of 9
1
Plant
cells
-
based
biological matrix composites
Eleftheria Roumeli
1
, Luca Bonanomi
1
, Rodinde Hendrickx
1
, Katherine Rinaldi
2
, Chiara
Daraio
1*
1
Division of Engineering and Applied Science,
California Institute of Technology, Pasadena, CA
91125, USA.
2
Division of Chemistry and Chemical Engineering, California Institute of Technology, Pasadena,
CA 91125, USA.
*Correspondence to:
daraio@caltech.edu
.
These authors contributed equally to this work.
The global increase in m
aterial
s
consumption
calls for innovative materials, with
tailored
performance
and
multi
-
functionality
, that are environmentally sustainable
. Composites from
renewable resources
offer
solutions to fulfil these demands
but
have so far been
dominated by
hybrid petrochemical
s
-
based matrixes reinforced by natural fillers.
Here
, we present biological
matrix composites with properties comparable
to
wood and commercial polymers
.
The
biocomposites are obtained from
culture
d,
undifferentiated plant cells, dehydrate
d and compressed
under controlled conditions
, forming a
lamellar
microstructure
.
Their stiffness and strength surpass
that of commercial plas
tics of similar density, like polystyrene, and low
-
density polyethylene,
while being entirely biodegradable. The properties can be
further
tuned varying the fabrication
process. For example, filler particles can be integrated during fabrication, to
vary
th
e mechanical
response or introduce new functionalities.
One Sentence Summary:
We
create natural
, biodegradable
composites
from
plant cells
with
p
roperties
akin
to commercial plastics of similar density
.
Polymer composite
s
are amongst the most widely produ
ced materials
(
1
)
.
However, the
ir
production and after
-
life use pose considerable environmental challenges
(
2
)
.
Most of the
produced
waste is disposed of in landfills or incinerated
(
3
)
.
Composite
s
components made of sustainable or
renewable resources, aka. biocomposites, offer promising solutions towards more sustainable
products
(
2
)
.
Although the majority of biocomposites still contain petroleum
-
derived plastics as
the main matrix material
(
4
,
5
)
,
research increasingly focus
es
on bio
-
derived or renewable matrix
materials
(
2
,
6
,
7
)
. Current challenges for fully bio
-
derived composites include balancing
production costs with performance, improving du
rability and assessing the
environmental impact
of m
anufacturing processing and post
-
use strategies
(
2
)
.
Engineer
ed
living materials (ELM) use living matter to fabricate and assemble the matrix
components
(
8
,
9
)
.
Examples include materials derived from yeast fermentation in the presence of
carbon nanotubes or graphene, which
combine
electrical and optical properties derived from the
synthetic fillers
,
and self
-
healing properties from the living cells
(
10
,
11
)
. Mate
rials that combine
living fungi or plant cells with carbon nanotubes
are structurally stable and
combine
electrical
conductivity
(
12
)
and temperature sensitivity
(
13
)
. Mycelium materials
already reached the market
for protective packaging, insulation
, and
acoustic panels
(
14
16
)
.
The combination of wood
particles, mycelium, and cellulose nanofibrils (CNF)
resulted in
composites with mechanical
properties superior to all
-
mycelium materials
(
17
)
.
However, the main drawback of all existing
2
biocomposites is their relatively low mechanical performance that renders them
un
suitable for
engineeri
ng and structural applications.
Plant materials
demonstrate an impressive range of mechanical properties
.
Their stiffness and
bending strength, for examp
le, can vary over three orders of magnitude
(
18
)
.
This remarkable
range depends on the native composition of the plant cell walls,
on the arrangement of the different
components within the cell
wall (see Supplementary Information),
and on the hierarchical
organization of the cells at the microscale.
Recently, chemical and/or thermo
-
mechanical post
-
processing of
natural
wood has been adopted to create high
-
performance materials, with properties
comparable to steel, ceramics and insul
ating foams
(
19
21
)
. However, wood processing relies on
deforestation, transportation to treatment plants and harsh chemical
treatments
, which are not
environmentally friendly.
Here
we describe a
new
class of biocomposites based on cultured and dehydrated
plant cells.
Our materials
retain the native plant cell wall composition
naturally secreted by growing plant
cells, to achieve mechanical performance comparable to structural and engineered woods, and
polymers.
We use undifferentiated, tobacco cells as a
model system. We characterize the
microstructure, composition and mechanical properties of the produced materials and show that
the incorporation of filler additives allows to improve the material’s performance and expand their
functionalities, for example
creating magnetic and electrically conductive materials.
We harvest plant cells from a
suspension
culture and compress them in a permeable mold, to
achieve a densified dehydrated structure (See Fig. 1A and Materials & Methods).
During
compression, water diffuses through the plant cell wall and the cell volume is gradually reduced.
When the cells reach a dry state, corresponding to approximately a 98% weight loss, the resulting
material consists only of a lamellar stack of compact
ed cell walls.
Cross
-
section scanning electron
microscopy (SEM) of the resulting material (Fig. 1B) illustrates the obtained microstructure.
We
compare it to
natural wood
(walnut, Fig. 1C), commercial medium density fiberboard (MDF, Fig.
1D), and plywood (
Fig. 1E). Our material is structurally similar to plywood and MFD, which are
compressed wood composites bound together with polymer adhesives.
Fig. 1.
(A)
Schem
atic of the fabrication method
. Plant cells are cultured, harvested and subjected
to a contr
olled compression and dehydration, resulting in a lamellar architecture when dry. SEM
cross
-
sectional views of the microstructure of
(B)
the biocomposite,
(C)
walnut,
(D)
MDF and
(E)
plywood at the same magnification.
W
e characterize the c
ell wall in livi
ng plant cells
extract
ed
from suspension cultures (Fig. 2A).
O
ptical and laser microscopy
shows
that
viable
cells are elongated,
with a
mean length of 170±60
μ
m
,
a mean width of 45±10
μ
m, and are surrounded by a thin primary cell wall containing
3
cellulose, pectin and phenolic compounds (Fig. 2B
-
D) (see Materials & Methods). Raman
spectroscopy of living cells (Fig. 2E) reveals the predominant vibrations
of
cellulose,
hemicellulose
s
,
pectin
,
and
the lignin precursors coniferyl alcohol and coniferald
ehyde
(
22
,
23
)
.
Compositional analysis
of the dry material shows that it is composed of 15%
cellulose,
20%
hemicelluloses,
6.8%
pectins and
6.3% lignols.
Thus, the obtained material is a biocomposite,
comprised of a heterogeneous mixture of naturally
synthesized biopolymers.
TGA curves
of the
biocomposite
reveal
four
distinct mass loss steps (Fig. 2F
).
The first derivative of mass loss (DTG)
peaks
correspond
to
: evaporation of bound water (peak 1),
and
degradation of pectins (peak 2),
hemicelluloses
(p
eak 3)
, cellulose
(peak 4),
and
phenolic compounds
(peak
5
-
6
)
(
24
)
. The char
residue is 10±5 wt%. The XRD patterns reveal multiple polymorphs of semicrystalline cellulose
(I, II and III, marked in Fig. 2G)
(
25
)
. Native cellulose from plant species crystalli
zes in the type
I polymorphs. In our dehydrated biocomposites, cellulose microfibrils partially undergo phase
transformations into crystal structures II and III, likely in response to the changing chemical
environment during cell dissociation, the pressure
applied during dehydration and the post
-
fabrication thermal treatment.
Fig. 2. (A)
Photograph of the cell culture.
M
icroscopy images of the cell
s
stained for
(B)
pectins
,
(C)
cellulose, and
(D)
lignols.
(E)
Raman spectrum of plant cells; peaks assigned to pectin (
P
),
cellulose (
C
), hemicellulose (
H
) and monolignols (
M
).
(F)
TGA (blue line) and DTG (black
dots
)
plots
of
the dehydrated biocomposite.
(G)
XRD pattern with
marked
contributions from cellulose
poly
morphs I
α
, I
β
, II and III.
(H)
Photograph of the biocomposite sample.
(I)
SEM image of a
cross
-
section, demonstrating the lamellar micro
-
structure.
(J)
TEM and
(K)
HRTEM images of
the biocomposite cross
-
sections
.
4
Optical and SEM observations of the
biocomposite
s
reveal an anisotropic, dense, lamellar
microstructure
comprised of
compacted plant cells (Fig. 2H
-
I). Transmi
ssion electron microscopy
(TEM)
demonstrates that the primary cell walls are preserved during cell compression and
dehydration (Fig.
2J
-
K).
Accepted models suggest that the primary cell wall is a multi
-
lamellated
structure consisting of cellulose microfibrils, arranged in various orientations within each plane
(from entirely isotropic to somewhat aligned, depending on cell type), bound
in a matrix of
hemicelluloses and pectins
(
26
)
. Even in the case of randomly distributed cellulose microfibrils in
the plane of the wall, the structure is considered highly anisotropic across thickness
(
26
)
.
TEM
images
of our biocomposites show an
average
dehydrated cell wall thickness of
185±57 nm
, and
cellulose microfibrils diameters ranging between 1 and 30 nm. High resolution TEM (HRTEM)
images confirm the presence of multi
-
lamellated structures, with cellulose microfibrils laying
across the consecutive
parallel planes (Fig. 2K, 3A
-
B). Using 3D tomographic reconstructions, we
analyze the spatial distribution of the cell wall components, and observe their fibrous organization
across multiple parallel planes, resulting in a highly anisotropic network (Fig.
3C). We observe a
hierarchical microstructure: at the cellular level,
a
lamellar architecture consisting of compacted
cells (Fig. 2I); at the sub
-
cellular level, an anisotropic, multi
-
lamellated structure
,
derived from
the
natural organization of the cell
wall components (Figs. 2J
-
K, 3B
-
C).
We perform tensi
le
and 3
-
point bending tests to characterize the mechanical performance
of
the dehydrated biocomposites. We compare them to different softwood
s
(pine), hardwoods
(poplar, oak
,
and walnut), commercial ply
wood
and
MDF
,
and synthetic plastics of similar density
(polystyrene, PS, polypropylene, PP, and low
-
density polyethylene,
LDPE
)
(Fig. 3D
-
E
,
Fig. S1).
Stress
-
strain plots obtained from the biocomposites (Fig. S2), show an initial linear elastic response
up
on loading, both under tension and bending, followed by a brittle failure at small strains (1±
0.3%). The Young’s modulus, calculated from the initial linear elastic part of the tension
experiments
,
is 2.5 ± 0.4 GPa, and the ultimate strength is 21.2 ± 3 M
Pa. The flexural modulus is
4.2 ± 0.4 GPa
,
and the modulus of rupture is 49.3 ± 3.2 MPa. Testing the flexural properties of the
biocomposite on the two perpendicular planes (see schematic in Fig. S3), reveals that stiffness
varies by a factor of ca. 1.75 i
n the two directions, while strength remains unaffected by orientation.
The
measured difference in stiffness
is due to the
anisotropic micro
-
structure of the biocomposite,
resulting from t
he fabrication process
which orients
the cells
nor
mal
to the
compression direction
.
We compare the m
echanical
properties
of different woods
and plastics
(Fig. 3D
-
E, Fig. S1).
Tension tests show that our biocomposites are stiffer than the other materials (Fig. 3D). However,
natural woods have higher strength (Fig. 3E
), which can be explained by the
ir
different
cellular
architectures,
cell wall composition
s
,
and
component
s
arrangement
s
within the secondary cell
walls. T
he
cells
used in our biocomposites
originate from the herbaceous plant
Nicotiana
tabacum
and they
naturally develop a thin, unlignified primary cell wall (we detect
only
a low
monolignol amount of 6.2 wt%).
These
cells do not form secondary cell walls and cannot self
-
organize in a hierarchical micro
-
structure in our cultures.
Regardless
, the mechanical
performance
of our biocomposites
is
comparable to that of commercial engineered woods and plastics
. They
surpass all literature
-
reported values for materials composed of plant cells, mycelium
,
or yeast
matrixes
(
11
,
14
,
27
)
(Fig. 3
G
).
5
Fig. 3. (A)
TEM of a cross
-
sectional area of the biocomposite.
G
ray arrows indicate the testing
direction for tensile experiments.
(B)
Selected subsection for tomography imaging.
(C)
3D
reconstruction of selected cell wall subsection. Gold corresponds to dark pixels
in the TEM,
showing how the cell wall material is distributed in the selected area.
(
D
)
Young’s modulus and
(
E
)
tensile strength
of the biocomposite and reference materials
.
(F)
Materials density.
(G)
Comparison of mechanical properties
of
this work (red
points),
and
literature
-
reported
biocomposites
(
10
12
,
14
,
17
,
27
)
.
(H)
Biodegradation
of
the biocomposite and natural pine.
Samples notation:
BC: pure
(without fillers)
biocomposite
;
1: pine; 2: poplar; 3: oak; 4: walnut;
5:
p
lywood; 6: MDF; 7
: PS;
8
: PP;
9
:
LD
PE.
A key factor in the design of sustainable materials is the
ir
end
-
of
-
life fate
. The realization of
biological matrix
materials
, such as those described here, offers an environmentally friendly
alternative
to non
-
degradable materials, which typically survive in landfills
. To assess the
biodegradability of our plant
-
based biocomposites, we perform agricultural soil incubation tests
(see Methods), comparing their mass loss with that of natural wood
(
28
)
. Resu
lts show an initial
mass gain corresponding to water uptake from the soil, in both natural wood and biocomposites
(Fig. 3
H
). The detectable mass loss due to biodegradation of the biocomposites begins 3 weeks
after incubation, while for natural wood it begi
ns about 7 weeks later. This can be associated to
the presence of lignin in natural wood, which is known to provide resistance to pathogen attacks
on cell walls
(
29
)
. We observe an almost complete biodegradation of the biocomposite 14 weeks
after initial i
ncubation
.
The proposed fabrication method allows us to use the natural biopolymer mixture as a matrix
and incorporate filler additives, which (i) in
troduces
new properties/functions in the composite
s
,
and (ii)
enables
further tuning of the mechanical perf
ormance.
The addition of different amounts
of carbon fibers (CF), for example, change
s
the biocomposites’
compressive modulus and strength
(Fig. 4A).
For CF concentrations below 5 wt% there is a gradual improvement of elastic modulus
and strength, followed
by a decrease for higher concentrations,
as
observed in polymer composites
because of
filler
s’
aggregation
(
30
)
.
D
ifferent filler particles expand the biocomposites’ property
space (Fig. 4B
).
W
e plot the elastic modulus as a function of density of different plant
-
based
biocomposites: pure cell matrix (BC), biocomposites containing various amounts of CF, halloysite
6
and montmorillonite nanoclays (NC) and graphene (G). Their properties lie at the i
ntersection of
natural cellular materials and commercial plastics (Fig. 4B), presenting elastic moduli spanning
over one order of magnitude.
F
iller additives also endow new functionalities, such as electrical
conductivity or magnetic properties. The electr
ical conductivity of plant cell/CF composites, for
example, can be tuned varying the CF content (Fig. 4C). Similarly, the addition of
13.5 wt%
iron
oxide nanoparticles (IN) in the plant cell matrix conveys ferro
-
magnetic properties, which allow
the biocomp
osite to support more than five times its weight when attracted by a magnet (Fig. 4D).
We have developed a new method to create natural biocomposite materials based on plant
cells. The method capitalizes on the plant cell’s ability to synthesize intricate
multi
-
lamellated
structures of cellulose, hemicellulose, lignin and pectin in their cell walls. In the future, the use of
different cell cultures and/or genetically modified species may allow the fabrication of materials
with significantly altered properti
es.
Similar fabrication approaches
can be
envisioned for
many
other biological systems (e.g. algae, fungi, etc.) that can provide complex elements as building
blocks for advanced composite biomaterials.
Fig. 4.
(A)
Compressive modulus and strength of
biocomposites with CF.
I
nset
:
SEM image of the
biocomposite with 1wt% CF (false colored).
(B)
Young’s modulus versus density for
various
materials and our biocomposites
.
Blue groups
correspond to
bending experiments, red groups
to
compression
.
(C)
IV curve
s for biocomposites with 1wt% and 20wt% CF.
(D)
Biocomposite with
IN
exhibiting magnetic properties.
7
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Acknowledgments:
Mr. Mark Ladinsky,
Dr. Stavros Amanatidis,
Dr. Yuchen Wei
,
Dr. Michael
Mello
,
Mr. Azhar Carim
,
Ms. Sarah Antilla and Mr. Duy Anh Nguyen for
support in experiments
.
Prof. Nathan Lewis for
providing access to the Raman facilities
.
Caltech Kavli Nanoscience
Institute
,
Gordon and Betty Moore
,
and
the
Beckman Foundation for gifts to Caltech to support
electron microscopy.
T
he Caltech Beckman Institute and the Arnold and Mabel Beckman
Foundation
for supporting the laser scanning imaging facilities
.
Funding
:
L.B. was supported by the Swiss National Science Foundation under the Early
Postdoc
.
Mobility project P2EZP2_175157.
K.R. and the Raman microscope were supported by
t
he
Joint Center fo
r Artific
ial Photosynthesis, a D
OE Energy Innovation Hub, supported through
the U.S. Department of Energy Office
o
f Science under award number DE
-
SC0004993.
Author
contributions
:
L.B.,
E.R., and C.D
.
conceived
and directed
the study.
L.B. and E.R.
designed the experiments.
E.R.
performed and oversaw all experiments, curated and analyzed
the
data,
generated the figures.
L.B. fabricated
and tested
biocomposites with carbon fibers.
R.H.
oversaw plant cell culture
s,
performed
biodegradation experiments
and
optical microscopy
.
K.R.
p
erformed
Raman measurements
. All authors discussed the data. E.R. and C.D. wrote the
manuscript with help from all authors.
Competing interests
:
Authors declare no competing interests.
Data and materials availability
:
All
data in the main text and supplementary material will be
made available upon request to the corresponding author.