The Thiol-Rich Interlayer in the Shell/Core Architecture of Mussel Byssal Threads

Abstract

The mussel byssus thread is an extremely tough core-shelled fiber that dissipates substantial amounts of energy during tensile loading. The mechanical performance of the shell is critically reliant on 3,4-dihydroxyphenylalanine's (Dopa) ability to form reversible iron-catecholate complexes at pH 8. However, the formation of these coordinate cross-links is undercut by Dopa's oxidation to Dopa-quinone, a spontaneous process at seawater conditions. The large mechanical mismatch between the cuticle and the core lends itself to further complications. Despite these challenges, the mussel byssus thread performs its tethering function over long periods of time. Here, we address these two major questions: (1) how does the mussel slow/prevent oxidation in the cuticle, and (2) how is the mechanical mismatch at the core/ shell interface mitigated? By combining a number of microscopy and spectroscopy techniques we have discerned a previously undescribed layer. Our results indicate this interlayer is thiol rich and thus will be called the thiol-rich interlayer (TRL). We propose the TRL serves as a long-lasting redox reservoir as well as a mechanical barrier.

Compartmentalized processing of catechols during mussel byssus fabrication determines the destiny of DOPA

“…In contrast, DOPA in the cuticle remains reduced and available for metal binding even after storage for 2 wk under basic conditions that typically favor DOPA oxidation. This is likely related to the recently discovered Cys-rich proteins believed to be present in the cuticle, which are proposed to function as a multifunctional reducing agent (34,47,48).…”

“…This step is crucial for the adhesion of mfp-3 and mfp-5 as DOPA-catechol is a much more efficient adherent than DOPAquinone (16). Along these lines, a family of putative cysteine-rich proteins were recently identified in a transcriptome of the cuticle gland from a related species (Mytilus californianus) (mfp-16 to 19), one of which has been recently localized in the cuticle secretory vesicles via proteomics (48). Recent elemental analysis of the cuticle with energy dispersive X-ray spectroscopy (EDS) has also revealed a high sulfur content within the cuticle colocalized with the DOPA-containing protein mfp-1 (34).…”

Following the thread: Mytilus mussel byssus as an inspired multi-functional biomaterial

“…It is appropriate to emphasize that mussels have no monopoly on protein DOPA; it is widely distributed in the structural materials of animals including molluscan periostracum and shell matrix, trematode eggshells, polychaete cement, tunicate test proteins and selachian capsules [86][87][88][89] . Recent transcriptomic analysis of the accessory gland suggests that a number of cysteine-rich proteins may also be present in the cuticle 31 , with one -mfp-17 -confirmed to be in the cuticle secretory vesicles 90 .…”

Hydroxyapatite Adsorbed at the Surface of the Byssus Fibers of Pinna Nobilis

“…[6][7][8] Byssal threads from the Mytilus genus show a similar composition, even though the nal threads are not equivalent in their mechanical properties and are characterized by a core-shell structure. [9][10][11] In particular, Mytilus byssal threads have a core made of anisotropic bundles of collagen bers, whereas the shell, known as the cuticle, is a composite of granules dispersed in a continuous, the granules are mainly made of His/3,4-di-hydroxyphenylalanine (DOPA) protein, which, at pH 5−8, readily binds iron to form cross-linking bis-and tris-catecholate-iron complexes. 10,12 Furthermore, a third interlayer region intercalated between the cuticle and core rich in cysteine has been individuated.…”

“…10,12 Furthermore, a third interlayer region intercalated between the cuticle and core rich in cysteine has been individuated. 11 In general, for the Mytilus genus, every single ber consists of an elastic proximal section and a stiff distal section besides the adhesive plaque at their distal end. The proximal and distal sections are both made of pepsin-resistant protein complexes consisting of a collagen core domain, variable anking regions, and DOPA-rich regions.…”