Mussel adhesion is dictated by time-regulated secretion and molecular conformation of mussel adhesive proteins

Abstract

Interfacial water constitutes a formidable barrier to strong surface bonding, hampering the development of water-resistant synthetic adhesives. Notwithstanding this obstacle, the Asian green mussel Perna viridis attaches firmly to underwater surfaces via a proteinaceous secretion (byssus). Extending beyond the currently known design principles of mussel adhesion, here we elucidate the precise time-regulated secretion of P. viridis mussel adhesive proteins. The vanguard 3,4-dihydroxy-L-phenylalanine (Dopa)-rich protein Pvfp-5 acts as an adhesive primer, overcoming repulsive hydration forces by displacing surface-bound water and generating strong surface adhesion. Using homology modelling and molecular dynamics simulations, we find that all mussel adhesive proteins are largely unordered, with Pvfp-5 adopting a disordered structure and elongated conformation whereby all Dopa residues reside on the protein surface. Time-regulated secretion and structural disorder of mussel adhesive proteins appear essential for optimizing extended nonspecific surface interactions and byssus' assembly. Our findings reveal molecular-scale principles to help the development of wet-resistant adhesives.

Mussel adhesion – essential footwork

“…During thread formation, byssal proteins are secreted incrementally along a distal to proximal trajectory. Plaque proteins, beginning with those at the distal end between the foot-tip and substratum, are deposited first, followed by the bulk of the plaque and thread core components (Yu et al, 2011b;Petrone et al, 2015). Finally, just before the thread disengages from the groove, the assembled structure is coated by a ∼5-µm-thick cuticle from the accessory gland, whereupon the new thread is recruited into load-bearing service (Fig.…”

“…preCOLs are trimeric with supersecondary triple helical collagen cores flanked by silk-like β-sheets in preCOL-D, and disordered elastin in preCOL-P and preCOL-NG (Arnold et al, 2012). It is highly probable that a different structure is gained upon pH-induced precipitation, as for variants of Mfp-3 (Wei et al, 2013a;Mirshafian et al, 2016;Petrone et al, 2015), which gain β-sheet structure during titration from pH 3 to 7.5. …”

“…The initial sequence of protein deposition at the distal end around the plaque has been investigated by time-lapse mass spectrometry (Yu et al, 2011;Petrone et al, 2015). Following acidification of the distal depression, Mfp-3 variants, Mfp-5 and Mfp-6 are secreted within seconds of one another.…”

Modular peptides from the thermoplastic squid sucker ring teeth form amyloid-like cross-β supramolecular networks

“…[34] In spider silks, the pH in spinning duct where elongation flow occurs is also acidic, [30,31] and this tight control of pH eventually regulates the final aggregation and assembly of fibroins into silk fibers, [32,33] with β-sheets forming from the concentrated dope under precise conditions of pH and salt concentration. [30] We suggest a similar mechanism for SRT, whereby His-rich modules contribute to maintaining a high concentration of suckerins while preventing aggregation.…”

“…pHs were selected (4.0, 7.0 and 8.6) in order to specifically investigate the possible influence of the imidazole ring protonation of His side chains, as well as to mimic the pH environment of the growth and development of the SRT. Indeed, the pH is likely to increase incrementally from the specialized epithelial cells [30][31][32][33][34] which produce the SRT proteins (~ pH 4) to the confined extracellular interface at the base of the SRT, and finally to their final supramolecular self-assembly at the ocean's aquatic pH of about 8.3. The overall goal of the assay was to gain insights into which peptides are the most active in interacting with their counterparts at each pH condition.…”