Muscling in on the mussels' grip

In situ Raman spectroscopy has been used to probe the chemical composition of the cuticle of the common bivalve mollusc commonly known as the mussel. The research provides the first direct evidence that the cuticle has a protein-based polymeric scaffold stabilized by dopa-iron complexes, which helps explain how mussels keep their grip on rocks even on the fiercest of stormy shorelines.

Matthew Harrington, Admir Masic, and Peter Fratzl of the Department of Biomaterials, at the Max Planck Institute for Colloids and Interfaces, Potsdam, Germany, Niels Holten-Andersen at the University of California, Santa Barbara and the University of Chicago, and Herbert Waite also at UCSB have prised open the secret of the marine mussel's byssus.

The byssus is a bundle of tough and extensible fibres that allow the animal to attach itself securely to wave-swept coastlines the world over. According to the researchers, localised accumulation of iron-mediated cross-links - dopa-iron complexes - creates hard knobs within an extended support matrix of biological polymer that itself has fewer of these molecular bridges. The knobbly coating of the byssus cuticle can be seen under the electron microscope. Tests reveal it to have epoxy-like hardness, while straining up to 100% without cracking.

The team suggests that mimicking this "design" strategy in novel composites and other materials could allow materials scientists and engineers to work with tough, abrasion-resistant, and stretchable, or extensible, coatings.

Harrington explains the motivation for studying the byssus cuticle: "Protective coatings are important for prolonging the lifetime of materials and devices. However, considering that hardness and extensibility are seldom coupled in engineered polymers or composites, understanding how one protects a flexible substrate becomes quite important." When smaller than microscopic tears occur in the byssal matrix during stretching, the cuticle is not simply ripped apart because these sub-microscopic tears do not proceed to form larger fissures that would otherwise lead to mechanical failure of the byssus and mussel detachment.

Central to understanding the peculiar mechanical behaviour of the cuticle are the high concentration of iron ions in the cuticle and the presence of an uncommon modification of the amino acid tyrosine known commonly as dopa. Dopa is found at high concentrations in the main cuticle component, mussel foot protein-1 (mfp-1), the researchers explain. Dopa is unlike typical amino acids due in that it has a significant affinity for forming chemical complexes with transition metal ions, particularly iron.

By using in situ Raman spectroscopy to probe the chemical composition of the cuticle, the team has obtained directly the first evidence that the cuticle is a protein-based polymeric scaffold stabilized by these dopa-iron complexes. Moreover, they also revealed how the dopa-iron complexes are distributed.

Team member Admir Masic, of the Max Planck Institute for Colloids and Interfaces, explains, "When 2-3 dopa residues complex with a single iron ion, they create an incredibly stable complex that can be utilized to cross-link structural proteins." These metal-protein complexes have a high breaking force (nearly half that of covalent bonds), but unlike covalent bonds they are reversibly breakable, making them ideal for creating sacrificial cross-links.

"Nature has evolved an elegant solution to a problem that engineers are still struggling with; namely, how to combine the properties of abrasion resistance and high extensibility in the same material", says Peter Fratzl, director of biomaterials at the MPI. The fine tuning of metal-protein chemistry and the submicron organization of cross-link density underpins this strategy. "Conceivably, this same strategy could be applied in engineered polymers and composites," he adds.