Humidity-Driven Supercontraction and Twist in Spider Silk.

Spider silk is a protein material that exhibits extraordinary and nontrivial properties such as the ability to soften, decrease in length (i.e., supercontract), and twist upon exposure to high humidity. These behaviors stem from a unique microstructure in combination with a transition from glassy to rubbery as a result of humidity-driven diffusion of water. In this Letter we propose four length scales that govern the mechanical response of the silk during this transition. In addition, we develop a model that describes the microstructural evolution of the spider silk thread and explains the response due to the diffusion of water molecules. The merit of the model is demonstrated through an excellent agreement to experimental findings. The insights from this Letter can be used as a microstructural design guide to enable the development of new materials with unique spiderlike properties.

On the Origin of Supercontraction in Spider Silk.

Spider silk is a protein material that exhibits extraordinary and nontrivial properties such as the ability to soften and decrease its length by up to ∼60% upon exposure to high humidity. This process is commonly called supercontraction and is the result of a transition from a highly oriented glassy phase to a disoriented rubbery phase. In this work, we derive a microscopically motivated and energy-based model that captures the underlying mechanisms that give rise to supercontraction. We propose that the increase in relative humidity and the consequent wetting of a spider silk have two main consequences: (1) the dissociation of hydrogen bonds and (2) the swelling of the fiber. From a mechanical viewpoint, the first consequence leads to the formation of rubbery domains. This process is associated with an entropic gain and a loss of orientation of chains in the silk network, which motivates the contraction of the spider silk. The swelling of the fiber is accompanied by the extension of chains in order to accommodate the influx of water molecules. Supercontraction occurs when the first consequence is more dominant than the second. The model presented in this work allows us to qualitatively track the transition of the chains from glassy to rubbery states and determine the increase in entropy, the loss of orientation, and the swelling as the relative humidity increases. We also derive explicit expressions for the stiffness and the mechanical response of a spider silk under given relative humidity conditions. To illustrate the merit of this model, we show that the model is capable of capturing several experimental findings. The insights from this work can be used as a microstructural design guide to enable the development of new materials with unique spider-like properties.

Molecular Mechanics of Beta-Sheets.

ß-Sheet protein structures and domains are widely found in biological materials such as silk. These assemblies play a major role in the extraordinary strength and unique properties of biomaterials. At the molecular level, the single ß-sheet structure comprises polypeptide chains in zig-zag conformations that are held together by hydrogen bonds. ß-sheet domains comprise multiple ß-sheets that originate from hydrophobic interactions between sheets and are held together by van der Waals interactions. In this work, we introduce molecular models that capture the response of such domains upon mechanical loading and illustrate the mechanisms behind their collapse. We begin by modeling the force that is required to pull a chain out of a ß-sheet. Next, we employ these models to study the behavior of ß-sheets that are embedded into and connected to an amorphous protein matrix. We show that the collapse of a ß-sheet occurs upon the application of a sufficiently high force that is transferred from the chains in the matrix to individual chains of the ß-sheet structure and causes shear. With the aim of understanding the response of ß-sheet domains, we derive models for the interactions between ß-sheets. These enable the study of critical forces required to break such domains. As opposed to molecular dynamics simulations, the analysis in this work yields simple expressions that shed light on the relations between the nanostructure of ß-sheet domains and their mechanical response. In addition, the findings of this work suggest how ß-sheet domains can be strengthened.

A microscopically motivated model for the swelling-induced drastic softening of hydrogen-bond dominated biopolymer networks.

The penetration of water into rubber-like protein networks such as cross-linked resilin, which is found in insects, can lead to changes in stiffness that range over several orders of magnitude. This softening effect cannot be explained by the volumetric changes associated with pure swelling/deswelling used to describe networks with covalent bonds. Rather, this property stems from the reversible swelling-induced breaking of hydrogen cross-linking bonds that connect the chains in the network. This work presents a model for the swelling and the mechanical response of hydrogen-bond dominated biopolymer networks. It is shown that the penetration of water molecules into the network leads to the breaking of non-covalent cross-linking sites. In turn, the network experiences a reduction in the effective chain-density, an increase in entropy, and a consequent decrease in free energy, thus explaining the dramatic softening. Additionally, the breaking of hydrogen bonds alters the micro-structure and changes the quantitative elastic behavior of the network. The proposed model is found to be in excellent agreement with several experimental findings. The merit of the work is twofold in that it (1) accounts for the number and the strength of non-covalent cross-linking bonds, thus explaining the drastic reduction in stiffness upon water uptake, and (2) provides a method to characterize the micro-structural evolution of hydrogen-bond dominated networks. Consequently, the model can be used as a micro-structural design-guide to program the response of synthetic polymers. STATEMENT OF SIGNIFICANCE: Hydrogen-bond dominated biopolymer networks are found in insects and have a unique structure that allows a dramatic reduction of several orders of magnitude in stiffness upon hydration. Understanding the micro-structure of such networks is key in the fabrication of new biomimetic polymers with tunable mechanical properties. This work introduces a microscopically motivated model that explains the dramatic reduction in stiffness and quantifies the influence of key micro-structural quantities on the overall response. The model is validated through several experimental findings. The insights from this work motivate further attempts at the fabrication of new biomimetic polymers and serve as a micro-structural design guide that enables the programming of the elastic swelling-induced response.

Toughening elastomers using mussel-inspired iron-catechol complexes.

Materials often exhibit a trade-off between stiffness and extensibility; for example, strengthening elastomers by increasing their cross-link density leads to embrittlement and decreased toughness. Inspired by cuticles of marine mussel byssi, we circumvent this inherent trade-off by incorporating sacrificial, reversible iron-catechol cross-links into a dry, loosely cross-linked epoxy network. The iron-containing network exhibits two to three orders of magnitude increases in stiffness, tensile strength, and tensile toughness compared to its iron-free precursor while gaining recoverable hysteretic energy dissipation and maintaining its original extensibility. Compared to previous realizations of this chemistry in hydrogels, the dry nature of the network enables larger property enhancement owing to the cooperative effects of both the increased cross-link density given by the reversible iron-catecholate complexes and the chain-restricting ionomeric nanodomains that they form.

Microphase Behavior and Enhanced Wet-Cohesion of Synthetic Copolyampholytes Inspired by a Mussel Foot Protein.

Numerous attempts have been made to translate mussel adhesion to diverse synthetic platforms. However, the translation remains largely limited to the Dopa (3,4-dihydroxyphenylalanine) or catechol functionality, which continues to raise concerns about Dopa's inherent susceptibility to oxidation. Mussels have evolved adaptations to stabilize Dopa against oxidation. For example, in mussel foot protein 3 slow (mfp-3s, one of two electrophoretically distinct interfacial adhesive proteins in mussel plaques), the high proportion of hydrophobic amino acid residues in the flanking sequence around Dopa increases Dopa's oxidation potential. In this study, copolyampholytes, which combine the catechol functionality with amphiphilic and ionic features of mfp-3s, were synthesized and formulated as coacervates for adhesive deposition on surfaces. The ratio of hydrophilic/hydrophobic as well as cationic/anionic units was varied in order to enhance coacervate formation and wet adhesion properties. Aqueous solutions of two of the four mfp-3s-inspired copolymers showed coacervate-like spherical microdroplets (ϕ ≈ 1-5 µm at pH ∼4 (salt concentration ∼15 mM). The mfp-3s-mimetic copolymer was stable to oxidation, formed coacervates that spread evenly over mica, and strongly bonded to mica surfaces (pull-off strength: ∼17.0 mJ/m(2)). Increasing pH to 7 after coacervate deposition at pH 4 doubled the bonding strength to ∼32.9 mJ/m(2) without oxidative cross-linking and is about 9 times higher than native mfp-3s cohesion. This study expands the scope of translating mussel adhesion from simple Dopa-functionalization to mimicking the context of the local environment around Dopa.

Aggregation behavior of rodlike ionogenic polymers in chloroform.

The rodlike ionogenic polymers poly(p-pyridylene-phenylene) and poly(p-pyridylene/phenylene-ethynylene) form polyelectrolytes when protonated with toluene sulfonic acid or ethane sulfonic acid in chloroform solution. This molecular modification, clearly indicated by a marked red shift of the UV absorption band, induces the formation of prolate, bundlelike aggregates, whose size and shape are obtained from their rotational dynamics as revealed by electric birefringence relaxation and their translational dynamics as measured by dynamic light scattering. The aggregates have a length of 400-600 nm and a high aspect ratio >15. In general, the polyelectrolyte molecules are arranged with their long axes parallel to the long axis of the aggregates. They probably attract each other through the electrostatic interaction with counterions. The counterions are not bound to specific sites but may be shifted under the action of an external electric field to account for the highly anisotropic electric polarizability. When inert salt or excess sulfonic acid is added, these compounds seem to accumulate within the aggregates and influence the attractive forces. This is generally leading to an elongation of the aggregates and, in the case of added salts, even to a marked reduction of birefringence.