of pHs, but the high activation energy at low pH makes it kinetically stable. At high pH, Dopaquinone forms readily and triggers mfps to solidify, thereby increasing cohesion (Burzio et al., 2000; McDowell et al., 1999; Zhao and Waite, 2006). In this way, Dopa redox modulates the balance between adhesion and cohesion. Although most of the literature focuses on adhesive forces, frictional forces arguably contribute more to holdfast performance. For example, when a single attached byssal thread with a plaque is pulled normal to the surface (e.g. lift), detachment resistance is low and largely adhesive; whereas, when pulled at low angles to the surface (e.g. drag), detachment resistance is an order of magnitude greater due to the added contribution of friction (Begley et al., 2013). Mussels have adaptations at multiple length scales (nm-cm) that utilize friction to dissipate energy (Danner et al., 2012b; Israelachvili et al., 1994), thereby reducing wave impact. These adaptations include, but are not limited to, the radial distribution of anchoring threads (Bell and Gosline, 1998; Qin and Buehler, 2013), the spatulate morphology of plaques (del Campo et al., 2007), the stiff to compliant thread gradient (Bertoldi and Boyce, 2007), the reversible deformation of threads in tension (Carrington, E, Gosline JM, 2006; Waite et al., 1998), and the cuticular coating. As the energy-tolerant, outermost covering of the byssus, the cuticle deserves particular attention for its adaptations against frictional damage because frictional forces are highly context-dependent and can also lead to stress concentration, damage, and catastrophic failure (Holten-Andersen et al., 2009a).
the cuticle granules are pre-formed by condensation of mussel foot protein-1 (mcfp-1) through extensive Dopa-Fe3+-complexation in the accessory gland (Harrington et al., 2010). The cuticle matrix consists of both mfp-1 and an acidic, chymotrypsin-labile, Ca2+-binding protein (Holten-Andersen et al., 2009a; Vitellaro Zuccarello, 1981). The flexible junctions between the granules and the matrix absorb and dissipate the impact of the high-energy surf by micro-cracking (Holten-Andersen et al., 2007) and reversible deformation (Bertoldi and Boyce, 2007; Carrington, E, Gosline JM, 2006), thereby minimizing damage to the byssus and preventing catastrophic failure. Based on these observations, understanding the molecular composition and hierarchical structure of the cuticle may help engineer hard, strain-tolerant materials. Chapter 2. Underwater delivery: Coacervation of mcfp-1 and hyaluronic acid Portions of this chapter have been printed as: Dusty Rose Miller, Saurabh Das, Huang, Songi Han, Jacob N. Israelachvili and J. Herbert Waite, “Mussel adhesive protein-derived complex coacervates mitigate frictional surface damage.” Submitted to Bioscience and Bioengineering June, 2015.
and able to withstand almost twice the strain achieved in the M. edulis cuticle (and its congener M. galoprovincialis) (Holten-Andersen et al., 2007, 2007, 2009a). Understanding these differences in binding tendencies and granule assemblies may contribute to the engineering of strain-tolerant, composite coatings for biomedical applications. Figure 3 - 9 Molecular schematic of mefp-1 and mcfp-1 binding to Fe3+. Left panel showing mcfp-1 binding to the surface and binding to Fe3+ but with free Dopa available for increased Fe3+-binding at high pH. For the sake of clarity, other amino acids are not shown Right panel showing mefp-1 with all available Dopa groups either binding to the surface or binding to Fe3+. Chapter 4. Enhanced wear protection conferred by mcfp1/HA coacervates
coacervate layer—a reconfiguration that has been described as incompressible “molecular ball bearings” (Klein, 2006). To further investigate the mcfp-1/HA coacervate, we adjusted the mixing ratio (7:3 and 3:7) and found that surface wear protection relied on the careful coordination of the mixing ratio. Although mcfp-1/HA coacervate at a 1:1 mixing ratio protected the surfaces from damage at high loads, mcfp-1/HA coacervate at 7:3 and 3:7 mixing ratios suboptimally protected surfaces, which damaged under only a quarter of the applied load (Figure 4a, 5). In this instance, damage was not due to insufficient adhesion—mcfp-1/HA coacervates with an excess of mcfp-1 or HA had higher and more variable adhesive/cohesive energies. Perhaps these molecules not involved in balanced electrostatic interactions (coacervate formation) become entangled, allowing shear forces to impact and damage the surface. The observation that as adhesion increases, wear protection decreases suggests that adhesion has an optimum for mitigating damage. Mussel byssal cuticle toughness and durability is widely attributed to covalent crosslinks and Ca2+ and Fe3+ complexation (Harrington et al., 2010; Holten-Andersen et al., 2009b). However, our results raise the interesting possibility that maintaining coacervates (fluid component) in all or part of the cuticle matrix could be adaptively beneficial for damage control as well as self-healing (by definition, fluids spontaneously self-heal). The excellent frictional damage mitigation by mcfp-1/HA coacervate reveals a significant untapped potential for coacervates in applications that require both adhesion
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