Hypoxia weakens mussel attachment by interrupting DOPA cross-linking during adhesive plaque curing

Marine mussels (Mytilus spp.) attach to a wide variety of surfaces underwater using a network of byssal threads, each tipped with a protein-based adhesive plaque that uses the surrounding seawater environment as a curing agent. Plaques undergo environmental post-processing, requiring a basic seawater pH be maintained for up to 8 days for the adhesive to strengthen completely. Given the sensitivity of plaques to local pH conditions long after deposition, we investigated the effect of other aspects of the seawater environment that are known to vary in nearshore habitats on plaque curing. The effect of seawater temperature, salinity and dissolved oxygen concentration were investigated using tensile testing, atomic force microscopy and amino acid compositional analysis. High temperature (30°C) and hyposalinity (1 PSU) had no effect on adhesion strength, while incubation in hypoxia (0.9 mg l^-1) caused plaques to have a mottled coloration and prematurely peel from substrates, leading to a 51% decrease in adhesion strength. AFM imaging of the plaque cuticle found that plaques cured in hypoxia had regions of lower stiffness throughout, indicative of reductions in DOPA cross-linking between adhesive proteins. A better understanding of the dynamics of plaque curing could aid in the design of better synthetic adhesives, particularly in medicine where adhesion must take place within wet body cavities.