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      Rapid self-assembly of complex biomolecular architectures during mussel byssus biofabrication

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          Abstract

          Protein-based biogenic materials provide important inspiration for the development of high-performance polymers. The fibrous mussel byssus, for instance, exhibits exceptional wet adhesion, abrasion resistance, toughness and self-healing capacity–properties that arise from an intricate hierarchical organization formed in minutes from a fluid secretion of over 10 different protein precursors. However, a poor understanding of this dynamic biofabrication process has hindered effective translation of byssus design principles into synthetic materials. Here, we explore mussel byssus assembly in Mytilus edulis using a synergistic combination of histological staining and confocal Raman microspectroscopy, enabling in situ tracking of specific proteins during induced thread formation from soluble precursors to solid fibres. Our findings reveal critical insights into this complex biological manufacturing process, showing that protein precursors spontaneously self-assemble into complex architectures, while maturation proceeds in subsequent regulated steps. Beyond their biological importance, these findings may guide development of advanced materials with biomedical and industrial relevance.

          Abstract

          Mussels attach to rocks using a byssus, which possesses unique properties of adhesion, toughness and self-healing. Here, the authors explore the fabrication process of mussel byssus demonstrating the self-assembly of specific proteins into multi-scale organized structures using artificially induced byssus threads.

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          Most cited references64

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          Iron-clad fibers: a metal-based biological strategy for hard flexible coatings.

          The extensible byssal threads of marine mussels are shielded from abrasion in wave-swept habitats by an outer cuticle that is largely proteinaceous and approximately fivefold harder than the thread core. Threads from several species exhibit granular cuticles containing a protein that is rich in the catecholic amino acid 3,4-dihydroxyphenylalanine (dopa) as well as inorganic ions, notably Fe3+. Granular cuticles exhibit a remarkable combination of high hardness and high extensibility. We explored byssus cuticle chemistry by means of in situ resonance Raman spectroscopy and demonstrated that the cuticle is a polymeric scaffold stabilized by catecholato-iron chelate complexes having an unusual clustered distribution. Consistent with byssal cuticle chemistry and mechanics, we present a model in which dense cross-linking in the granules provides hardness, whereas the less cross-linked matrix provides extensibility.
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            Underwater contact adhesion and microarchitecture in polyelectrolyte complexes actuated by solvent exchange

            Polyelectrolyte complexation is critical to the formation and properties of many biological and polymeric materials, and is typically initiated by aqueous mixing followed by fluid-fluid phase separation, such as coacervation. Yet little to nothing is known about how coacervates evolve into intricate solid microarchitectures. Inspired by the chemical features of the cement proteins of the sandcastle worm, here we report a versatile and strong wet-contact microporous adhesive resulting from polyelectrolyte complexation triggered by solvent exchange. After premixing a catechol-functionalized weak polyanion with a polycation in dimethyl sulphoxide (DMSO), the solution was applied underwater to various substrates whereupon electrostatic complexation, phase inversion, and rapid setting were simultaneously actuated by water-DMSO solvent exchange. Spatial and temporal coordination of complexation, inversion and setting fostered rapid (∼25 s) and robust underwater contact adhesion (Wad ≥ 2 J m(-2)) of complexed catecholic polyelectrolytes to all tested surfaces including plastics, glasses, metals and biological materials.
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              Mussel protein adhesion depends on thiol-mediated redox modulation

              Mussel adhesion is mediated by foot proteins (mfp) rich in a catecholic amino acid, 3, 4-dihydroxyphenylalanine (dopa), capable of forming strong bidentate interactions with a variety of surfaces. A facile tendency toward auto-oxidation, however, often renders dopa unreliable for adhesion. Mussels limit dopa oxidation during adhesive plaque formation by imposing an acidic, reducing regime based on thiol-rich mfp-6, which restores dopa by coupling the oxidation of thiols to dopaquinone reduction.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                06 March 2017
                2017
                : 8
                : 14539
                Affiliations
                [1 ]Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Research Campus Golm , 14424 Potsdam, Germany
                Author notes
                [*]

                These authors contributed equally to this work.

                Article
                ncomms14539
                10.1038/ncomms14539
                5343498
                28262668
                752e80b2-04d3-4742-bed8-74b24989d742
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 19 August 2016
                : 06 January 2017
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