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      Involvement of sulfated biopolymers in adhesive secretions produced by marine invertebrates

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          ABSTRACT

          Many marine invertebrates use adhesive secretions to attach to underwater surfaces and functional groups borne by their adhesive proteins and carbohydrates, such as catechols and phosphates, play a key role in adhesion. The occurrence of sulfates as recurrent moieties in marine bioadhesives suggests that they could also be involved. However, in most cases, their presence in the adhesive material remains speculative. We investigated the presence of sulfated biopolymers in five marine invertebrates representative of the four types of adhesion encountered in the sea: mussels and tubeworms for permanent adhesion, limpets for transitory adhesion, sea stars for temporary adhesion and sea cucumbers for instantaneous adhesion. The dry adhesive material of mussels, sea stars and sea cucumbers contained about 1% of sulfate. Using anti-sulfotyrosine antibodies and Alcian Blue staining, sulfated proteins and sulfated proteoglycans and/or polysaccharides were identified in the secretory cells and adhesive secretions of all species except the tubeworm. Sulfated proteoglycans appear to play a role only in the non-permanent adhesion of sea stars and limpets in which they could mediate cohesion within the adhesive material. In mussels and sea cucumbers, sulfated biopolymers would rather have an anti-adhesive function, precluding self-adhesion.

          Abstract

          Summary: Sulfate groups borne by adhesive macromolecules play a role in attachment to underwater surfaces in marine invertebrates using non-permanent adhesion, but not in those using permanent or instantaneous adhesion.

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          Most cited references62

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          BIOLOGICAL ADHESIVES. Adaptive synergy between catechol and lysine promotes wet adhesion by surface salt displacement.

          In physiological fluids and seawater, adhesion of synthetic polymers to solid surfaces is severely limited by high salt, pH, and hydration, yet these conditions have not deterred the evolution of effective adhesion by mussels. Mussel foot proteins provide insights about adhesive adaptations: Notably, the abundance and proximity of catecholic Dopa (3,4-dihydroxyphenylalanine) and lysine residues hint at a synergistic interplay in adhesion. Certain siderophores—bacterial iron chelators—consist of paired catechol and lysine functionalities, thereby providing a convenient experimental platform to explore molecular synergies in bioadhesion. These siderophores and synthetic analogs exhibit robust adhesion energies (E(ad) ≥-15 millijoules per square meter) to mica in saline pH 3.5 to 7.5 and resist oxidation. The adjacent catechol-lysine placement provides a "one-two punch," whereby lysine evicts hydrated cations from the mineral surface, allowing catechol binding to underlying oxides.
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            Mussel adhesion - essential footwork.

            Robust adhesion to wet, salt-encrusted, corroded and slimy surfaces has been an essential adaptation in the life histories of sessile marine organisms for hundreds of millions of years, but it remains a major impasse for technology. Mussel adhesion has served as one of many model systems providing a fundamental understanding of what is required for attachment to wet surfaces. Most polymer engineers have focused on the use of 3,4-dihydroxyphenyl-l-alanine (Dopa), a peculiar but abundant catecholic amino acid in mussel adhesive proteins. The premise of this Review is that although Dopa does have the potential for diverse cohesive and adhesive interactions, these will be difficult to achieve in synthetic homologs without a deeper knowledge of mussel biology; that is, how, at different length and time scales, mussels regulate the reactivity of their adhesive proteins. To deposit adhesive proteins onto target surfaces, the mussel foot creates an insulated reaction chamber with extreme reaction conditions such as low pH, low ionic strength and high reducing poise. These conditions enable adhesive proteins to undergo controlled fluid-fluid phase separation, surface adsorption and spreading, microstructure formation and, finally, solidification.
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              Understanding Marine Mussel Adhesion

              In addition to identifying the proteins that have a role in underwater adhesion by marine mussels, research efforts have focused on identifying the genes responsible for the adhesive proteins, environmental factors that may influence protein production, and strategies for producing natural adhesives similar to the native mussel adhesive proteins. The production-scale availability of recombinant mussel adhesive proteins will enable researchers to formulate adhesives that are water-impervious and ecologically safe and can bind materials ranging from glass, plastics, metals, and wood to materials, such as bone or teeth, biological organisms, and other chemicals or molecules. Unfortunately, as of yet scientists have been unable to duplicate the processes that marine mussels use to create adhesive structures. This study provides a background on adhesive proteins identified in the blue mussel, Mytilus edulis, and introduces our research interests and discusses the future for continued research related to mussel adhesion.
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                Author and article information

                Journal
                Biol Open
                Biol Open
                BIO
                biolopen
                Biology Open
                The Company of Biologists Ltd
                2046-6390
                15 November 2018
                20 September 2018
                20 September 2018
                : 7
                : 11
                : bio037358
                Affiliations
                [1 ]Cell Biology Unit, Research Institute for Biosciences, University of Mons , 23 Place du Parc, 7000 Mons, Belgium
                [2 ]Biology of Marine Organisms and Biomimetics Unit, Research Institute for Biosciences, University of Mons , 23 Place du Parc, 7000 Mons, Belgium
                Author notes
                [* ]Author for correspondence ( Patrick.Flammang@ 123456umons.ac.be )
                Author information
                http://orcid.org/0000-0001-9938-1154
                Article
                BIO037358
                10.1242/bio.037358
                6262867
                30237291
                f235e5df-fc4e-4c61-9e3e-65222d24cc2c
                © 2018. Published by The Company of Biologists Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 26 July 2018
                : 6 September 2018
                Funding
                Funded by: the Fund for Scientific Research of Belgium;
                Funded by: COST Action European Network of Bioadhesion Expertise;
                Award ID: CA15216
                Categories
                Research Article

                Life sciences
                sulfate,marine adhesion,mussel,tubeworm,sea star,limpet,sea cucumber
                Life sciences
                sulfate, marine adhesion, mussel, tubeworm, sea star, limpet, sea cucumber

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