Professional Documents
Culture Documents
THE EUROPEAN
PHYSICAL JOURNAL E
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK
Department of Macromolecular Science and Key Laboratory of Molecular Engineering of Polymers of Ministry of Education,
Fudan University, 200433 Shanghai, P.R. China
Received 4 August 2004 / Received in nal form 6 October 2004
c EDP Sciences, Societ`
Published online 22 February 2005
a Italiana di Fisica, Springer-Verlag 2005
Abstract. Spider silk is attractive because it is strong and tough. Moreover, an enormous range of mechanical properties can be achieved with only small changes in chemical structure. Our research shows that
the full range of thermo-mechanical properties of silk bres can be predicted from mean eld theory for
polymers in terms of chemical composition and the degree of order in the polymer structure. Thus, we can
demonstrate an inherent simplicity at a macromolecular level in the design principles of natural materials.
This surprising observation allows in depth comparison of natural with man-made materials.
PACS. 87.15.La Mechanical properties 81.05.Lg Polymers and plastics; rubber; synthetic and natural
bers; organometallic and organic materials
1 Introduction
Spider silk is a strong and tough polypeptide that is optimised by nature to full a wide range of functions using
subtle changes in chemical composition and, importantly,
morphological structure at a nanometer scale [1,2]. Attempts to emulate the attractive properties of silk and
other natural polymers are frustrated by a lack of quantitative structure-property relations, which are the subject
of this work.
In order to develop a quantitative model for silk, let us
take the radical step of looking at silk from the perspective
of a user. Silk bres are produced by a spider to manage
mechanical energy for dierent tasks without breaking: to
store elastic energy in supporting its own weight or for the
structural framework of a web, and to absorb kinetic energy to capture ying insects. Here we identify the mechanisms at a molecular level that dictate energy storage
and dissipation in a polymer and derive straightforward
analytical relations for the full range of mechanical properties that are possible in silk. These relations are expressed
in terms of a small number of energy-based parameters
with a direct fundamental link to chemical composition
and morphological order. In this way, we hope to elucidate some of the key design principles in natural polymers.
Moreover, this approach can be applied also to much simpler man-made polymers, thereby oering the potential
for the design of improved synthetic polymers.
Why look specically at spider silk? Although silkworm silk is strong, the oscillatory motion of the worm
during spinning leads to great uctuations in mechanical properties [3,4]. Spider silks, on the other hand, are
evenly spun, which provides a model natural bre with
superb combinations of strength and toughness. Such silks
range from drag-line with a modulus and strength of about
10 GPa and 1 GPa respectively to capture thread with a
more modest strength, but because of its high extensibility
a comparably high toughness.
Figure 1 shows a schematic diagram of the stressstrain prole of a silk bre through a general loading cycle and also the deformation through to break. The initial modulus, Ei , takes an upper value for dragline silk of
about 15 GPa, down to about 4 GPa for capture thread.
The yield strain, y , under ambient conditions is usually
about 2%. Other parameters of yield stress, y , post-yield
modulus, Ey , and stress and strain to break, b and b respectively, are dependent upon the detailed composition
and morphology of the silk polymer. Generally, a high initial modulus and failure stress has a lower strain to failure,
and vice versa.
Recent experimental measurements of dynamic mechanical and stress-strain properties of single bres of
Nephila Major Ampullate drag-line silk (over a wide range
of temperatures from 100 to +350 C) suggest that the
mechanisms in silk deformation are no more complex than
for any other semi-crystalline polymer [5]. The small insert
in Figure 1 is a typical stress-strain plot at 15 C while
Figure 2 shows the temperature dependence of dynamic
tensile modulus and loss tangent for the same silk, with
200
Fig. 1. Schematic diagram of the stress-strain prole of a spider silk in a deformation cycle and during strain to break.
The insert shows experimental curves for a dragline silk discussed in the text. The numbered regions relate to the following
deformation processes: 1. Initial elastic zone through to yield: amorphous domains change from glass to rubberlike states at
yield. 2. Post-yield elastic zone of a crystal-reinforced rubber. 3. Plastic zone as mechanical energy transforms rubber states
back to glass. 4. Recoverable elastic energy: approximately the sum of zones 1 and 2.
Fig. 2. Experimental DMTA data for tensile modulus and loss tangent and initial modulus from tensile tests for the mechanical
properties of a dragline silk discussed in the text.
rubber, but glassy, which means that care must be exercised in the use of the term rubber in any model [7]. The
conventional alternative to network models for polymers
is detailed molecular dynamics simulations [12]. However,
structures such as silk require enormous model calculations to simulate dimensions and time scales far shorter
than those of experiment. Consequently understanding
the mechanisms that quantitatively control complex mechanical properties are at present virtually impossible
with such a black-box approach. The same comments on
structure-property relations can be applied equally well to
semicrystalline synthetic polymers and bres, which are
dominated by phenomenological models, based upon continuum theory [13,14].
2 Model
Our work is based on two premises of energy storage and
energy dissipation. The rst implies that the high modulus
and great strength of silk are due to the high cohesive
energy density of hydrogen bonding between the amide
segments of the backbone in the primary silk protein
(Spidroin) molecules. The second premise implies that silk
toughness is due to the high energy density absorbed in
the post-yield work-hardening phase through to break.
The premises are derived from the dierent molecular
level mechanisms characterised in the stress-strain prole of Figure 1 i.e. 1) the change at yield of the amorphous domains from glass to rubber 2), the post-yield
complex modulus 3), the plastic behaviour as the rubbery
state converts back to glass and 4) the recoverable elastic
energy.
The analysis uses a mean-eld modelling method
called Group Interaction Modelling (GIM) that has been
used before to predict the engineering properties of polymers like poly(styrene) and poly(carbonate) [15]. GIM applies the ensemble average values of the thermodynamic
energy terms of a characteristic mer unit (at a molecular
level) to a potential function that quanties the relationship between intermolecular energy and separation distance between polymer chains. Thus, GIM allows analytical structure-property relations for mechanical properties
to be derived by a combination of mathematical processing
of the potential function and application of continuumlevel physics of a materials energy-storage and energyloss. Hence, the quantitative physical links between structure and properties are transparent at all stages of the
modelling process.
To avoid unnecessary controversy over crystalline fractions (see introduction), let us take the straightforward
position that silk consists of ordered and disordered
phases, and that the more rigid ordered domains are dispersed at a nanometer scale within the less rigid amorphous phase. The nanoscale morphology allows the two
phases to share energy at the molecular level and behave
in bulk as a homogeneous material (e.g. [16]). Energy sharing at a nanoscale is a key aspect in natural materials, and
has been discussed quantitatively for bone, which consists
of organic and inorganic layers to form a rigid and tough
natural hybrid nanocomposite [17].
201
Co = 52 kJ/mol ordered or
42 kJ/mol disordered
Vw = 40 cc/mol
M = 72
N =8
= 400 K
The Lennard-Jones potential function for the binding energy, C, per group for a strongly bonded onedimensional polymer chain in a weak three-dimensionally
202
bonded lattice can be written in terms of the thermal energy of skeletal mode vibrations, HT , and the congurational energy, Hc , by
C = Co + Hc + HT = Co + Hc +
3
6
Vo
Vo
= Co
2
V
V
N R T D1 (T )
4
(1)
d2 C
C
= 18
2
dV
V
(2)
is then the fraction of mechanical energy converted irreversibly to heat. The most appropriate form of the model
expression is
1.5 105 L B dE
B dE
=
.
(3)
tan A
E dT
M
E dT
The parameter A takes a general value of about unity in
units of K/GPa, and specically for poly(alanine) A
1.5 K/GPa. This expression can be inverted to allow elastic modulus to be calculated from the loss prole of a polymer, which is easier to predict from the chemical structure
using models for relaxation mechanisms. Note that bulk
modulus is the reference value of elastic modulus before
any relaxation mechanisms allow transient spatial redistribution of groups of atoms under strain to reduce the
value of modulus
tan dT
E = B exp
.
(4)
AB
The loss tangent peaks of the silk in Figure 2 are due to relaxation events in the dierent atomic groups of the polymer chain. In particular, the peaks below about 300 C
are local phase transition events in the disordered fraction.
The peak at about 70 C is conventionally attributed to
hydrocarbon interactions [26], and the higher temperature
peak at about 200 C is shown below to be attributed to
amide segment interactions. The temperature of the peaks
can be predicted as local glass transition temperature, Tg ,
events in terms of model parameters for the specic group
interactions by the relation [15]
Tg = 0.224 + 0.0513
Co
.
N
(5)
203
Co (J/mol)
Tg (K/ C)
tan
Fraction
Hydrocarbon
9000
205/68
19
0.5
Amide: 1 H-bond
33000
4 + fdis
479/206
68
0.5
Fig. 3. Predicted dynamic mechanical properties for a model silk with ford = 0.66, to be compared with the experimental plots
in Figure 2.
4 Stress-strain profile
Energy in the potential function used to predict thermomechanical properties in silk is dependent upon the dimensions occupied by the interacting groups of atoms.
This can be used to make a transformation of the temperature dependent dynamic mechanical properties to predictions of stress-strain curves to break. To do this, temperature, T , is used as a dummy variable to calculate
consistent pairs of values of strain, , and tensile stress, ,
using the linear coecient of thermal expansion, , that
is predicted in GIM by the relation derived by dierentiating the potential function of equation (1) with respect
to temperature
0.45
N
0.0001 K1
Co
T
=
T
dT
(7)
E dT .
(8)
Five key parameters are needed to map the overall stressstrain proles that are possible with spider silk: initial
204
(a)
(b)
Fig. 4. (a) Predicted stress-strain proles of silks with dierent degrees of order, ford . (b) Experimental stress-strain curves
for silks within the predicted envelope of properties shown as a dashed line: silks curves identied by markers at break point:
various dragline silks (4), Bombyx mori drawn evenly at dierent rates [3, 4], Argiope trifasciata dragline silk [31],
Laboratory spun recombinant silk based upon Spidroin II [32].
Ey (b y ) Ng R T D1 (T )
=
2
V
1.2 108 J/m3 . (9)
The left hand side of equation (9) is the mechanical energy density as the sum of plastic and elastic terms, which
are regions 2 and 3 in Figure 1. The right hand side of
equation (9) is the change in energy due to the change in
degrees of freedom through the phase change, and its numerical value is a direct quantitative measure of the toughness of a polymer as the area under a stress-strain curve
to break. For example, synthetic engineering polymers
poly(carbonate) and poly(ether ether ketone) (PEEK)
have values 0.5 108 and 0.4 108 J/m3 respectively, and
are thus far less tough than spider silk by a factor of more
than two. Polymers such as poly(ethylene) and Nylon may
have comparable model measures of toughness, but they
require a high degree of molecular orientation to achieve
the stiness of dragline silk and do not have the higher
temperature stability imparted by the hydrogen bonding
in the high amide group concentration in dry silk.
For ease of calculation, the Debye function takes a
value of 0.7 for the model = 400 K and the volume
is taken to be V 1.5Vw = 60 cc/mol. Figure 4a shows
the full range of stress strain proles predicted for the
model silk at dierent values of the single model variable ford , and all other parameters are calculated from
ford using the structure-property relations derived above.
Experimental plots of stress-strain for some typical silk
types are plotted in Figure 4b for comparison with predictions, with each curve labelled or explained in the gure
caption. The overall limiting envelope of predicted stressstrain proles has the correct general form, and future
work will explore the detailed bounds of the failure envelope due to energy absorption mechanisms post-yield,
such as the formation of new hydrogen bonds in the more
oriented strained structure.
205
Co
(kJ/mol)
24.3
56
16
10
3
1
2
1
1
0
4.5
28.8
35.8
18
45
10.8
0
10.2
36.1
58.5
40.8
52.8
15.2
0
15
72
107
57
101
31
0
2
5
4
4
7
3
7.7
32
12
41
12
68
2
8
Group
Structure
Number
Peptide base
-R groups
Glycine (G)
Alanine (A)
Glutamine (Q)
Tyrosine (Y)
Leucine (L)
Arginine (R)
Serine (S)
- CCONH -H
-CH3
-CH2 CH2 CONH2
-CH2 PhOH
-CH2 C(CH3 )2
-CH2 CH2 CH2 NHC(NH2 )2
-CH2 OH
Average -R
Total average
Modelling was originally formulated to develop structureproperty relations for polymer processing rheology and
to include such non-Newtonian eects as shear-thinning
and strain-induced crystallisation due to macromolecular
strain [30]. Thus, we expect that the model presented here
for silk properties will provide a valuable direct link to help
understand the production of silk bres with controlled
mechanical properties.
For funding we thank the British EPSRC (grant
GR/NO1538/01) and BBSRC (S12778) as well as the
European Commission (grant G5RD-CT-2002-00738), the
National Natural Science Foundation of China (NSFC,
No. 20244005) and the AFSOR of the United States of
America (grant F49620-03-1-0111).
206
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
References
1. D. Fox, New Scientist, 24 April 1999, pp. 3841
2. F. Vollrath, Reviews in Molecular Biotechnology 74, 67
(2000)
3. Z. Shao, F. Vollrath, Nature 418, 741 (2002)
4. F. Vollrath, D. Knight, in Handbook of Biopolymers, edited
by A. Steinb
uchel, S. Fahnestock (Wiley-VCH, Heidelberg
and New York, 2003), Chap. 2, p. 25
5. Z. Shao, Y. Yang, X. Chen, P. Zhou, D. Knight, D. Porter,
F. Vollrath, Spider silk performs as much tougher material
at low temperatures, Adv. Mater. (in press)
6. D.T. Grubb, L.W. Jelinski, Macromolecules 30, 2860
(1997)
7. J.D. van Beek et al., PNAS 99, 10266 (2002)
8. B.L. Thiel et al., Biopolymers 34, 1089 (1994); B.L. Thiel,
Biopolymers 41, 703 (1997)
9. J.M. Gosline et al., in Silk Polymers: Materials Science and
Biotechnology, edited by Kaplan et al., ACS Symposium
Series 544 (ACS Press, New York, 1994), Chap. 27, p. 328
10. M.A. Becker et al., in Silk Polymers: Materials Science and
Biotechnology, edited by Kaplan et al., ACS Symposium
Series 544 (ACS Press, New York, 1994), Chap. 17, p. 185
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.