Single-molecule mechanics of mussel adhesion

Abstract

The glue proteins secreted by marine mussels bind strongly to virtually all inorganic and organic surfaces in aqueous environments in which most adhesives function poorly. Studies of these functionally unique proteins have revealed the presence of the unusual amino acid 3,4-dihydroxy-L-phenylalanine (dopa), which is formed by posttranslational modification of tyrosine. However, the detailed binding mechanisms of dopa remain unknown, and the chemical basis for mussels' ability to adhere to both inorganic and organic surfaces has never been fully explained. Herein, we report a single-molecule study of the substrate and oxidationdependent adhesive properties of dopa. Atomic force microscopy (AFM) measurements of a single dopa residue contacting a wet metal oxide surface reveal a surprisingly high strength yet fully reversible, noncovalent interaction. The magnitude of the bond dissociation energy as well as the inability to observe this interaction with tyrosine suggests that dopa is critical to adhesion and that the binding mechanism is not hydrogen bond formation. Oxidation of dopa, as occurs during curing of the secreted mussel glue, dramatically reduces the strength of the interaction to metal oxide but results in high strength irreversible covalent bond formation to an organic surface. A new picture of the interfacial adhesive role of dopa emerges from these studies, in which dopa exploits a remarkable combination of high strength and chemical multifunctionality to accomplish adhesion to substrates of widely varying composition from organic to metallic.3,4-dihydroxylphenylalanine ͉ atomic force microscopy ͉ mussel adhesive protein N umerous living creatures rely on physical adhesion to biotic and abiotic objects for essential activities, such as movement, protection, and self-defense (1-3). From a purely functional point of view, bioadhesion can be of two major types: temporary and permanent. A characteristic example of a temporary bioadhesive strategy is given by the specialized foot hairs used by geckos for climbing sheer surfaces (1). A classic example of permanent bioadhesion is exemplified by mussels, (4) which secrete holdfasts essential for stability within the tidal marine environment. The remarkable features of mussel adhesion include the ability to achieve long-lasting adhesion in a wet environment (3) and adherence to virtually all types of inorganic and organic surfaces (5). The adhesive apparatus of the mussel consists of a series of byssal threads that tether the organism to a substrate (Fig. 1A). At least five specialized adhesive protein subtypes known to contain 3,4-dihydroxy-L-phenylalanine (dopa) at concentrations ranging from a few mol % to 27 mol % (Fig. 1B) are found within the distal adhesive pad of the widely studied blue mussel, Mytilus edulis (6). The highest dopa content occurs in M. edulis foot protein (Mefp)-3 (21 mol %) and Mefp-5 (27 mol %) (7, 8), both of which are localized near the interface between the adhesive pad and the substrate (Fig. 1C).The role of dopa in mussel adhesi...

Self-Assembly and Adhesion of DOPA-Modified Methacrylic Triblock Hydrogels

“…11 In addition, single molecule measurements of the DOPA/TiO 2 interaction indicate that a stronger interaction is observed at low pH than at high pH. 18 A further complicating factor for high pH values is that DOPA oxidation to the quinone form occurs more readily under these conditions, producing forms that are no longer adhesive. These oxidation reactions are presumably responsible for the diminished strength of the DOPA/ TiO 2 interaction observed at high pH values in the single molecule experiments 18 and are observed in our experiments as well.…”

Ultrathin Covalently Bound Organic Layers on Mica: Formation of Atomically Flat Biofunctionalizable Surfaces

“…Despite a general acceptance that the catechol moiety in mussel proteins is central to their adhesion ability,7 its exact adhesion mechanism is still unknown 8. Butler et al.…”

“…Such an approach would require both facile and strong adhesion, combined with the presence of a moiety that can be routinely used for post‐attachment functionalization. The current approaches7, 8 do not provide such a handle, and as such there is still need for a platform that allows various surface modification strategies and a stepwise observation of the assembly processes of biological nanostructures in a controlled fashion 10…”

Resolving Non‐Specific and Specific Adhesive Interactions of Catechols at Solid/Liquid Interfaces at the Molecular Scale

“…The catechol/quinone transformation significantly alters the adhesive properties of Dopa 20. For example, Lee et al 4a. speculated that at high pH Dopa and primary amines possibly crosslink to form strong covalent bonds, as assumed by Burzio and Waite21 earlier.…”

“…In particular, Lee et al 4a. immobilized single, Dopa‐terminated molecules on AFM tips and quantified their adhesion forces and interaction kinetics with titania surfaces.…”