PerspectiveMaterials Science

Holding On by a Hard-Shell Thread

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Science  09 Apr 2010:
Vol. 328, Issue 5975, pp. 180-181
DOI: 10.1126/science.1187598

Mussels anchor to surfaces in turbulent aqueous environments with a remarkable acellular tissue, the byssus, or “beard.” The threadlike byssal attachments are strong yet highly extensible, and have a thin cuticle coat that is harder than the core of the thread itself. On page 216 of this issue, Harrington et al. (1) present results that show how the chemistry of byssal thread cuticle may impart these distinctive mechanical properties.

The major cuticular protein in mussels, called mfp-1 (mussel foot protein 1), contains 10 to 15 mol % of the catecholic amino acid 3,4-dihydroxyphenyl-l-alanine (dopa). The core proteins of the threads are collagen-like and contain very little dopa. The mussel employs a truly elegant approach to byssal thread fabrication (see the figure). In a series of events that are reminiscent of industrial approaches to polymer injection molding, the mussel injects liquid protein solution onto the substrate surface and into a groove along the length of the foot. The protein solidifies in a short period of time. Detachment of the foot reveals the newly formed thread and adhesive plaque. The mussel then repeats this process many times to secure its attachment to the substrate.

The mussel relies on the durability of the byssus for its survival. The byssal threads have very robust mechanical properties, and have been shown to have self-healing capacity (2). Harrington et al. focused on the mechanochemistry of the byssal thread cuticle. Earlier studies of byssal threads revealed the cuticle to be about five times as stiff as the core and enriched in iron and calcium, but otherwise free of detectable inorganic mineral phases (3, 4). Catechols are known to have a high affinity for transition metals, including iron, and iron ions can bind either two or three dopa molecules to form bis- and tris-complexes, respectively (5).

Making strong attachments.

A still image is shown of a mussel attached to a surface. The attachment process is revealed in movie S1. As the foot detaches from the surface, it leaves behind an intact byssal thread and adhesive pad.

Movie S1

Video showing mussel attachment process in detail.

The possibility of iron complexation by dopa, together with evidence for colocalization of mfp-1 and iron in the thread cuticle, has led to speculation of a mechanical role for dopa-iron complexes (4). However, direct chemical and spectroscopic evidence for the localization of dopa-iron complexes in byssal thread cuticle has been lacking. Harrington et al. filled this gap and established a framework for understanding the possible mechanical function of dopa-iron coordination in the mussel byssal thread cuticle. The authors used in situ confocal Raman spectroscopy on slices of byssal thread tissue to demonstrate the existence of dopa-iron complexes within the thread cuticle. The submicrometer resolution of the technique allowed detection of higher dopa-iron content within cuticular granules as opposed to the continuous cuticular matrix.

An earlier observation that cuticle hardness is reduced by ∼50% upon chelation of iron by EDTA (3), along with the observation by Harrington et al. of a disappearance of Raman spectroscopic signal of dopa-iron, suggested a connection between dopa-iron complexes and mechanical properties (3). The authors propose a model whereby dopa-iron complexation contributes both hardness and extensibility to the thread cuticle. Additional detailed experiments will likely be necessary to further elucidate the chemomechanical basis for these properties. However, single-molecule experiments have demonstrated substantial bond-rupture forces between dopa and metal oxide surfaces (6). These results, together with the successful use of catechols as anchors for grafting molecules onto metal oxide surfaces (711), leave little doubt that dopa-metal coordination interactions of the type spectroscopically detected by Harrington et al. can impart mechanical stabilization.

Evidence is accumulating for metal coordination as a biological strategy for fabricating mechanically competent organic tissues in which there is little or no inorganic mineral present. For example, in the case of the hard load-bearing jaws of polychaetes, a type of annelid worm, coordination complexes between histidine and copper or zinc are suggested to play an important role in mechanical performance of the tissue (12). By contrast, in the dopa-iron complexes of the byssal thread cuticle, metal coordination occurs entirely through catechol.

Metal coordination bonds acting as crosslinks in polymer and protein systems are expected to behave quite differently under applied force than covalent cross-links do. For example, coordination bonds can be considered sacrificial, in that they can break under an applied load, but then re-form when the load is withdrawn. It will be interesting to see if this molecular behavior proves to be the underlying basis of the macroscopic observations of self-healing in byssal threads. Synthetic materials scientists exploiting dopa-iron complexes will likely be inspired by this study. Indeed, one report exists of self-assembly and stabilization of collagen-like peptides mediated by catechol-iron interactions (13).

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