Catechol-Vanadium Binding Enhances Cross-Linking and Mechanics of a Mussel Byssus Coating Protein

Abstract

Inspired largely by chemistry discovered in the byssus fibers of marine mussels, 3,4-dihydroxyphenylalanine (DOPA)−metal coordination has emerged as an effective cross-linking strategy for producing a range of highperformance supramolecular polymers and adhesives with desirable mechanical properties. Recent findings have revealed that mussels often use vanadium in these complexes to enhance the cohesion, rather than solely iron as conventionally believed. Here, we utilized a recombinant DOPA-functionalized mussel protein (rMfp-1-DOPA) to investigate the implications of vanadium-based cross-linking using both nanomechanical and spectroscopic methods. We discovered that DOPA−V cross-linking can strengthen the cohesion of the protein network by nearly twofold compared with DOPA−Fe. Spectroscopic analysis with UV−vis, Raman, and EPR indicated that vanadium is more effective at forming tris-DOPA−metal complexes under the pH ranges relevant to byssus formation and function, especially when starting with the V III form. Furthermore, when compared with a pure catechol control, rMfp-1-DOPA can form DOPA−V complexes at very low pH values relevant to the byssus formation process, suggesting that the protein sequence may be adapted for V binding. These findings provide evidence that DOPA−V coordination is advantageous for both the formation and function of the byssus, which is highly relevant for continued efforts to develop mussel-inspired metallopolymers.

Essential Role of Thiols in Maintaining Stable Catecholato-Iron Complexes in Condensed Materials

“…Not surprisingly, the addition of Fe 3+ to the like-charged mfp-1 coacervates with DTT significantly elevated cohesion (199.4 ± 12.1 mN at pH 5.5 and 289.42 ± 58.62 at pH 7), given the formation of Fe-DOPA complexes and enhanced electrostatic adhesion between positively charged lysine and negatively charged Fe-DOPA complex. Diluted mfp-1 (no coacervate) exhibited high cohesive forces with metals but without thiols in previous SFA experiments. , This SFA result demonstrates that the mfp-1 coacervates exhibit their highest cohesive forces with FeCl 3 under DTT-reducing conditions. In addition, it suggests that the rheology of mfp-1 coacervates can be toggled up or down depending on the oxidation and metal coordination state of DOPA.…”

“…Diluted mfp-1 (no coacervate) exhibited high cohesive forces with metals but without thiols in previous SFA experiments. 18,50 This SFA result demonstrates that the mfp-1 coacervates exhibit their highest cohesive forces with FeCl 3 under DTT-reducing conditions. In addition, it suggests that the rheology of mfp-1 coacervates can be toggled up or down depending on the oxidation and metal coordination state of DOPA.…”

Microfluidic-like fabrication of metal ion–cured bioadhesives by mussels

“…Furthermore, the detection of V in the MSPs is especially noteworthy because it is seldom used in biology in functional roles—especially not as a cross-linking element in materials ( 34 ). It has been recently shown that mussels may preferentially use DOPA-V cross-links to mechanically stabilize the outer protective cuticle of the byssus ( 13 ), and in vitro nanomechanical studies have shown that DOPA-V cross-linking can provide cohesive forces between byssus protein films that are nearly twofold greater than those with DOPA-Fe cross-linking ( 35 ). However, this metal preference has not yet been corroborated in the plaque.…”

Probing and Manipulating Noncovalent Interactions in Functional Polymeric Systems

“…Besides Fe 3+ , catechol is also able to coordinate with other metals (e.g., Cu, Zn, Al), and its interaction with vanadium (in the form of V 3+ and VO 2– ) was investigated. At the same ion concentration, the cohesion measured between two recombinant mfp-1 films in the presence of V is much higher than that with Fe, following the trend of V 3+ > VO 2– > Fe 3+ , and the formation of tris-catechol–V complexes could occur at much lower pH values (e.g., pH = 4) . Lee et al detected the interactions of an individual catechol group on a Ti surface by SMFS, and the measured rupture force suggested a dissociation energy of ∼93 kJ/mol, attributed to a strong catechol–Ti coordination .…”

“…At the same ion concentration, the cohesion measured between two recombinant mfp-1 films in the presence of V is much higher than that with Fe, following the trend of V 3+ > VO 2− > Fe 3+ , and the formation of tris-catechol−V complexes could occur at much lower pH values (e.g., pH = 4). 136 Lee et al detected the interactions of an individual catechol group on a Ti surface by SMFS, and the measured rupture force suggested a dissociation energy of ∼93 kJ/mol, attributed to a strong catechol−Ti coordination. 137 This coordination was also demonstrated to be regulated by solution pH.…”