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Abstract

Mussels produce an exceptional proteinaceous adhesive so they can withstand waves and currents. Metal ions bound to modified tyrosine residues play an important role in reinforcing the adhesive. Priemel et al. brought together a variety of spectroscopy and microscopy techniques to study the cellular mechanisms involved in adhesive fabrication in mussels (see the Perspective by Wilker). They found that metal ion–rich vesicles are secreted alongside vesicles containing the adhesive protein and mix in a microfluidic-like process within interconnected microchannels found in the lateral duct of the mussel foot to create porous, adhesive plaque filaments. —MAF Mussels mix metal ions with fluid proteins in secretory microchannels to fabricate a wet bioadhesive. To anchor in seashore habitats, mussels fabricate adhesive byssus fibers that are mechanically reinforced by protein-metal coordination mediated by 3,4-dihydroxyphenylalanine (DOPA). The mechanism by which metal ions are integrated during byssus formation remains unknown. In this study, we investigated the byssus formation process in the blue mussel, Mytilus edulis, combining traditional and advanced methods to identify how and when metals are incorporated. Mussels store iron and vanadium ions in intracellular metal storage particles (MSPs) complexed with previously unknown catechol-based biomolecules. During adhesive formation, stockpiled secretory vesicles containing concentrated fluid proteins are mixed with MSPs within a microfluidic-like network of interconnected channels where they coalesce, forming protein-metal bonds within the nascent byssus. These findings advance our understanding of metal use in biological materials with implications for next-generation metallopolymers and adhesives.