMoO4$xH2O nanowire assemblies for chiral photonic crys-
tals.18 Electrospinning technique was exploited to helicoidally arrange continuous
nylon nanofibers and polyvinyl alcohol nanofibers into impact-resistant Bouligand
structural film and hydrogel.19,20 Helical self-assembly and fields-assisted 3D print-
ing techniques were also developed for Bouligand structural design.21–24 In addi-
tion, various methods for fabricating nacre-inspired layered nanocomposites have
been developed.2,12,16 These studies have verified the structurally biomimetic
effectiveness for optimizing materials’ properties. However, natural wisdoms are still
underused; coupling the fibrous Bouligand structure and discontinuous nacreous
staggered structure together to design high-performance nanocomposites and un-
derstanding structurally cooperative mechanical effects remain largely unexploited.
Although the advantages of the discontinuous Bouligand structure have been
proven theoretically,8 how to use superior nanofiber building blocks to construct
this structure and achieve desired performance optimization remains challenging.

Here, we present a programmable sliding-shear-induced assembly strategy to con-

trollably align discrete nanofiber building blocks to bring the discontinuous stag-
gered structural characteristic into Bouligand structure and achieve synergetic
toughening. Discrete silicon-based xonotlite (CaSi) nanofibers and natural
biopolymer sodium alginate (SA) are used as reinforcement and matrix, partly due
to their eco-friendliness and accessibility.25,26 By helical assembly of CaSi nanofibers
in SA solution and sol-gel-film transition, we fabricate macroscale biomimetic
discontinuous Bouligand structural nanocomposites. The resultant nanocomposites
exhibit superior mechanical performance, surpassing many natural and biomimetic
Bouligand structural counterparts, and engineering materials. They hold great
promise as sustainable materials for mechanically protective and biomedical appli-
cations. The implementation of the discontinuous Bouligand structural design and
the programmable assembly strategy will facilitate the creation of advanced nano-
composites from more nanofiber building blocks.
1Divisionof Nanomaterials & Chemistry, Hefei
National Laboratory for Physical Sciences at the
Microscale, Institute of Energy, Hefei
RESULTS AND DISCUSSION Comprehensive National Science Center, CAS
The construction of biomimetic discontinuous Bouligand structure can be divided Center for Excellence in Nanoscience,
Department of Chemistry, Institute of Biomimetic
into two steps, including unidirectionally aligning discrete nanofibers and helically Materials & Chemistry, Anhui Engineering
stacking the obtained nanofiber lamellae. An integrated manufacturing system, Laboratory of Biomimetic Materials, University of
Science and Technology of China, Hefei 230026,
including several modules of solution injection and transport, sliding brushing on China
the substrate, platform rotation, and heat drying, was designed to achieve this struc- 2CAS Key Laboratory of Mechanical Behavior and
ture (Figure 1A; details can be seen in experimental procedures). Under the influ- Design of Materials, CAS Center for Excellence in
Complex System Mechanics, Department of
ence of wet sliding shear force, CaSi (Ca6(Si6O17)(OH)2) nanofibers (diameter:
Modern Mechanics, University of Science and
20–30 nm; length: up to 10 mm; Figure S1) are expected to arrange in the control- Technology of China, Hefei 230026, China
lable manner (bottom right inset in Figure 1A) due to their discontinuity, high aspect 3Department of Mechanical Engineering,
ratio (300–500) and good interfacial interaction with SA matrix (Figure S2).14,27 The University of Colorado, Boulder, Boulder, CO
80309, USA
advantage of the sliding-shear-induced nanofiber assembly strategy lies in wide 4Lead contact
applicability; it does not require special properties (such as electric or magnetic field
*Correspondence:
responsiveness, helical self-assembly, etc.) of nanofibers themselves.21–24 With ghuailing@ustc.edu.cn (H.-L.G.),
further assistance of heat drying process, nanocomposite films with ordered shyu@ustc.edu.cn (S.-H.Y.)
arrangement of CaSi nanofibers can be obtained. As revealed by scanning electron https://doi.org/10.1016/j.matt.2022.02.023

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B C

Figure 1. The programmable nanofiber assembly system and biomimetic discontinuous

Bouligand structure
(A) Schematic of the programmable assembly system, including several modules. Bottom right
inset is the schematic of sliding-induced nanofiber alignment; arrow indicates sliding direction.
(B) Schematic of the discontinuous Bouligand structure assembled by discrete nanofibers.
Semicircular yellow arrow indicates gradually twisted alignment of nanofibers within one complete
Bouligand structural period.
(C) Cross-sectional SEM image of the prepared biomimetic 20  twisted nanocomposite, showing
helicoidal arrangement of CaSi nanofibers. Curved yellow arrow indicates gradually twisted
alignment of nanofibers within a partial period.

microscope (SEM) and orderliness-related calculation, different contents of CaSi

nanofibers all can arrange unidirectionally in SA matrix (Figures S3–S8). The ob-
tained ordered structure contrasts sharply to the structure obtained from uncon-
trolled self-deposition process (Figure S9).

Then, biomimetic nanocomposite films with discontinuous Bouligand arrangement

of CaSi nanofibers can be facilely prepared with the assistance of platform rotation
(Figure 1B). The mass fraction of CaSi nanofibers in the biomimetic nanocomposites
was set as 20 wt % according to the experimentally optimal tensile strength of uni-
directional films (Figure S10).13 Nanocomposites mentioned below are all prepared
based on this ratio. Here, the rotation angles were set as 20 , 30 , 45 , and 90 ,
respectively, to verify the structural controllability of the proposed assembly method
and explore the structure-performance relationship. As shown in Figures 1C, 2A–2D,
and S11–S17, nanocomposite films with twisted and 90 crossed nanofiber align-
ment were fabricated. Periodic or gradient fracture patterns (or light-dark change)
at the cross sections of these films are visible.5,7,28 Furthermore, taking the polished

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A E
a1 a2 B

C D F

G H

Figure 2. The cross-sectional microstructures of the prepared films and nanoindentation tests
(A) Cross-sectional SEM images of the unidirectional film. White points are endpoints of nanofibers. Yellow dot in a 1 and short line in a 2 indicate
nanofiber alignment direction parallel and perpendicular to the viewing direction, respectively.
(B) Cross-sectional SEM image of the biomimetic 20 twisted film. The nearly gradient-distributed white points (through thickness direction) reflect
helicoidal organization of nanofibers.
(C and D) Cross-sectional SEM images of different magnifications showing the film with 90  crossed angle.
(E) Schematic of nanoindentation. Red arrow indicates that the needle tip travels across two structural periods through thickness direction. The relative
angle variation between needle tip and nanofiber axis will affect mechanical responses.
(F) Representative load-displacement curves of nanoindentation on different locations of the biomimetic 20  twisted film.
(G and H) Scatter diagrams of modulus position and hardness position, measured by nanoindentation of the biomimetic 20 twisted film.

cross section of the film with 20 deviation angle as an example, we performed nano-
indentation test, which is often used in the characterization of natural Bouligand
structural materials.5,29–33 The nearly regular variation (periodic oscillation) of
modulus and hardness with varying indentation positions means that the orientation
of CaSi nanofibers is gradually changed,5,30,31 partly certifying the realization of the
designed Bouligand structure (Figures 2E–2H and S18).

Bouligand structure and discontinuous nacreous staggered structure endow natural

materials with excellent mechanical properties. It is interesting and meaningful to
explore the influence of the discontinuous Bouligand structure (or the coupled struc-
ture) on the mechanical behavior of materials. Here, systematic mechanical studies
were performed on these prepared nanocomposites. For uniaxial tensile test, as
shown in Figures 3A–3C and S19, the biomimetic discontinuous Bouligand structural

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A B C

D E F

G H

Figure 3. The uniaxial tensile properties of the films with different twisted angles
(A–C) Tensile strength, energy absorption per unit volume, and Young’s modulus of the films, respectively. For 0  deviation angle (unidirectional) case,
the loading direction is perpendicular to the nanofiber axis.
(D and E) Strength comparison of the films with engineering plastics (D) and natural materials (E).
(F–H) Strength and toughness comparisons of the films with the reported biomimetic materials with similar constituents (F), natural Bouligand structural
materials (G), and the reported biomimetic Bouligand structural materials (H).
Data in (A–C) are represented as mean G SEM.

nanocomposite film with small (20 ) deviation angle exhibits optimal strength
(356.1 MPa), elongation at break (14.1%), and energy absorption per unit volume
(28.8 MJ m
3), outperforming the prepared nanocomposites with bigger deviation
angles and with disordered structure (Figure S20). The optimal small-angle helicoi-
dal organization is possibly associated with the well interlayer coupling capability
that alleviates the local stress concentration and nanofiber reorientation strength-
ening.4 These obtained mechanical parameters are superior to those of many natural
Bouligand structural materials (fish scale, lamellar bone, hammer of mantis shrimp,
and exoskeleton of crab), reported biomimetic analogues (cellulose nanocrystal-
polyvinyl alcohol [PVA], carbon fiber-acrylonitrile-butadiene-styrene [ABS], nylon

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A B C

D E

F G

Figure 4. The tear-associated energy absorption per unit volume and crack propagation of the films with different twisted angles
(A) Tear-associated energy absorption per unit volume of the films. Inset is the schematic of tear test.
(B and C) SEM images of fracture surface of the unidirectional film. Notch direction is parallel to nanofiber axis.
(D) SEM image of fracture surface of the 20  twisted film.
(E) Enlarged view of (D).
(F) Further enlarged view of (E); yellow area indicates fiber bridging zone (FBZ), and orange area indicates crack twisting zone (CTZ). The combination of
CTZ and FBZ underlying the 20  twisted film partially reflects the mechanical advantages of the discontinuous Bouligand structure. White arrows
indicate the stretching and tearing of SA matrix.
(G) Simulated crack morphology of the 20  twisted Bouligand structure, which is composed of alternated CTZ and FBZ.
Data in (A) are represented as mean G SEM.

fiber-epoxy, and SiC fiber-polymethyl methacrylate [PMMA] composites), and engi-

neering plastics (Figures 3D, 3G, and 3H; Tables S1–S3).10,34 In addition, they sur-
pass those of many other natural structural materials (nacre, dentine, and
bamboo)35–38 and biomimetic materials with similar constituents (Figures 3E and
3F; Tables S4 and S5). When taking density into account for structural applications,
the density of the prepared nanocomposites (1.62 g cm
3) here is still relatively
higher than that of pure organic natural and synthetic materials while comparable
to that of many composites (Tables S1–S5).

In addition to tensile resistance, the superiority of the biomimetic discontinuous

Bouligand structure also manifested in tear resistance. As shown in Figure 4A, the
optimal tear-associated energy absorption per unit volume exists in the biomimetic
nanocomposite film with small deviation angle. Specifically, the energy absorption
per unit volume of the 20 twisted film is as high as 1.54 MJ m
3, which is 2.3 times

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that of the unidirectional case (0.67 MJ m
3), 1.79 times that of the 90 crossed case
(0.86 MJ m
3), and 1.28 times that of the 45 twisted case (1.2 MJ m
3). The failure
zones near the cracks were captured by digital images (Figure S21). We can see that
the small-angle twisted film exhibits much larger stress-related whitening zone,
which implies the increased plastic yielding zone and energy dissipation.39 The dif-
ference in whitening drives us to examine the fracture surface morphology. For the
unidirectional film (notch direction is parallel to nanofiber axis), crack propagates
mainly through SA matrix via interface damage mode. The exposed nanofibers are
parallel to crack surface, and a relatively flat fracture surface was observed (Figures
4B and 4C). For the biomimetic nanocomposite films with small deviation angles
(especially the 20 twisted case), the fracture surfaces exhibit periodic morphologies
through thickness direction (Figures 4D–4F, S22, and S23), partly reflecting twisted
crack propagation, extensive energy dissipation, and thus the mechanical advan-
tage of Bouligand structure. These crack characteristics are obviously different
from those of the unidirectional anisotropic film (Figures 4B and 4C) and the 90
crossed structural film that features pull-out of nanofibers with hardly any crack
twisting signal (Figure S24). In addition, the unique periodic twisted crack propaga-
tion can be found in a pre-notched thick laminate with 20 twisted structure under
three-point bending load (Figure S25), which reflects the similarity with that of nat-
ural biological tissues, such as Bouligand structural lamellar bone,40 and further ver-
ifies the robustness of constructing macroscale biomimetic discontinuous Bouligand
structure.

Natural Bouligand structural materials are constructed from hierarchically arranged

nanofiber building blocks.4,6,16 Conversely, engineering Bouligand structural mate-
rials or fibrous laminates are often composed of continuous micromillimeter-sized
fibers,28,41 which motivates us that the biomimetic Bouligand structural design im-
plemented here based on discontinuous nanofibers will result in rich interfaces for
toughening. The interface-derived toughening can be understood from the activ-
ities of CaSi nanofibers and surrounding SA matrix. SEM images of fracture surfaces
provide some clues. Given the discontinuity of the nanofibers and the derived pull-
out and slippage behavior, the periodic fracture surfaces can be further roughened
in each microlayer (constructed by one time of brushing process), exhibiting
enlarged crack area, wide stress distribution, and high energy dissipation (Figures
4D–4F, S22, and S23). In addition, the stretching and tearing of SA matrix can be
found, further reflecting large plastic deformation and additional energy dissipation
(Figure 4F). It can be concluded that the mechanical superiority brought by discon-
tinuous nanofibers reflects the rationality of introducing discontinuous structural
characteristic (more interface) into Bouligand structure. Mechanical simulations
were performed to provide qualitative insights into the crack propagation and dam-
age morphology in the biomimetic discontinuous Bouligand structure (details can
be seen in experimental procedures). For the nanofibrous helicoidal organization
under uniaxial tension, crack can partly extend following the twisted nanofiber orien-
tation and forming crack twisting zone (CTZ), when the nanofiber lamellae deviated
from the tensile direction. For the lamellae where nanofibers were nearly parallel to
the loading direction, nanofibers would be pulled out or broken because they were
aligned in a discontinuous pattern, resulting in nanofiber bridging zones (FBZs) (Fig-
ure 4F).3 Figure 4G shows that the simulated crack morphology of the small-angle
20 twisted helicoidal organization is composed of alternated CTZ and FBZ.
Although there exist discontinuous transition regions between CTZ and FBZ, the
hybrid fracture modes are in well agreement with our experimental investigations
(Figures 4D–4F). Discontinuous nanofibers form the main body of the Bouligand
structure and can induce crack twisting and simultaneously enhance crack bridging

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via nanofibers’ pull out and slippage. It can be speculated that the toughening
mechanisms underlying the hybrid fracture modes in our biomimetic discontinuous
Bouligand structural nanocomposites result in the excellent mechanical properties.
The resultant nanocomposites are in stark contrast to engineering continuous mac-
rofiber-reinforced plastics that are negatively characterized by delamination and
brittleness.9 Overall, the small-angle twisted discontinuous Bouligand structure
allows the nanocomposites to synergistically optimize stress distribution, alleviate
local stress concentration, and redirect crack propagation, ultimately leading to
enhanced damage tolerance (Figures 4A and 4D–4G).

Superior tear resistance endowed by the Bouligand structure is the dominant reason
for Arapaima gigas fish scales resisting the bite from piranha.4 Actually, the scale’s
helicoidal organization also helps resist puncture for protecting the underlying soft
tissue. Here, we further performed puncture tests on the prepared nanocomposites
to evaluate the ability to resist sharp attack, because this ability is critical for
mechanically protective applications and has practical significance (Figure 5A). This
out-of-plane loading can partly examine the microscale interlayered interaction of
the nanocomposites that are essentially prepared via layer-by-layer technique. Due
to the well interlayer coupling capability and stress transfer efficiency of the small-
angle 20 twisted Bouligand structural nanocomposite, large crack area without
obvious delamination was observed after piercing (Figure 5B). This phenomenon is
significantly different from that observed for other nanocomposites with large-angle
twisted structures and with unidirectional structure (Figures 5C and S26). For the
large-angle twisted nanocomposites, it can be speculated that the extent of damage
region will decrease due to the poor interlayered stress transfer (leading to high shear
stress and unexpected delamination), so energy needed to puncture becomes lower.
For the unidirectional anisotropic nanocomposite, stress distribution is localized and
directional, which also leads to delamination and small damage region. Therefore,
the nanocomposite with small (20 ) deviation angle exhibits optimal puncture resis-
tance (Figures 5D–5F). Its peak force and total energy are 6.41 N and 1.52 mJ, which
are higher than those of the unidirectional case (4.01 N and 0.97 mJ) and the 90
crossed case (5.04 N and 1.18 mJ). Impressively, the optimal puncture resistance is
also superior to that of some engineering plastics (Figure S27).

In addition, the merit endowed by biomimetic discontinuous Bouligand structure

manifested in low-speed impact scenario (Figures 5G–5I and S28–S30). Compared
with the unidirectional anisotropic film showing nonuniform and directional crack
field, the 20 twisted Bouligand structural film shows a more extensive and radial
crack field (Figure 5G). For the unidirectional case, crack favors to extend along
the nanofiber axis, where effective fracture energy reaches the minimum, i.e., the
intrinsic fracture energy.3 In contrast, for the small-angle twisted case, enhanced
effective fracture energy resulting from crack twisting and fiber bridging is approx-
imately identical in any direction, thus leading to a radial crack pattern. We observed
the fracture morphology of the films after low-speed impact tests. The periodic un-
dulating and large fracture area of the discontinuous Bouligand structural film also
reflects synergetic toughening that enables the film more resistant to crack propaga-
tion (Figures S29 and S30). As shown in Figures 5H and 5I, its peak force and
total energy are 128.58 N and 0.13973 J, which are higher than those of the unidi-
rectional case (96.25 N and 0.08336 J). Furthermore, cyclic bending tests were per-
formed on the films with prebuilt microholes (Figure 5J) to investigate their
fatigue behaviors and abilities to inhibit crack propagation, which are vital for
potential flexible device applications. Cyclic bending loading puts forward higher
requirements on the structural and interfacial stabilities of the films. As shown in

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A B C

D E F

G H I

J K L M
j1
j2

Figure 5. The puncture and impact properties of the films with different twisted angles
(A) Schematic of puncture and low-speed impact tests.
(B) SEM image of fracture surface of the 20  twisted film after piercing.
(C) SEM image of fracture surface of the unidirectional film after piercing.
(D) Puncture force-displacement curves of the films with different twisted angles.
(E and F) Peak force and total energy of the films with different twisted angles.
(G–I) Surface crack patterns (G), peak force (H), and total energy (I) of the unidirectional film and the 20  twisted film.
(J) Schematic of cyclic bending test. It is worth noting that the film in (j1 ) is in the naturally stretched state and does not bear tensile load; the film in (j 2 ) is
in the bent state.
(K) Digital snapshot of the 20  twisted film after 30,000 bending cycles.
(L) Digital snapshot of the unidirectional film (bending loading direction is parallel to nanofiber alignment direction) after 14,700 bending cycles.
(M) Digital snapshot of the unidirectional film (bending loading direction is perpendicular to nanofiber alignment direction) after 28,693 bending cycles.
Data in (E), (F), (H), and (I) are represented as mean G SEM.

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Figures 5K and S31, benefiting from well interlayer coupling capability and stress
transfer efficiency, the biomimetic discontinuous Bouligand structural film can sus-
tain more than 30,000 bending cycles without obvious crack propagation. It seems
that the centrally located prebuilt microhole crack is trapped in the nearly isotropic
Bouligand structure. In contrast, the unidirectional film exhibits serious crack prolif-
eration and completely fractures within 30,000 bending cycles due to anisotropic
structure-induced stress concentration (Figures 5L, 5M, S32, and S33). It needs to
be mentioned that the flexibility of SA matrix is better than that of the inorganic
CaSi nanofiber. When the bending loading direction is perpendicular to the nano-
fiber axis, the load is mainly applied to the SA matrix and the cyclic stability is better.

Systematic structural and mechanical investigations have demonstrated that the bio-
mimetic discontinuous Bouligand structure endows the nanocomposites with excel-
lent mechanical performance. Featuring mild waterborne preparation, eco-friendli-
ness, sustainability, and biocompatibility, the biomimetic nanocomposites are
expected to replace some engineering plastics (Table S6)42 and serve as packaging,
flexible device substrates, or armor materials. A simple temperature-stimulus dis-
player can be constructed via printing thermochromic pattern on the prepared
film. The flower pattern can disappear and reappear by controlling temperature (Fig-
ure S34). The mechanically superior film endows this displayer with stable thermal
detection application. Actually, bioelectronic devices also can be expected by inte-
grating our film with other functional layers. In addition, CaSi nanofiber within the
nanocomposites establishes potential for bone repair, because it is apatite’s precur-
sor and can induce the deposition of apatite under the environment of simulated
body fluids.43 Combining CaSi with SA, the biomimetic nanocomposites enable
application prospects in the field of tissue engineering.25,26 It is worth noting that
we only exemplarily used CaSi nanofiber and SA biopolymer to prepare the biomi-
metic nanocomposites. More nanofibers (such as silicon carbide and aluminum ox-
ide) and polymers (such as polyethersulfone and polyimide) with excellent intrinsic
properties can be orderly assembled, and applications will be more extensive.

Conclusions
In this work, we realize the design and fabrication of macroscale biomimetic discon-
tinuous Bouligand structural nanocomposites via a programmable assembly system.
Unique discontinuous Bouligand structure enables the obtained nanocomposites
remarkable interlayer coupling capability, high stress transfer efficiency, tortuous
crack propagation, and thus superior mechanical properties. Synergetic toughening
mechanisms of the biomimetic structure were experimentally and theoretically evi-
denced. It needs to be mentioned that moderate moisture within these waterborne
nanocomposites will regulate nanofiber-matrix interfacial hydrogen bonding and
facilitate the activation of toughening mechanisms based on nanofibers’ activities.
These nanocomposites exemplarily prepared from CaSi nanofiber and SA hold po-
tential for mechanically protective and biomedical applications. More importantly,
combining the programmable, mild, materials-independent, and scalable assembly
strategy, the biomimetic discontinuous Bouligand structural design is enlightening
to improve the engineering of continuous macrofiber-reinforced plastics and
develop advanced nanocomposites based on superior nanofiber building blocks.

EXPERIMENTAL PROCEDURES
Resource availability
Lead contact
Further information and requests for resources and materials should be directed to
and will be fulfilled by the lead contact, Shu-Hong Yu (shyu@ustc.edu.cn).

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Materials availability
This study did not generate new, unique reagents.

Data and code availability

This study did not generate or analyze datasets or code.

Preparation of CaSi-SA suspension

SA solution (2%) was prepared by dissolving SA powders (Sinopharm Chemical Re-
agent) in deionized water (DIW) via mechanical stirring at room temperature. CaSi
nanofiber was prepared by referring to a previous study.44 In a typical process,
200 mL Ca(NO3)2$4H2O (Sinopharm Chemical Reagent) aqueous solution (0.5 M)
was dropwise added into 200 mL Na2SiO3$9H2O (Sinopharm Chemical Reagent)
aqueous solution (0.5 M) at room temperature under mechanical stirring. The
mixture was then transferred into a 500-mL Teflon-lined, stainless-steel autoclave
and heated at 200 C for 24 h and then cooled down naturally. The resultant white
product was washed several times by DIW and ethanol and dried at 120 C for 24 h.
The product was dispersed into DIW via mechanical stirring and ultrasonic treat-
ment to form CaSi nanofiber suspension with a concentration of 10.0 mg mL
1.
Appropriate amounts of CaSi and SA were mixed together under mechanical stir-
ring (2 h) and ultrasonic treatment (0.5 h) to form homogeneous CaSi-SA
suspension.

The programmable nanofiber assembly system

Schematic of the programmable assembly is shown in Figure 1A. It contains four
modules that are solution injection and transport, wet directional sliding brushing
on flat substrate, substrate rotation, and thermal drying system. The operation of
several modules can be flexibly controlled by a computer software program.

The programmable assembly process for discontinuous Bouligand structural

nanocomposites
The homogeneous CaSi-SA suspension can be poured into a syringe that was
mounted on the syringe pump. The suspension can be transported to the root of
the brush (bristles) with controllable styles (speed, interval, and time). Continuous
liquid transport can facilitate the suspension to flow along the bristle root toward
the tip. The flowing process will propel CaSi nanofibers to preliminarily align. After
that, the sliding brushing step (1 cm s
1) will transfer the pre-oriented nanofibers to
the glass substrate and further help them align, forming an ordered CaSi-SA gel mi-
crolayer. Furthermore, the thermal drying system can turn the gel microlayer into a
film (3 to 4 mm) and the substrate can controllably rotate. In this way, when the next
brushing step is programmatically performed, certain twisted angle is already
formed. In the process of preparing films, the first and last brushing directions
remain the same. Unidirectional structural film can be prepared without running
platform rotation module. The thickness of the resultant films is controllable by sus-
pensions dosage and brushing times. Films can be further stacked into laminate with
solvent (water) welding and hot pressing.

Sample characterizations
SEM images were obtained by a Carl Zeiss Supra 40 instrument at the accelerating
voltages of 2–5 kV. Transmission electron microscopy (TEM) images were obtained
by a Hitachi H-7650 instrument at an acceleration voltage of 120 kV. X-ray diffraction
(XRD) test was carried out on a PW1710 instrument with CuKa radiation (l =
0.15406 nm). Macroscopic morphologies were recorded by a digital camera. Orien-
tationJ plug-in within ImageJ software was employed to quantify the nanofiber

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orderliness of the prepared films. Film transmittance was measured on a UV-

2501PC/2550 instrument (Shimadzu).

Mechanical tests
Tensile, tear, puncture, and bending tests were performed on an Instron 5565A ma-
chine using 500 N load cell. Low-speed impact tests were performed on an Instron
CEAST 9350 machine. Nanoindentation tests were performed on the Hysitron PI 85
Triboindenter. Cyclic bending experiments were performed on an LYPL-S50N me-
chanical, low-frequency, spring-fatigue-testing machine. For tensile tests, the films
with thickness of 100 mm were carefully cut into 4-mm-wide and 15-mm-long stripes
using a sharp blade. Tests were performed at a loading rate of 0.1 mm s
1 with a
gauge length of 5 mm. For the unidirectional film, loading direction is parallel or
perpendicular to nanofiber axis. For the films with different twisted angles, loading
direction is parallel to the nanofiber axis within surface microlayer of films. Unless
specifically mentioned, the length direction of the film is always parallel to the nano-
fiber axis within surface microlayer. For tear tests, the films (4 mm wide 3 15 mm
long 3 100 mm thick) were notched to approximately half of the width using a sharp
blade. Tests were performed at a loading rate of 0.1 mm min
1 with a gauge length
of 5 mm. For the unidirectional film, notch direction is parallel to the nanofiber axis.
For puncture tests, the films (10 mm wide 3 10 mm long 3 100 mm thick) were
clamped on the man-made holding device that leaves a circular hollow area with a
diameter of 5 mm in the central position. The diameter of the needle tip was
200 mm, and the puncture loading rate was 50 mm min
1. For single-notched,
three-point bending experiment, the polished film laminate (2 mm wide 3 15 mm
long 3 2 mm thick) was notched to approximately half of its thickness using diamond
saw and then sharpened using a razor blade. The bending loading rate was 1 mm s
1.
For low-speed impact tests, the films (12 cm wide 3 12 cm long 3 100 mm thick)
were clamped, leaving a circular hollow area with a diameter of 4 cm in the central
position. The tip diameter of the hemispherical-tip impactor was 2 cm, and the
impact energy was set at 0.7 J with a corresponding contact velocity of
0.78 m s
1. For cyclic bending experiments, the films (1 cm wide 3 5 cm long 3
100 mm thick) were installed on the machine (Figure 5J). The distance in the natural
state is 3.4 cm, and the minimum distance after bending is 1.8 cm. The operating fre-
quency is 1 Hz. The centrally located microhole with a diameter of about 100 mm was
generated by a steel needle. For nanoindentation tests, the film laminate (4 mm
thick) was fixed and its polished cross section faces upwards. The cross-sectional di-
rection of the microlayer of the film laminate is inclined 45 relative to the x (or y) axis
moving direction of the needle tip (Figure S18). The purpose of tilt test is to reduce
the interference between points. Berkovich indenter was employed. The peak
loading force is 8,000 mN, and the normal distance between points is about
1.5 mm. All samples were stored at a relative humidity of 40% at 25 C for 24 h
before tests.

Thermochromic pattern preparation

Screen printing mold with flower pattern was commercially purchased. Biomimetic
20 twisted film (30 mm thick) was prepared and attached to glass substrate. The
thermochromic flower pattern was achieved through printing (CHRO-T400B mate-
rial, Prtronic Store) and thermal curing (60 C for 4 h).

Fracture mechanics analyses for toughening mechanisms

A fracture mechanics model for the Bouligand structure with discontinuous fibers was
developed to analyze the toughening mechanisms.3,8,45–47 The Bouligand structure
was characterized by a coordinate system, where x axis is the crack propagation

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direction, z axis is the direction of tensile loading, and y axis orients perpendicular the
x-z plane. The dimensionless coordinates are given by x = x=d; y = y=d; z = z= d,
where d is the fiber diameter.

The mathematical representation of the twisted crack shape in the Bouligand struc-
ture can be described by45

z = y tanðxgÞ;
l=2%y%l=2; (Equation 1)

where g is the deviation angle and l = l=d is the dimensionless fiber length.

The dimensionless local energy release rate G = G=G0 can be calculated by3

G = maxðGt = G0 ; Gb = G0 Þ; (Equation 2)

where G0 is global energy release rate and Gt and Gb are local energy release rate in
crack twisting zone and fiber bridging zone and can be calculated based on previous
studies, respectively.45–47 Crack morphology and the normalized local energy
release rate are shown in Figure 4G.

Based on the calculated crack shape and local energy release rate, the dimension-
c
less effective fracture energy Geff = Gceff =Gint can be calculated as3

 Z 0:5l Z p=g 
c
Geff = pl g ðG cos b = G0 Þdxdy ; (Equation 3)

0:5l 0

where Gint is the intrinsic fracture energy and b is the kinking angle between the
normal to the deflected crack plane and the normal to the undeflected crack plane.
c
The Geff represents an enhancement factor of the fracture energy due to the crack
tilting and bridging enabled by the twisted structure. The model reveals that this
enhancement depends only on the deviation angle if the material properties (e.g.,
aspect ratio of the nanofiber) are fixed, and there exists an optimal deviation angle
for achieving the maximal toughening efficiency (i.e., the maximal enhancement of
fracture energy).

SUPPLEMENTAL INFORMATION
Supplemental information can be found online at https://doi.org/10.1016/j.matt.
2022.02.023.

ACKNOWLEDGMENTS
This work was financially supported by National Key Research and Development Pro-
gram of China (2021YFA0715700), National Natural Science Foundation of China
(22005289, 21975241, 21521001, and 51732011), Key Research Program of Frontier
Sciences from Chinese Academy of Sciences (QYZDJ-SSWSLH036), University Syn-
ergy Innovation Program of Anhui Province (GXXT-2019-028), Fundamental
Research Funds for the Central Universities (WK2480000005), and China Postdoc-
toral Science Foundation (2019TQ0294 and 2020M671870). This work was partially
carried out at the USTC Center for Micro and Nanoscale Research and Fabrication.
We thank Ruo-Gu Zhang, Ping Gu, Sai-Sai Cao, Xing-Long Gong, Rui Wang, and
Zhen He for assistance.

AUTHOR CONTRIBUTIONS
S.-M.C., H.-L.G., and S.-H.Y. conceived the idea and designed the experiments.
S.-H.Y. and H.-L.G. supervised the research. S.-M.C., S.-C.Z., X.-Y.L., Z.-B.Z., and

Matter 5, 1–15, May 4, 2022 13

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ll
S.-M.W. performed the experiments and analyzed the data. K.W. and Y.N. per-
formed theoretical analyses. X.S., Y.Z., and H.W. provided valuable advice for me-
chanical analyses. S.-M.C., H.-L.G., K.W., X.S., and S.-H.Y. co-wrote the manuscript.
All authors discussed the results.
DECLARATION OF INTERESTS
The authors declare no competing interests.
Received: November 21, 2021
Revised: January 19, 2022
Accepted: February 23, 2022
Published: March 21, 2022
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