Natural underwater adhesives

Abstract

The general topic of this review is protein-based underwater adhesives produced by aquatic organisms. The focus is on mechanisms of interfacial adhesion to native surfaces and controlled underwater solidification of natural water-borne adhesives. Four genera that exemplify the broad range of function, general mechanistic features, and unique adaptations are discussed in detail: blue mussels, acorn barnacles, sandcastle worms, and freshwater caddisfly larva. Aquatic surfaces in nature are charged and in equilibrium with their environment, populated by an electrical double layer of ions as well as adsorbed natural polyelectrolytes and microbial biofilms. Surface adsorption of underwater bioadhesives likely occurs by exchange of surface bound ligands by amino acid sidechains, driven primarily by relative affinities and effective concentrations of polymeric functional groups. Most aquatic organisms exploit modified amino acid sidechains, in particular phosphorylated serines and hydroxylated tyrosines (dopa), with high-surface affinity that form coordinative surface complexes. After delivery to the surfaces as a fluid, permanent natural adhesives solidify to bear sustained loads. Mussel plaques are assembled in a manner superficially reminiscent of in vitro layer-by-layer strategies, with sequentially delivered layers associated through Fe(dopa)3 coordination bonds. The adhesives of sandcastle worms, caddisfly larva, and barnacles may be delivered in a form somewhat similar to in vitro complex coacervation. Marine adhesives are secreted, or excreted, into seawater that has a significantly higher pH and ionic strength than the internal environment. Empirical evidence suggests these environment triggers could provide minimalistic, fail-safe timing mechanisms to prevent premature solidification (insolubilization) of the glue within the secretory system, yet allow rapid solidification after secretion. Underwater bioadhesives are further strengthened by secondary covalent curing.

Byssal proteins of the freshwater zebra mussel,Dreissena polymorpha

“…Charge separation has also been observed in an adhesive protein of the sandcastle worm (Phragmatopoma californica), pc-3A, which has an acidic N-terminus and basic C-terminus (Wang & Stewart 2012). Like zebra mussels, sandcastle worms also contain both acidic and basic proteins (Endrizzi & Stewart 2009;Stewart et al 2011). It has been suggested that such segregation of charges indicates a possible role for complex coacervation in the adhesion process of marine mussels and sandcastle worms, which has several advantages for underwater adhesion, as recently reviewed elsewhere (Lee et al 2011).…”

Microphase Behavior and Enhanced Wet-Cohesion of Synthetic Copolyampholytes Inspired by a Mussel Foot Protein

“…6,7 Coacervation benefits adhesion in several important ways: (1) high polymer concentration increases density, (2) the low interfacial energy improves wetting, (3) high diffusivity maintains good mixing, and (4) reduced viscosity eases delivery. 1 Mfp-3s is localized to the plaque−substratum interface ( Figure 1b) together with mfp-3f and mfp-5. Due to its amphiphilic and ampholytic structural characteristics (Figure 2a), mfp-3s is capable of self-coacervation 8 and is more stable at oxidation than other mfps.…”

Correlation between surface chemistry and settlement behaviour in barnacle cyprids (Balanus improvisus)

“…In aqueous environments, the capacity of materials to wet and de-wet plays an important role in the interfacial dynamics between the substrate, water and adhesives of fouling organisms Petrone 2013). Such sessile organisms have developed specialised sensory systems that enable them to find optimal substrates via detection of surface physicochemical features (Clare & Nott 1994;Callow et al 2005;Aldred et al 2006;Bielecki et al 2009;Stewart et al 2011). Many fouling organisms, such as barnacles and mussels, have evolved adhesive secretions with superior abilities compared to synthetic glues, to attach to submerged surfaces with diverse properties (Nott 1969;Ödling et al 2006;Stewart et al 2011;Kamino 2013).…”

“…Such sessile organisms have developed specialised sensory systems that enable them to find optimal substrates via detection of surface physicochemical features (Clare & Nott 1994;Callow et al 2005;Aldred et al 2006;Bielecki et al 2009;Stewart et al 2011). Many fouling organisms, such as barnacles and mussels, have evolved adhesive secretions with superior abilities compared to synthetic glues, to attach to submerged surfaces with diverse properties (Nott 1969;Ödling et al 2006;Stewart et al 2011;Kamino 2013). These highly specialised glues thus allow fouling organisms to cope with the unpredictability of surfaces found in the marine environment (Nott & Foster 1969;Walker & Yule 1984;Aldred & Clare 2008;Aldred et al 2011;Maruzzo et al 2011).…”