PerspectiveBiological Adhesives

Positive charges and underwater adhesion

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Science  07 Aug 2015:
Vol. 349, Issue 6248, pp. 582-583
DOI: 10.1126/science.aac8174

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PHOTO: ANDREW FULLER

When visiting a beach, we can see that mussels, oysters, and barnacles attach themselves to rocks even while being pounded by waves. These organisms remain affixed by secreting adhesives. Human efforts to make such wet-setting glues are often foiled by the presence of water. Instructions on tubes of adhesives remind us that the surfaces must be clean and dry, given that our materials interact better with water than with the pieces of a broken dish. On page 628 of this issue, Maier et al. (1) have divulged a potentially key part of the underwater adhesion story. Mussels appear to gain surface access for glues by using their own protein-based ions to outcompete the ions in their saltwater environment.

When mussels identify an inviting location to settle down, they deposit a mixture of proteins that contains the rare amino acid 3,4-dihydroxyphenylalanine (Dopa). The catechol side chain of Dopa (i.e., 1,2-dihydroxybenzene) can bond onto rocky substrates via hydrogen bonding and metal chelation to provide surface adhesion (2, 3). Oxidation of Dopa to a semiquinone or a quinone initiates coupling chemistry to bring about covalent bonding for creating cohesion within the material. Iron bound by Dopa is needed for these processes, both in the adhesive plaques (4) and threads (5) of the animal's attachment assembly.

Other marine microorganisms such as bacteria also require iron to survive and have developed an approach for scavenging the needed metals from their surroundings. Siderophores are small molecules excreted into the water for capturing iron and pulling it back into the cells (6). These siderophores often rely upon catechol groups for binding iron. Although bacteria and mussels use their catechol chemistries for different purposes, Maier et al. have now made an intellectual bridge between these phenomena to gain insight into fundamental chemical processes that control underwater adhesion.

Sticking in the salty seas.

Mussels have devised clever strategies for binding to rocks. Catechol-containing adhesive proteins attach to anionic surfaces when in air or pure water. Maier et al. have found that in salt water, surface-bound cations deter access to proteins. To wipe the surface clean, mussel proteins contain their own cations for displacing salts. Catechols, and the animals, can then stick.

ILLUSTRATRION: ADAPTED FROM C. DEL GROSSO/PURDUE UNIVERSITY

Siderophores were used in experimental studies to represent macromolecular adhesive proteins. A surface forces apparatus measured the energies of pulling apart two mica surfaces on length scales of 1 to 5 nm. Of particular concern was the subset of mussel proteins known to reside at the interface between animal and rock. These proteins contain high levels of lysine and arginine that make them positively charged. Have mussels created a cationic glue for binding to anionic, inorganic surfaces? To find out, three classes of siderophore molecules were made that had only catechols, only cations, or both catechols and cations.

Adhesion energies in salt water were the highest when both catechols and positive charges were part of the molecule. Although siderophores bearing cations alone also showed attachment, the strength was only ∼15% of that when coupled to catechols. By themselves, catechols barely bonded at all. A surprise here is that the combination of catechols and cations yielded greater binding than the sum of the individual components. A type of synergy appears to be present when binding a surface submerged in sea water.

Having only catechols in the molecule and no cations resulted in appreciable bonding, but only when the environment was pure water, not salt water. On their own, catechols appear unable to drill through the barrier of hydrated cations associated atop anionic surfaces in the sea. Cations within the compounds studied here, and by extension in mussel adhesive proteins, seem to be present for the purpose of clearing surfaces of bound salts and making way for catechol adhesion.

Deciphering the detailed workings of biology is always captivating, especially when the insights influence how we design synthetic materials. Mussel proteins have been inspiring the development of several polymer systems with pendant catechol groups. These cutting-edge adhesives can sometimes bond more strongly than our favorite store-bought products such as Super Glue (7) and even function well under water (8).

Perhaps given the magnitude of the challenge, little has been reported on synthetic catechol adhesives for substrates submerged in sea water. In one example, a combination of catechols and positive charges did not increase binding, although the lysine groups may not have colocalized near the catechols within these hydrogels (9). Bulk adhesion in sea water has been studied with a polymeric adhesive containing catechols and varying amounts of ammonium cations (10). Bonding increased when cations were added into the polymer. However, incorporation of cations actually decreased adhesion when the substrates were in air rather than a salty environment. Such macroscopic results are consistent with—and now explained by—the molecular-level study of Maier et al.

The classic adhesive chemistries of acrylates, epoxies, and urethanes practically cower when facing waterlogged surfaces or environments. These recent insights may herald the availability of tailored adhesives for different wet environments. The hardware store may have one aisle for mussel-mimicking glues with both catechols and cations for when you need to bond parts in salt water. For gluing in pure water or air, visit the aisle with catechols but no added positive charges. Before we can buy such materials at the store, many questions remain. How much charge yields the best adhesion? Why are mussel proteins in the bulk of the adhesive, not just at the surface, also cationic? Even in pure water, how can catechols find a way past surface-associated waters to bind substrates? Finally, is the cationic adhesive strategy used by mussels a general theme throughout marine biology, or just one solution?

References and Notes

  1. Acknowledgments: Thanks to C. Del Grosso for help with the illustration. Support provided by NSF (grants CHE-0952928, DMR-1309787) and Office of Naval Research (grants N000141310245, N000141310327) is gratefully appreciated.

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