Science 374, 206–211 (2021)
Mussels produce byssus fibers to anchor themselves to surfaces in marine environments. Although the adhesive plaque at the end of this protein-based fiber was known to contain reinforcing crosslinks between metal ions and 3,4-dihydroxyphenylalanine (DOPA) residues, how metal is obtained and introduced during plaque formation has remained unknown. Using a combination of microscopy, micro-computed tomography and spectroscopy, Priemel et al. obtained a detailed visualization of the mussel secretory machinery and snapshots of the plaque-formation process. The mussel foot contains a network of longitudinal ducts (LDs) lined with cilia and surrounded by plaque gland cells, each dense with vesicles containing plaque proteins rich in DOPA and other aromatic amino acids. The area surrounding the LDs also contains metal storage particles (MSPs) that harbor iron and vanadium ions in complex with catechol-containing molecules. As plaque vesicles are secreted into the LD lumen and move from the proximal end toward the distal end, they progressively mix with secreted metal ions from the MSPs, forming crosslinks and transitioning to a solid phase as they proceed to the LD exit. The storage of metal ions in MSPs and their controlled secretion indicates that metal is actively added to the byssus fiber rather than being passively obtained from seawater, as had been previously suggested, and also explains how the mussel avoids premature crosslinking of the plaque. Insights from this study could inform the fabrication of new biologically inspired adhesives and other biomaterials.
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