-
ARTICLE
Received 3 Sep 2012 | Accepted 12 Aug 2013 | Published 10 Sep
2013
Carbon nanotubes on a spider silk scaffoldEden Steven1, Wasan R.
Saleh2, Victor Lebedev3, Steve F.A. Acquah4, Vladimir Laukhin5,
Runa G. Alamo6
& James S. Brooks1
Understanding the compatibility between spider silk and
conducting materials is essential to
advance the use of spider silk in electronic applications.
Spider silk is tough, but becomes soft
when exposed to water. Here we report a strong afnity of
amine-functionalised multi-walled
carbon nanotubes for spider silk, with coating assisted by a
water and mechanical shear
method. The nanotubes adhere uniformly and bond to the silk bre
surface to produce tough,
custom-shaped, exible and electrically conducting bres after
drying and contraction. The
conductivity of coated silk bres is reversibly sensitive to
strain and humidity, leading to
proof-of-concept sensor and actuator demonstrations.
DOI: 10.1038/ncomms3435 OPEN
1 National High Magnetic Field Laboratory, Department of
Physics, Florida State University, 1800 East Paul Dirac Drive,
Tallahassee, Florida 32310, USA.2Department of Physics, College of
Sciences, University of Baghdad, Baghdad 10071, Iraq. 3 Institut de
Ciencia de Materials de Barcelona (ICMAB-CSIC)/CIBER-BBN, Campus
UAB, Bellaterra 08193, Spain. 4 Department of Chemistry and
Biochemistry, Florida State University, 95 Chieftan Way,
Tallahassee,Florida 32306, USA. 5 Institucio Catalana de Recerca I
Estudis Avancats (ICREA), Barcelona 08010, Spain. 6Department of
Chemical and BiomedicalEngineering, FAMU-FSU College of
Engineering, 2525 Pottsdamer Street, Tallahassee, Florida
32310-6046, USA. Correspondence and requests for materialsshould be
addressed to E.S. (email: [email protected]).
NATURE COMMUNICATIONS | 4:2435 | DOI: 10.1038/ncomms3435 |
www.nature.com/naturecommunications 1
& 2013 Macmillan Publishers Limited. All rights
reserved.
-
The immense demand for electronics, and thus theelectronic waste
and environmental pollution it generates,poses a growing problem
that will require innovative
solutions1. Many toxic elements and non-biodegradable
plasticsare commonly found in conventional electronics, and efforts
todevelop new eco-friendly electronic designs are
thereforedesirable. Incorporation of natural materials into these
designsis advantageous to reduce the quantity of toxic components
of theelectronic devices. Moreover, natural materials often
possesscomplex and robust physical properties that can be harnessed
forelectrical and sensor applications. Spider silk (SS) is one
suchmaterial and the combination of its toughness2 and
bio-compatibility3,4 makes the material strategically important
forimplant, electrical, sensor and actuating applications.SS, a
protein-based natural polymer, is a exible but strong
material due to its helical-elastic and b-sheet
crystallinecomposition5,6. An unrestrained neat SS bre expands in
bothlength and diameter7,8 when humidied up to B70 or 80%relative
humidity (RH). At higher RH, the bre
experiencessupercontraction710, where it shrinks in length, expands
indiameter and becomes soft. This bre shrinkage is typically
anirreversible process11. The bre softening, however, is a
reversibleprocess12. In addition, the bre also experiences
cycliccontraction11, a phenomenon different from
supercontraction,where the bre extends when exposed to a
high-humidityenvironment. These factors are key to the work
presented here.For technological applications, where constant
strength
and exibility in a variable environment are desired,
super-contraction may be regarded as a problem. However,
bothsupercontraction and cyclic contraction can be exploited
foractuating applications. For example, it has been shown that
SSbres can be used as a biomimetic muscle with an exceptionalwork
density, 50 times higher than other biological musclebres,
estimated to be capable of lifting a 5 kg mass with a1mm thick SS
bre11. SS bres can also be used as contact13
or shadow14 masks during thin lm deposition, generatingmicro-13
or nano patterned14 features without lithographicprocessing.
Moreover, starting from its intrinsic properties, SSbres can serve
as a versatile scaffold upon which additionalfunctions can be
built. For example, CdTe15, magnetite16 andgold16,17 nanoparticles
can be used to functionalise SS foruorescent, magnetic and
electronic applications, respectively.Gold-functionalised bres
(Au-SS) have been shown to beelectrically robust down to cryogenic
temperatures17. Eventhough Au-SS possesses sufcient exibility for
use aselectrodes in microelectronics17, generally its elasticity
andelectrical continuity are not adequate for electronic sensors
oractuating devices.Here we show that supercontraction, and in
particular, silk
bre softening, provides a simple and effective route of
SSfunctionalisation with carbon nanotubes (CNTs), enabling usein
electronic applications including sensors and actuatingdevices. We
report a strong afnity for amine-functionalisedmultiwall CNTs
(f-CNTs) to adhere to natural Nephila clavipesSS bres. Adhesion is
facilitated by water and mechanical shear,and enhanced by polar
interactions and bonding between the SSand f-CNT side groups. The
process results in SS bresuniformly coated with f-CNTs (f-CNT-SS)
providing anelectrically conducting path, and thereby a
self-monitoringmechanism for physical changes and/or stimuli to the
f-CNT-SS structure. The f-CNT-SS bres are B300% tougher thanneat
silk bre, versatile and multi-functional, and exhibitpolar
(Supplementary Movie 1), shapeable, conducting, exible,strain- and
humidity-sensitive properties. Proof-of-conceptf-CNT-SS-based heart
pulse sensor and current-driven actuatordevices are
demonstrated.
ResultsWater-based f-CNT coating of SS bres. We discovered that
bymixing a bundle of dragline SS bres (B2 cm long) with a drypowder
of f-CNTs (Methods section), applying a few drops ofwater, and then
pressing and shearing the mixture between twoTeon
(Polytetrauoroethylene) sheets, the bres turned veryblack, and when
dried, contracted to a well-dened geometrywhere the silk bres were
uniformly coated with nanotubes(Fig. 1). The neat bundle contained
multiple dragline silk bres intheir natural double-stranded
arrangement (each strand has adiameter of B4 mm), all of which were
coated simultaneously.After the coating process, the dragline silk
bres were wellseparated into individually coated single-strand bres
(referred toas single bres for the rest of the paper), accompanied
by smallisolated f-CNT aggregates (Supplementary Fig. S1).This
separation allowed reliable extraction of single silk bres
from the bundle. SEM and TEM images of the single silk breshow
that the f-CNTs are attached to the SS structure (Fig.
2ad),including some penetration of the nanotubes into the SS
surface(Fig. 2e). This procedure produces a basic uniform
annularf-CNT coating with thickness of B80100 nm with
occasionalf-CNT aggregates of B1 mm in diameter and
thickness(Supplementary Fig. S2). Additional SEM and TEM images
ofanother silk bre are available (Supplementary Figs S1 and S2).We
have also performed a control experiment involving pre-
supercontracted bres. The neat bres are rst immersed in awater
bath for 30min, followed by air drying, and then the water-based
f-CNT coating is performed. The water-based procedure isalso
effective on these pre-supercontracted bres, indicating thatthe
initial shrinkage of silk bre is not the most important factorto
achieve the effective coating, but it is the softening of the
breduring supercontraction.We note that a dry powder of pure
multiwall CNTs
(MWCNTs) does not provide effective initial dispersion
andadhesion to the SS bre (Supplementary Fig. S3). As a result, it
isnot possible to coat the SS bre with pure MWCNTs using
ourwater-based method. Likewise, only SS bres exhibit an
effectivef-CNT coating compared with nylon, polyester, cotton and
someacrylic bres where either spotty or no coating was
observed.Unlike water, other solvents such as hexane, toluene,
methanol,ethanol, acetone, dichloromethane and dimethylsulphoxide
donot facilitate a uniform coating.
Fourier transform infrared spectroscopy. To examine moreclosely
the nature of the f-CNT/SS interface, and in particular
theinteraction between the NH2 side group of the f-CNTs and SS
Dryf-CNT-SS
bundle
Press and shear
WetMix
Figure 1 | f-CNT-SS processing steps. A neat SS bundle is mixed
with a dry
f-CNTpowder. The mixture is then wet, pressed, sheared between
two PTFE
substrates, and air dried. Scale bar: 2mm.
ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3435
2 NATURE COMMUNICATIONS | 4:2435 | DOI: 10.1038/ncomms3435 |
www.nature.com/naturecommunications
& 2013 Macmillan Publishers Limited. All rights
reserved.
-
protein structure, Fourier transform infrared (FTIR)
spectro-scopy is employed. The overall FTIR spectra of both the
neat SSand f-CNT-SS are similar (Fig. 3a), showing almost
identicalfeatures in the amide I (1,7001,600 cm 1) and amide
II(1,5001,400 cm 1) region18,19. As the absorption in amide Iand
amide II regions is sensitive only to the secondarystructure of the
SS bres19, this indicates that there are nomajor secondary
structure transformations after the f-CNTcoating; therefore, the
b-sheet and coil composition in the SSprotein structures remain the
same.However, a distinct feature in the amide III (1,350
1,200 cm 1) region18,19 is observed. Contrary to the amide Iand
II regions, the absorption in the amide III region issensitive to
the structure of amino acid side-chains19. InFig. 3c, a peak
intensity reduction is observed for theabsorption corresponding to
the O-H bond of aspartic andglutamic acid (1,254 cm 1)19,
indicating transformations of afraction of the acid hydroxyl
groups. The content of O-Hgroups subjected to the transformations
is extracted fromdeconvolution of the bands, as shown in
SupplementaryFig. S4. The reduction is very subtle (Supplementary
Fig. S5),as expected, due to the low abundance of aspartic
andglutamic acids in SS bres (maximum abundance of B0.6and B8.8%,
respectively)20. Additional evidence for chemicalinteractions is
revealed by the change in the C-H symmetricstretching absorption
prole observed in 2,9002,800 cm 1region (Fig. 3b), where the peak
intensities at 2,851 (CH2stretch) and 2,872 cm 1 (CH3 stretch) are
reduced andincreased, respectively, after the CNT coating21,22. How
theacid hydroxyl group transformation affects the C-H
stretchingabsorption is not yet understood. As a control, we
havealso compared the FTIR spectra of neat bres with bresthat have
been subjected to water, shear and pressure withoutthe f-CNTs. We
conrm that no observable difference inthe FTIR spectrum is observed
after the treatment(Supplementary Fig. S5).
Raman spectroscopy. Raman spectroscopy has been used toevaluate
the effects of the water-based method on the propertiesof the
f-CNTs being used. In Fig. 4, the Raman spectrum of asingle
f-CNT-SS bre is compared with the spectrum of a drypowder of the
f-CNT control sample. Owing to the thin f-CNT
Figure 2 | Single f-CNT-SS bre surface proles. (a) SEM image of
f-CNT-SS. The diameter of the bre is B6.5 mm. Scale bar: 10mm.
(b,c) MagniedSEM images of f-CNT-SS surface showing a uniform
mat-like covering. Scale bars: 1 mm. (d) TEM cross section of a
dragline silk bre with f-CNTcoating (red arrow). Silk folding due
to uneven sectioning. Scale bar: 1 mm. (e) TEM image indicating
nanotube penetration (red arrows) into the silkstructure. Scale
bar: 250 nm.
0.25
0.20
0.15
0.10
0.05
0.00
3,500 3,000 2,500
3,0000.0
0.5
0123
Abso
rban
ce (a
.u.)
Abso
rban
ce (a
.u.)
0
21
0246
Abso
rban
ce (a
.u.)
2,900 2,800 1,300 1,250 1,200
Wavenumber (cm1)
Wavenumber (cm1)Wavenumber (cm1)
2,000 1,500 1,000
Figure 3 | FTIR spectra of neat and f-CNT-SS bres. (a) Combined
FTIR
spectra normalised to the amide I peak at 1,625 cm 1 (red: neat
bres,blue: f-CNT-SS). (b) Expanded view of the spectra between
3,000 and
2,800 cm 1. Arrows indicate the position of the peaks of
interest.(c) Expanded view of the spectra near amide III region. A
subtle reduction in
the peak intensity near 1,260 cm 1 is observed after f-CNT
coating.
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3435 ARTICLE
NATURE COMMUNICATIONS | 4:2435 | DOI: 10.1038/ncomms3435 |
www.nature.com/naturecommunications 3
& 2013 Macmillan Publishers Limited. All rights
reserved.
-
coating, a weak background signal that comes from the SS
bre(Supplementary Fig. S6) is observed in the spectrum. Except
forthe partial contribution of the background signal, both
thef-CNT-SS bre and the control sample exhibit similar
D-band(B1,300 cm 1) and G-band (B1,600 cm 1) peaks, which
areassociated with disordered and graphitized carbon,
respectively.With the SS background subtracted, the normalized
spectrum off-CNT-SS is almost identical to that of the control
(inset ofFig. 4), including the D-band/G-band peak intensity ratio,
indi-cating that no additional disorder is introduced during
thecoating process. The uniformity of the f-CNT coating is con-rmed
by the similarity of the Raman spectra for three randomareas of the
same bre (Supplementary Fig. S6).
Tensile properties. The strength of the f-CNT-SS bre (B0.6GPa)
is lower than that of a neat bre (B1.4GPa), but is verysimilar to
the strength of the supercontracted dry bre (B0.6GPa), as shown in
Fig. 5. However, the f-CNT-SS bre has alarger extensibility (dened
as the maximum strain allowedbefore breaking) of B73%, compared
with that of the neat(B16%) and dry supercontracted (B47%) bres.
Therefore, thetoughness (dened as the area under the stressstrain
curve) off-CNT-SS bre is improved to B290MJm 3, B300% morethan that
of a neat bre. A summary of the tensile properties ofthe bres is
presented in Supplementary Tables S1 and S2.
Electrical conductivity. The conductivity extracted from
theresistance of a single f-CNT-SS is in the range of 1215 S cm
1(see Methods for calculation details). This value is consistent
withthat of a buckypaper control sample (B13 S cm 1) made usingthe
same f-CNT powder with benzoquinone cross-linkers fol-lowing the
procedure described in the study by Ventura et al.23
The single f-CNT-SS conductivity value is also consistent with
thereported value24 for MWCNT array samples of 714 S cm 1.
Custom shaped f-CNT-SS. As shown in Fig. 6a, it is possible
toshape the f-CNT-SS into various forms while it remains
con-ducting. The f-CNT-SS is rst wet using de-ionized water andbent
into the desired shape. After drying, the f-CNT-SS shape
ismaintained and the conductivity stays within 20% of its
originalvalue. This process can be repeated to obtain other shapes
withsimilar conducting properties. The softness of f-CNT-SS while
inthe wet state may mitigate the formation of CNT cracks duringthe
bending process.
Temperature-dependent resistance. The shapeable property
off-CNT-SS allows us to make clamped or woven electrode
con-gurations for electrical measurements. Electrodes can be madeby
wetting the f-CNT-SS bres, and then winding and weavingthem onto a
four-terminal copper wire resistance circuit (Fig. 6b).After
drying, the bres contract, squeezing the outer two copperwires
(current leads) and increasing the tension between the innertwo
copper wires (voltage leads). The contracted f-CNT-SS/cop-per
electrical contacts are robust in ambient or vacuum envir-onment
down to cryogenic temperatures. The resistance (R)follows a
three-dimensional (3D) variable range hopping(VRH)25 behaviour RR0
exp ([T0/T]1/4) down to B4.3 K(Fig. 6c), with a barrier energy
T0B108K, consistent with that ofa pressed pure-MWCNT pellet
reported in the literature26. Thisbehaviour is compared with that
of a buckypaper control sample(Supplementary Fig. S7). At higher
temperature, T430K, thebuckypaper follows a 3D VRH behaviour with
T0B53K, com-parable with the case of the f-CNT-SS. However, at
o30K, thebuckypaper exhibits one-dimensional (1D) VRH behaviour,
forexample: RR0 exp ([T0/T]1/2).
Strain-dependent resistance. Under a strain Dl/l of up to at
least50% (Fig. 7a), a single f-CNT-SS bre remains conducting,
andthe f-CNT coating can expand and contract in unison with the
SSbre, thereby maintaining an electrical linkage without crossing
apercolation threshold. In some cases, it is possible to obtain
bresthat in the dry state under ambient conditions can be
stretchedup to 200% of the initial length while remaining
conducting(Supplementary Movie 2; a bundle of bres was used in the
videofor clear visualization). With a gauge factor
(DR/R)/(Dl/l)1.20.02 (Fig. 7b), this leads immediately to
proof-of-conceptapplications such as strain-sensitive resistive
sensors for heart-pulse monitoring (Fig. 7c). The f-CNT coating
also provideselectrical readout to monitor strain changes due to
humidityvariation (Fig. 7d). We note that for a thicker f-CNT or
goldcoating, no humidity response was observed.
f-CNT-SS annealing and actuator function. We observed thatan
application of 100 mA current with a 40-s duration perma-nently
reduced the resistance of f-CNT-SS by B15%(Supplementary Fig. S8).
The result was conrmed on threeseparate f-CNT-SS bres. A systematic
decrease in post-annealedresistance was observed up to 150 mA.By
using the f-CNT coating as a local heating element, it was
possible to utilize a single f-CNT-SS bre as a
current-driven
12
10
8
6
Inte
nsity
(a. u
.)
4
2
1,000
1,000 1,500
1,200 1,400 1,600Raman shift (cm1)
Raman shift (cm1)
1,800 2,000
2,000
Normalized10
5
0Int
ensi
tyD-band
G-band
Figure 4 | Raman spectra of f-CNT-SS bre and dry f-CNT
powder.
The f-CNT-SS spectrum has been offset to show the linear
background
contribution more clearly (blue: f-CNT-SS bre, red: dry f-CNT
powder).
Inset shows background-subtracted and normalized spectrum of
f-CNT-SS,
showing an overlap with the spectrum of the control sample.
1.4
1.2
1.0
0.8
0.6
0.4
0.2
0.0
Stre
ss (G
Pa)
100806040200Strain (%)
Neat
Dry supercontracted
f-CNT-SS
Figure 5 | Tensile properties of neat and processed SS single
bres.
Measurement was performed at 25% RH to reduce the effects of
water
vapour absorption on the tensile properties (dashed lines: neat
bres,
circles: dry supercontracted bres, solid lines: f-CNT-SS
bres).
ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3435
4 NATURE COMMUNICATIONS | 4:2435 | DOI: 10.1038/ncomms3435 |
www.nature.com/naturecommunications
& 2013 Macmillan Publishers Limited. All rights
reserved.
-
actuator (Fig. 8). The actuator could be operated in two
modes.First, the contraction mode (Fig. 8b) was achieved by
applying a100-mA current to a single f-CNT-SS bre in its natural
partially
hydrated state under ambient conditions (55% RH, 23 C). Thelocal
heat (B5mW) generated by a 100-mA current dehydratedthe bre,
therefore contracting the bre by B1% of its original
Wovenf-CNT-SScontact
Clampcontact
Copperwire
f-CNT-SS
I+ V+ V I
10.5
10.0
9.5
0.4 0.6
25020015010050Temperature (K)
10
20
30
40
Res
ista
nce
(k)
(1/T ) 1/4
Ln(R
)
Figure 6 | Custom-shaped f-CNT-SS for clamped and woven
electrodes. (a) Photographs of f-CNT-SS shaped into coil, ring,
knotted and letter forms.
(b) Photograph of clamped (I) and woven (V) contacts used to
characterize the temperature-dependent resistance of f-CNT-SS with
clampI contact expansion. Scale bar: 500mm. (c) VRH nature (that
is, ln(R)B(1/T)1/4) of f-CNT-SS.
1.81.61.41.21.00.8
0 10 20 30 40
810
815
0 100 200 3000.0
20
40
601572 b.p.m.
10
R (%
)
RH
(%
)
5
00 20 40 60 80
0.2
Stra
in (%
)
Res
ista
nce
(k)
0.4
400Strain (%) Time (s)
Time (min)
Res
ista
nce
(M
)
Figure 7 | Strain-dependent resistance of f-CNT-SS. (a)
Strain-dependent resistance of a single f-CNT-SS bre up to 50%
strain. (b) Cyclic strain test
of a single bre with a 1.2 gauge factor (red line: resistance,
blue line: strain). (c) Demonstration of the strain sensitive
resistance of f-CNT-SS to
heart pulses. A bundle of f-CNT-SS with RB11 kO was used in this
device. Left and right scale bars correspond to 1 cm and 1mm,
respectively. (d) Cyclic RHtest up to 70% RH of a 2 2mm2 f-CNT-SS
mat with RB100O (red line: DR, blue line: RH).
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3435 ARTICLE
NATURE COMMUNICATIONS | 4:2435 | DOI: 10.1038/ncomms3435 |
www.nature.com/naturecommunications 5
& 2013 Macmillan Publishers Limited. All rights
reserved.
-
length (1.8mm). Consequently, the mass (35mg) was lifted byB25
mm (Fig. 8b). The lifting action occurred almost instanta-neously
(r1 s). After B5min, the bre relaxed close to itsoriginal length
due to rehydration. A longer time was required tofully rehydrate.
The slow relaxation rate may be due tothe vapour absorption rate
intrinsic to the SS. Operation atlower temperature and/or higher RH
may decrease the brerelaxation time.In contrast with the
contraction mode, the extension mode was
achieved by applying a current after the initial dehydration.
Herean application of current extended the bre by B0.15% of
itsdried length, lowering the mass by B4 mm (SupplementaryMovie 3).
Furthermore, both the bre extension and contractionactions occurred
within 1 s. In principle, increasing the appliedcurrent would
increase the extension length primarily due tothermal expansion. In
both cases, we conrmed the repeatabilityof this behaviour for three
different single f-CNT-SS bres.
DiscussionThe essential aspects leading to the realization of
the f-CNT-SSmaterial are as follows. The f-CNTs are polar, with
positive chargeat the amine sites. The SS is a protein-based
polymer where theamino acid groups vary along the backbone, some
are neutral andsome polar27. By mechanical mixing, the dry f-CNT
powder ispartially dispersed and adheres to the SS bres due to
polarinteraction (Supplementary Fig. S3). When water is applied to
themixture, the f-CNTs disperse further and the SS bres
experiencehydrogen bond breaking8, resulting in bre swelling and
softening.As a result, the surface area of the bre is increased,
allowing moref-CNTs to adhere to the bre. Applications of shear and
pressurebring the f-CNTs in closer proximity to the surface of the
bre,promoting both physical and chemical interactions between
them.Upon drying, the SS bre matrix shrinks further as
hydrogenbonding is re-established8,28, concentrating the CNT array
andmaking it electrically conducting.The FTIR spectra in Fig. 3
indicate a change in the nature of
the SS carboxylic acids, consistent with the aqueous
chemicalreaction between the NH2 side groups of the f-CNT and
theCOOH component of aspartic and glutamic acids in the SS. Asour
water-based method is performed at room temperature,amide formation
is unlikely because this type of reactionnormally occurs at high
temperatures22. However, ionic andhydrogen bonding are both likely
to occur. In an aqueoussolution, for example with pH of 47, some
amount of side-chaincarboxylic acids and amines are typically
ionized. By applyingshear and pressure, ionic bonding between them
is promoted. Inparallel, the NH2 side groups may form hydrogen
bonding withthe non-ionized aspartic and glutamic acids
(SupplementaryFig. S9). The formation of hydrogen bonding at
roomtemperature has been observed in the fabrication of
buckypaperfrom O-H-functionalised CNTs29. Even though the f-CNT
anchoring to the SS bre is minimal due to the smallabundance of
aspartic and glutamic acids, it generates asignicant grafting, such
that when combined with the van derWaals interaction and the
natural tendency of the f-CNTs toentangle, a new hybrid functional
silk bre is produced(Supplementary Fig. S9).The intimate adherence
of the f-CNTs on the SS bre is the key
factor that results in many of the observed phenomena such asthe
improved extensibility and toughness of the f-CNT-SS bre.The
toughness of f-CNT-SS bres can be attributed rst to
thesupercontraction that occurs during the coating process
andsecond to the distribution of SS radial deformation by the
f-CNTcoating. SS bres generally become tougher after being
super-contracted. The release of internal pre-stress8 in neat SS
bresduring supercontraction accounts for the additional energy
theycan absorb before rupturing. The f-CNT coating may
furtherimprove the toughness by effectively distributing the SS
radialdeformations associated with the rupture point during
theextension process. A SS bre experiences a very large
radialdeformation when strained longitudinally, with a Poisson
ratio (ameasure of how much the diameter of the bre shrinks when
thebre is extended) of B1.5 (ref. 30). In contrast, a CNT
network,such as the buckypaper, experiences signicantly less
deformation(Poisson ratio up to 0.3), except in some special
cases31. Ifintimately connected to the SS bre, this can reduce the
radialdeformation of the silk bre at the highest rupture point,
forexample, in the middle of the bre, allowing further
extensionbefore it ruptures.The uniformity of the f-CNT coating is
demonstrated by the
absence of sudden jumps in the resistance versus strain curve
upto at least 50% strain (Fig. 5a). The uniform adherence
strengthbetween the f-CNT to SS and f-CNT to f-CNT contacts
allowshomogenous strain distribution during extension, similar to
themechanism observed in CNT-elastomer or
gold-elastomersystems32,33, where extensions of 4100 or 20% are
observed,respectively. Additional exibility may be provided by the
breshrinkage during the water-based processing, which
effectivelyconcentrates the f-CNT network. We emphasize that no
f-CNTcrosslinkers are used in our water-based coating method.
Withoutcrosslinkers, it has been reported that the f-CNT network
istypically very brittle23.The 3D VRH transport of the f-CNT-SS
reveals that the
conductivity is dominated by inter-tube charge carrier
hoppingbetween the f-CNTs34, which may be related to the
submicronlength of the f-CNTs used (therefore resulting in a larger
numberof inter-tube contacts). The T0 and conductivity of the
f-CNT-SSand the benzoquinone-crosslinked buckypaper are
similar.This suggests that the simple water-based coating method
iseffective. The slightly higher T0 could mean that the f-CNTswere
not as tightly entangled as in the case of crosslinkedbuckypaper,
resulting in a slightly higher contact resistancebetween the
f-CNTs.
Weight
f-CNT-SS
0 A 100 A 0 A
Drying contraction
100 A 0 A 100 A
Figure 8 | F-CNT-SS actuator activated by Joule heating. (a)
Photograph of a 35mg mass hanging on a single f-CNT-SS bre. Scale
bar: 250mm. (b) Cyclicf-CNT-SS contraction. The bre was allowed to
relax for 1 h before the next current cycle to ensure full
rehydration. Scale bar: 150mm.
ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3435
6 NATURE COMMUNICATIONS | 4:2435 | DOI: 10.1038/ncomms3435 |
www.nature.com/naturecommunications
& 2013 Macmillan Publishers Limited. All rights
reserved.
-
The application of an annealing current under ambientconditions
indicates a reduction in the contact resistance of thef-CNT
network. A similar effect is observed in carbon nanobre(CNF)gold
interconnects, where the application of an annealingcurrent at
ambient condition reduces the contact resistancebetween the CNFgold
interconnects35. As the f-CNT coating onthe SS surface is very
thin, B80100 nm, a 100-mA annealingcurrent may generate a
considerable current density that heats theCNTCNT joints, producing
better contacts.Owing to the thin, exible and porous nature of the
f-CNT
network, external stimuli such as varying strain and
humiditylevels will affect the SS bre. We emphasize that for
gold-coated(B20-nm thick) or thicker f-CNT coated SS (several
micrometrethick; Methods section), and neat buckypaper (B30 mm
thick),the humidity response is not observed.As a local heating
element, the f-CNT coating allows us to
drive the SS-based actuator reported earlier11 using
electricalcurrents in contraction and extension mode by exploiting
theswelling/de-swelling and thermal expansion/contraction of
thesilk bre, respectively. The f-CNT-SS contraction ofB1% in
ourproof-of-concept demonstration (performed at 55% RH)
iscomparable to the reported value in the previous study11. Intheir
case, the average contraction for lifting a 9.5-mg mass isB1.7% in
the full-humidity range of 9010% RH. Assuming alinear correlation
between the contraction length and RH, weexpect that a variation of
RH from 55 to 10% will generate anaverage contraction of 0.95%,
which agrees very well with ourresult. This suggests that our
coating approach does not degradethe actuating properties of the
silk bre.In conclusion, we have developed a simple and effective
water-
based and shear-assisted method of fabricating tough,
versatile,exible and multi-functional f-CNT-SS bres.
Amine-functiona-lised MWCNT adheres effectively to the SS bre, as
revealed bySEM and TEM images and by structural changes in the
carboxylicacid of the SS as observed in the FTIR spectra. The
uniformity ofthe coating is further conrmed from the Raman spectra,
strain-dependent resistance and electrical conductivity estimation.
Thecharge carrier transport is primarily driven by inter-tube
chargehopping, as revealed by the 3D VRH
temperature-dependenttransport. The combination of a thin, exible
and porous CNTnetwork with SS bres is synergistic, resulting in
polar, custom-shapeable, self-monitoring and actuating devices.
MethodsCNTcoating. N. clavipes dragline silk bres were harvested
from its natural habitatand used in the experiments. According to
the product specications, theMWCNTs (NanocylTM NC3152) are
submicron in length, functionalised withNH2 groups (o0.5 wt %),B10
nm in average diameter, and have carbon purity of495%. From the TEM
image (Supplementary Fig. S10), it was observed that
theamine-functionalised MWCNT (hereafter f-CNT) is composed of B17
nanotubelayers. The f-CNT coating method is outlined in Fig. 1. Dry
f-CNT powderand SS bres were rst mixed mechanically. The pre-coated
bres were wet by fewdrops of water on a Teon substrate. The wet
bres were pressed and shearedbetween two Teon substrates, followed
by air drying under ambient conditions.We also obtained f-CNT-SS
with a thicker coating (510 mm, SupplementaryFig. S11) by dipping
the neat bres into a benzoquinone/f-CNT solution20 anddrying at 50
C, repeatedly 2030 times. However, in addition to the more
complexpreparation, the bres produced with this method (compared
with the water-basedprocedure) were not as extendable. The
benzoquinone/f-CNT solution was alsoused to make the buckypaper
control sample.
TEM and SEM imaging. Bundles of f-CNT-SS bres were rst xed with
3%glutaraldehyde in water solution (diluted from 50% glutaraldehyde
in water solu-tion purchased from Electron Microscopy Sciences) for
2 hours at room tem-perature. The bres were then dehydrated in
ethanol, followed by embedding inEpo-x (5:25 hardener/resin weight
ratio, Electron Microscopy Sciences) at 50 Cfor 4 h. A Leica
Ultracut E microtome was used to obtain 90-nm thick sections
off-CNT-SS embedded in epoxy that were then transferred onto TEM
100 meshcopper grids. TEM images were obtained with a cold
eld-emission JEOL JEM-
ARM 200F at 80 keV. SEM images were obtained by eld-emission
JEOL JSM-7410F SEM at 5 keV.
FTIR spectroscopy. FTIR spectroscopy was performed under
attenuated totalreectance (ATR)-FTIR mode using the Smart Orbit
diamond ATR accessoryof the Thermo Scientic Nicolet 6700
spectrometer. The measurements werecarried out in absorption mode
between 4,000 and 400 cm 1 with 2 cm 1resolution at 23 C and B25%
RH. The same silk bres were used for each set ofmeasurements, for
example, before and after treatment or CNT coating. Beforeeach
measurement, the samples were stored under low-humidity conditions
using aPetri dish with a desiccant.
Raman spectroscopy. Raman spectroscopy was performed using a
RenishawInvia micro-Raman with a 785-nm excitation wavelength, 3mW
power, 50magnication, 20 s exposure and two accumulations. The
samples were mountedon a gold substrate to reduce undesired
background Raman signals.
Tensile properties. Stressstrain measurements of single silk
bres were carriedout using Dynamical Mechanical Analyser (DMA,
Q800, TA Instruments) instrain-ramping mode. The measurements were
performed at a 2% per min strainrate under 23 C and 25% RH. Prior
to each stressstrain measurements, thediameter of each single silk
bre was determined using an optical microscope( 500 magnication)
with dark eld illumination. A lithographically patternedscale with
1-mm resolution was used as a reference. The single silk bre
wasmounted between two Kapton pads connected by a thin Kapton
bridge. The brewas secured using a hard 2850 Stycast epoxy (cured
at 23 C for 24 h). After thepads were clamped into the DMA, the
bridge was cut. To ensure reliability, the dataobtained from bres
that broke near the clamp edges were not used.
Resistivity measurement. The electrical conductivity of the
single f-CNT-SS brewas estimated on a 1.2-cm long sample in
four-terminal conguration with carbonpaste electrical contacts. The
distance between the inner electrodes was 2mm(RB810 kO). Typical
geometrical factors were used in the estimation, for example,the
supercontracted SS bre diameter of B6.5 mm (Fig. 2a and
SupplementaryFig. S1) and f-CNT coating of B80100 nm (Fig. 2e and
Supplementary Fig. S2).Using these values, the cross-section area
of the annular CNT coating wasestimated to be between 1.6 and 2.04
mm2. The electrical conductivity of thebuckypaper control sample
was estimated using a sample with length, width,thickness and
resistance of 0.276mm, 172.5 mm, 30 mm and 41O, respectively.
Theresistance was measured using a Keithley 6221 current source and
a Keithley2182A nanovoltmeter in a four-terminal conguration.
Strain-dependent resistance. A Parker Actuator 401XR
translational stage with aCompax3S Servo Drive System was used to
exert strain on the sample at0.3 mms 1 rate. Single bres or bundles
of f-CNT-SS were mounted in a four-terminal conguration using
carbon paste.
f-CNT-SS for heart pulse monitoring. f-CNT-SS bundle was mounted
in a four-terminal resistance conguration using carbon paste on a
substrate with a gapbetween the voltage leads to allow the f-CNT-SS
bundle to bend during mon-itoring. The carbon paste contacts were
protected by enamel coating.
Humidity-dependent resistance. Single bres or bundles of
f-CNT-SS weremounted on a G10 substrate in four-terminal
conguration using carbon paste andwere placed inside a custom-made
humidity chamber.
f-CNT-SS actuator. A single f-CNT-SS bre was mounted between two
G10substrates in a two-terminal electrical conguration using carbon
paste. A piece of35mg solder wire with a 24-mm gold wire hook was
used as a hanging weight.Current was applied with a Keithley 6221
current source and the f-CNT-SSmovement was recorded with an
optical microscope equipped with a digitalcamera. Video analysis
was performed to obtain the displacement behaviour of
thef-CNT-SS.
References1. Robinson, B. H. E-waste: an assessment of global
production and
environmental impacts. Sci. Total Environ. 408, 183191 (2009).2.
Yang, Y. et al. Toughness of spider silk at high and low
temperatures.
Adv. Mater. 17, 8488 (2005).3. Allmeling, C., Jokuszies, A.,
Reimers, K., Kall, S. & Vogt, P. M. Use of spider
silk bres as an innovative material in a biocompatible articial
nerve conduit.J. Cell Mol. Med. 10, 770777 (2007).
4. Kim, D.-H. et al. Dissolvable lms of silk broin for ultrathin
conformalbio-integrated electronics. Nat. Mater. 9, 511517
(2010).
NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3435 ARTICLE
NATURE COMMUNICATIONS | 4:2435 | DOI: 10.1038/ncomms3435 |
www.nature.com/naturecommunications 7
& 2013 Macmillan Publishers Limited. All rights
reserved.
-
5. Gosline, J. M., Guerette, P. A., Ortlepp, C. S. & Savage,
K. N. The mechanicaldesign of spider silks: from broin sequence to
mechanical function. J. Exp.Biol. 202, 32953303 (1999).
6. van Beek, J. D., Hess, S., Vollrath, F. & Meier, B. H.
From the cover: themolecular structure of spider dragline silk:
folding and orientation of theprotein backbone. Proc. Natl Acad.
Sci. USA 99, 1026610271 (2002).
7. Guinea, G. V., Elices, M., Perez-Rigueiro, J. & Plaza, G.
Self-tightening of spidersilk bres induced by moisture. Polymer 44,
57855788 (2003).
8. Ene, R., Papadopoulos, P. & Kremer, F. Supercontraction
in Nephila spiderdragline silkRelaxation into equilibrium state.
Polymer 52, 60566060 (2011).
9. Shao, Z. & Vollrath, F. The effect of solvents on the
contraction and mechanicalproperties of spider silk. Polymer 40,
17991806 (1999).
10. Work, R. W. A Comparative study of the supercontraction of
major ampullatesilk bers of orb-web-building spiders (Aranae). J.
Arachnol. 9, 299308 (1981).
11. Agnarsson, I., Dhinojwala, A., Sahni, V. & Blackledge,
T. A. Spider silk as anovel high performance biomimetic muscle
driven by humidity. J. Exp. Biol.212, 19901994 (2009).
12. Gosline, J. M., Denny, M. W. & Demont, M. E. Spider silk
as rubber. Nature309, 551552 (1984).
13. Steven, E., Jobiliong, E., Eugenio, P. M. & Brooks, J.
S. Adhesive stampelectrodes using spider silk masks for electronic
transport measurements ofsupra-micron sized samples. Rev. Sci.
Instrum. 83, 046106 (2012).
14. Morales, P., Rapone, B., Caruso, M. & Flammini, D.
Spider-silk-basedfabrication of nanogaps and wires. Nanotechnology
23, 255304 (2012).
15. Chu, M. & Sun, Y. Self-assembly method for the
preparation of near-infrareduorescent spider silk coated with CdTe
nanocrystals. Smart Mater. Struct. 16,24532456 (2007).
16. Mayes, E. L., Vollrath, F. & Mann, S. Fabrication of
magnetic spider silk and othersilk-bre composites using inorganic
nanoparticles. Adv. Mater. 10, 801805 (1998).
17. Steven, E. et al. Physical characterization of
functionalized spider silk: electronicand sensing properties. Sci.
Technol. Adv. Mater. 12, 055002 (2011).
18. Hu, X., Kaplan, D. & Cebe, P. Dynamic protein-water
relationships duringb-sheet formation. Macromolecules 41, 39393948
(2008).
19. Barth, A. Infrared spectroscopy of proteins.
BBA-Bioenergetics 1767,10731101 (2007).
20. Creager, M. S. et al. Solid-state NMR Comparison of various
spiders draglinesilk ber. Biomacromolecules 11, 20392043
(2010).
21. Kawai, T. Photoregulation of molecular orientation of
stearic acid in a polyioncomplex LB lm containing azobenzene
derivative. J. Phys. Chem. B 103,55175521 (1999).
22. Ramanathan, T., Fisher, F. T., Ruoff, R. S. & Brinson,
L. C. Amino-functionalized carbon nanotubes for binding to polymers
and biologicalsystems. Chem. Mater. 17, 12901295 (2005).
23. Ventura, D. N. et al. Assembly of cross-linked multi-walled
carbon nanotubemats. Carbon 48, 987994 (2010).
24. Jakubinek, M. B. et al. Thermal and electrical conductivity
of tall, verticallyaligned carbon nanotube arrays. Carbon 48,
39473952 (2010).
25. Mott, N. F. Conduction in non-crystalline materials. Phil.
Mag. 19, 835852(1969).
26. Yosida, Y. & Oguro, I. Variable range hopping conduction
in multiwalledcarbon nanotubes. J. Appl. Phys. 83, 49854987
(1998).
27. OBrien, J. P., Fahnestock, S. R., Termonia, Y. &
Gardner, K. H. Nylons fromnature: synthetic analogs to spider silk.
Adv. Mater. 10, 11851195 (1998).
28. Eles, P. T. & Michal, C. A. Strain dependent local phase
transitions observedduring controlled supercontraction reveal
mechanisms in spider silk.Macromolecules 37, 13421345 (2004).
29. Han, J. T., Jeong, H. J. & Lee, G.-W. Buckypaper from
thin multiwalled carbonnanotubes. Proc. SPIE 7037, 703717
(2008).
30. Koski, K. J., Akhenblit, P., McKiernan, K. & Yarger, J.
L. Non-invasivedetermination of the complete elastic moduli of
spider silks. Nat. Mater. 12,262267 (2013).
31. Hall, L. J. et al. Sign change of Poissons ratio for carbon
nanotube sheets.Science 320, 504507 (2008).
32. Zhang, Y. et al. Polymer-embedded carbon nanotube ribbons
for stretchableconductors. Adv. Mater. 22, 30273031 (2010).
33. Lacour, S. P., Wagner, S., Huang, Z. & Suo, Z.
Stretchable gold conductors onelastomeric substrates. Appl. Phys.
Lett. 82, 24042406 (2003).
34. Jin, R. et al. The effect of annealing on the electrical and
thermal transportproperties of macroscopic bundles of long
multi-wall carbon nanotubes. Phys. B288, 326330 (2007).
35. Kitsuki, H. et al. Length dependence of current-induced
breakdown in carbonnanober interconnects. Appl. Phys. Lett. 92,
173110 (2008).
AcknowledgementsThis work was supported in part by NSF-DMR
1005293 and 1105129, and carried out atthe National High Magnetic
Field Laboratory, supported by the NSF, the DOE and theState of
Florida. W.R.S. thanks Fulbright Visiting Scholar 2011 program. The
Barcelonagroup thanks MICINN (CTQ2010-19501) and CIBER-BBN, an
initiative funded by theVI National R&D Plan 20082011,
Iniciativa Ingenio 2010, Consolider Program. Wethank Drs Yi-Feng Su
and Xixi Jia for assistance in the TEM study. We would also like
tothank Dr Jin Gyu Park for the assistance in the tensile
measurement and Raman spec-troscopy study. We are grateful for the
access to DMA and Raman spectroscopy facilitiesprovided by
HPMI.
Author contributionsE.S., W.R.S. and S.F.A.A. conceived the
original idea and performed preliminaryexperiments. V.Le. and V.La.
characterized the strain-dependent resistance. R.G.A.and E.S.
performed the FTIR spectroscopy and analysis. E.S. performed the
restof the experiments. E.S. and J.S.B. wrote the manuscript and
contributed to projectplanning.
Additional informationSupplementary Information accompanies this
paper at http://www.nature.com/naturecommunications
Competing nancial interests: The authors declare no competing
nancial interests.
Reprints and permission information is available online at
http://www.nature.com/reprintsandpermissions/
How to cite this article: Steven, E. et al. Carbon nanotubes on
a spider silk scaffold.Nat. Commun. 4:2435 doi: 10.1038/ncomms3435
(2013).
This work is licensed under a Creative Commons
Attribution-NonCommercial-ShareAlike 3.0 Unported License. To view
a copy of
this license, visit
http://creativecommons.org/licenses/by-nc-sa/3.0/
ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms3435
8 NATURE COMMUNICATIONS | 4:2435 | DOI: 10.1038/ncomms3435 |
www.nature.com/naturecommunications
& 2013 Macmillan Publishers Limited. All rights
reserved.
title_linkResultsWater-based f-CNT coating of SS fibresFourier
transform infrared spectroscopy
Figure1f-CNT-SS processing steps.A neat SS bundle is mixed with
a dry f-CNT powder. The mixture is then wet, pressed, sheared
between two PTFE substrates, and air dried. Scale bar:
2thinspmmRaman spectroscopy
Figure2Single f-CNT-SS fibre surface profiles.(a) SEM image of
f-CNT-SS. The diameter of the fibre is sim6.5thinspmgrm. Scale bar:
10thinspmgrm. (b,c) Magnified SEM images of f-CNT-SS surface
showing a uniform mat-like covering. Scale bars:
1thinspmgrFigure3FTIR spectra of neat and f-CNT-SS fibres.(a)
Combined FTIR spectra normalised to the amide I peak at
1,625thinspcm-1 (red: neat fibres, blue: f-CNT-SS). (b) Expanded
view of the spectra between 3,000 and 2,800thinspcm-1. Arrows
indicate the posiTensile propertiesElectrical conductivityCustom
shaped f-CNT-SSTemperature-dependent resistanceStrain-dependent
resistancef-CNT-SS annealing and actuator function
Figure4Raman spectra of f-CNT-SS fibre and dry f-CNT powder.The
f-CNT-SS spectrum has been offset to show the linear background
contribution more clearly (blue: f-CNT-SS fibre, red: dry f-CNT
powder). Inset shows background-subtracted and
normalizedFigure5Tensile properties of neat and processed SS single
fibres.Measurement was performed at 25percnt RH to reduce the
effects of water vapour absorption on the tensile properties
(dashed lines: neat fibres, circles: dry supercontracted fibres,
solid liFigure6Custom-shaped f-CNT-SS for clamped and woven
electrodes.(a) Photographs of f-CNT-SS shaped into coil, ring,
knotted and letter forms. (b) Photograph of clamped (IPlusMinus)
and woven (VPlusMinus) contacts used to characterize the
temperature-depFigure7Strain-dependent resistance of f-CNT-SS.(a)
Strain-dependent resistance of a single f-CNT-SS fibre up to
50percnt strain. (b) Cyclic strain test of a single fibre with a
1.2 gauge factor (red line: resistance, blue line: strain). (c)
DemonstratiDiscussionFigure8F-CNT-SS actuator activated by Joule
heating.(a) Photograph of a 35thinspmg mass hanging on a single
f-CNT-SS fibre. Scale bar: 250thinspmgrm. (b) Cyclic f-CNT-SS
contraction. The fibre was allowed to relax for 1thinsph before the
next current cMethodsCNT coatingTEM and SEM imagingFTIR
spectroscopyRaman spectroscopyTensile propertiesResistivity
measurementStrain-dependent resistancef-CNT-SS for heart pulse
monitoringHumidity-dependent resistancef-CNT-SS actuator
RobinsonB. H.E-waste: an assessment of global production and
environmental impactsSci. Total
Environ.4081831912009YangY.Toughness of spider silk at high and low
temperaturesAdv.
Mater.1784882005AllmelingC.JokusziesA.ReimersK.KallS.VogtP. M.Use
of spider sThis work was supported in part by NSF-DMR 1005293 and
1105129, and carried out at the National High Magnetic Field
Laboratory, supported by the NSF, the DOE and the State of Florida.
W.R.S. thanks Fulbright Visiting Scholar 2011 program. The
Barcelona grACKNOWLEDGEMENTSAuthor contributionsAdditional
information