High Strength Underwater Bonding with Polymer Mimics of Mussel

Feb 8, 2017 - When it comes to underwater adhesion, shellfish are the true experts. Mussels, barnacles, and oysters attach to rocks with apparent ease...
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High Strength Underwater Bonding with Polymer Mimics of Mussel Adhesive Proteins Michael A. North,† Chelsey A. Del Grosso,† and Jonathan J. Wilker*,†,‡ †

Department of Chemistry, Purdue University, 560 Oval Drive, West Lafayette, Indiana 47907-2084, United States School of Materials Engineering, Purdue University, 701 West Stadium Avenue, West Lafayette, Indiana 47907-2045, United States

‡

S Supporting Information *

ABSTRACT: When it comes to underwater adhesion, shellfish are the true experts. Mussels, barnacles, and oysters attach to rocks with apparent ease. Yet our man-made glues often fail when trying to stick in wet environments. Results described herein focus on a copolymer mimic of mussel adhesive proteins, poly(catechol-styrene). Underwater bonding was examined as a function of parameters including polymer molecular weight and composition. In doing so, several surprising results emerged. Poly(catechol-styrene) may be the strongest underwater adhesive found to date. Bonding even exceeded that of the reference biological system, live mussels. Adhesion was also found to be stronger under salt water than deionized water. Such unexpected findings may contradict an earlier proposal in which charged amino acids were suggested to be key for mussel adhesive function. Taken together, these discoveries are helping us to both understand biological adhesion as well as develop new materials with properties not accessed previously. KEYWORDS: adhesive, biomimetic, mussel, polymers, underwater

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INTRODUCTION Underwater adhesion presents several technical challenges.1 When applied to submerged substrates, glues interact with water instead of forming adhesive bonds atop the surface or cohesive bonds within the bulk. Although man-made adhesives do not work well underwater, nature has been addressing such design constraints for eons. A trip to the beach will show rocks covered by organisms including oysters, barnacles, sea grasses, and tube worms, each sticking with adhesives.1−3 The common blue mussel (Mytilus edulis) has gained a measure of fame by being the role model for our understanding of wet bonding (Figure 1).1−3 This shellfish attaches upon depositing a mixture of proteins containing an atypical amino acid, 3,4-dihydroxyphenylalanine (DOPA) (Figure 1).1−4 Cross-linking of these proteins generates cured glue. Despite such insights, we still do not understand how this system can work so well in an environment that tends to be particularly harsh toward adhesion. Furthermore, we have not yet been able to take what we have learned from biology and transition this knowledge into fully functioning biomimetic materials.5 In recent years, there has been a blossoming of material systems that mimic various aspects of mussel adhesive proteins.1−3,6−9 Quite often, synthetic polymers are used to substitute for the protein backbone and derivatives of catechol are appended to these chains for providing the cross-linking and adhesion chemistry of DOPA (Figure 1).7,8,10−22 Notable findings have included hydrogels being developed with selfhealing properties.23 In terms of adhesion, dry bonding strengths of mussel mimicking polymers have been able to exceed those of long established commercial products including © 2017 American Chemical Society

Figure 1. Underwater bonding of a marine mussel and poly(catecholstyrene). The structures of 3,4-dihydroxyphenylalanine (DOPA) in a protein and poly[(3,4-dimethoxystyrene)-co-(styrene)] are shown. The mussel is attached to a piece of aluminum. The polymer is forming a lap shear joint between two aluminum substrates. Catecholcontaining components are highlighted in yellow.

Super Glue.20 Despite these advances, we are still lacking high strength bonding with synthetic materials when used underwater. We have also not developed much context for the performance of biomimetic materials in comparison to the biological counterparts. In work described here, a polymer Received: January 9, 2017 Accepted: February 8, 2017 Published: February 8, 2017 7866

DOI: 10.1021/acsami.7b00270 ACS Appl. Mater. Interfaces 2017, 9, 7866−7872

Research Article

ACS Applied Materials & Interfaces

Figure 2. Polymer influences upon underwater bonding. (a) Adhesion as a function of molecular weight for poly(catechol-styrene). (b) Changes in adhesion with varying catechol content of the polymers. Data are reported with mean values ± 90% confidence intervals.

spectra and gel permeation chromatograms are provided in the SI section (Figures S1 and S2). To test underwater bonding, polished aluminum substrates were submerged into a tank of artificial seawater (Figure 1). Poly(catechol-styrene) was dissolved into chloroform and the solution deposited onto a substrate. The choice of chloroform was dictated by needing a solvent denser than water such that the adhesive formulation did not float up and off the substrate. Initial studies with acetone solvent, being miscible with water, brought about rapid precipitation and no surface bonding of the water insoluble polymer. Hydrophobic solvents such as chloroform are unable to dry a submerged surface.9,28−30 Waters remain bound to high energy surfaces even when covered by hydrophobic liquids or after movement to ambient environments.9,28−30 In other words, surface-bound waters are almost always present, creating a barrier to adhesive materials from making beneficial contacts. Furthermore, delivering polymers to surfaces in hydrophobic solvents is not a means of displacing these waters and fostering bonding. If achieving underwater bonding was a simple matter of placing polymers into hydrophobic solvents, then several commercial products would likely already have demonstrated suitable performance. After deposition of the polymer solution onto one substrate, a second piece of aluminum was then placed atop the first to create a lap shear joint. Addition of a weight held the substrates together during a cure period, the assembly was removed from the tank, and then pulled apart immediately by a materials testing system to quantify bonding. Maximum force at failure was divided by substrate overlap area to provide adhesion values (in MPa). In all cases examined here bond failure was of a cohesive nature. Figure S3 shows that, after testing, there was polymer distributed evenly across both substrates. During mechanical testing, all bonds failed in a brittle fashion, indicating drying and insignificant amounts of solvent persisting within the bond. Data in Figure 2a show how adhesion changed as a function of molecular weight. Performance appeared to have peaked at ∼85 000 g/mol. To determine statistical differences in the mean values of adhesion for poly(catechol-styrene) as a function of molecular weight, data were examined by an analysis of variance (ANOVA). Post hoc comparisons were performed using Tukey’s honest significant difference (HSD) test. The null hypothesis, that there is no difference in adhesion

system is shown to bond underwater with high strengths in bulk applications. Several aspects of polymer design were explored and, in the end, underwater bonding exceeded that achievable by the animals after which this material was modeled. In many regards, the findings are surprising and serve to influence our understanding of the important chemical features used by biological adhesives.

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RESULTS AND DISCUSSION Polymer Design. Prior studies have shown that the random copolymer poly[(3,4-dihydroxystyrene)-co-styrene] (“poly(catechol-styrene)”) is a useful mimic of mussel adhesive proteins in terms of dry bonding performance (Figure 1).13,20 Catechol groups pendant from a polystyrene host can represent, respectively, DOPA distributed throughout the polypeptide chains of mussel adhesive proteins.13,20 The copolymers were synthesized on gram scales, thereby enabling bulk adhesion testing. Dry bonding of the polymer was appreciable, well into the Megapascal (MPa) range for lap shear joints between metal, plastic, and wood substrates.13,20 How well might the dry bonding of this biomimetic system transfer to underwater applications? In terms of polymer composition and molecular weight, which derivatives should bring about the highest underwater bonding performance? Looking at the proteins found in a mussel’s adhesive plaque does not provide too much help with regard to design. The DOPA content can range from 3% to 30% of all amino acids.24 Molecular weights are as low as 6000 and as high as 110 000 g/mol.25 Adhesion Studies. In order to explore underwater adhesion, a logical starting point was a polymer of ∼33% 3,4dihydroxystyrene and ∼67% styrene, given prior data on this poly[(3,4-dihydroxystyrene)33%-co-(styrene)67%] composition yielding maximum dry adhesion.13 Molecular weight can have a major impact upon adhesion, with shorter chains providing surface wetting, yet longer molecules being best at bringing about polymer−polymer interactions for cohesion.16,26,27 Poly(catechol-styrene) of several different molecular weights was made here by changing the ratio of n-butyl lithium polymerization initiator to monomers in the reaction feed (Table S1 of the Supporting Information, SI). The catechol content of these polymers was held between 27% and 33% (Table S1). Representative proton nuclear magnetic resonance 7867

DOI: 10.1021/acsami.7b00270 ACS Appl. Mater. Interfaces 2017, 9, 7866−7872

Research Article

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styrene) giving rise to optimal performance with dry versus underwater conditions can be explained by lower molecular weight species providing enhanced ability to wet surfaces over higher molecular weight analogs. Lower catechol content decreases cohesive cross-linking. These findings tell us that increasing surface bonding at the expense of bulk cohesion is an important design aspect of creating underwater adhesives. Benchmarking Performance. Making comparisons between adhesion data is often difficult, given variations in several parameters including substrate choice, cure conditions, joint type, and testing methods. However, we can gain some context for how poly(catechol-styrene) compares to prior efforts. Bulk lap shear joints between aluminum substrates with charged catechol containing polymers have been reported at 0.35 MPa for polyoxetanes in humid conditions with partial drying.15 When in a coacervate phase of a polyanion condensed with Ca2+ cations, strengths up to 1.2 MPa were found.14 Neutral catechol-containing polyvinylpyrrolidone applied to wetted glass and then cured underwater was at 1.3 MPa17 and a polyacrylate between wet glass bonded at 1.6 MPa.35 Beyond mussel mimicking systems is a metal complex guest and macrocycle host, each surface grafted onto silicon, yielding up to 1.1 MPa underwater.36 A light cured bisphenol-acrylate adhered aluminum underwater at 1.2 MPa.37 Improvements in bulk adhesive performance are typically gradual, with a factor of 2X enhancement being quite significant. With strengths up to ∼3 MPa in this current study, bulk underwater adhesion with poly(catechol-styrene) was appreciable. In order to have benchmarks for direct comparisons, bonding was carried out with a range of commercial glues including common adhesives and specialty materials billed for wet applications. All glues were applied underwater with constant conditions including quantity of adhesive, cure time, cure temperature, and substrate type. Figure 3 provides data

strength with changes to polymer molecular weights, was rejected at a confidence level of 95% (P < 0.05). ANOVA showed statistical differences (P < 0.05) between mean adhesion of poly(catechol-styrene) at varying molecular weights. Statistical results from Tukey’s HSD test indicated that mean adhesion of polymers with molecular weights of ∼85 000 g/mol were significantly different from those of 30 000 g/mol and below. These results suggest that adhesive performance increased with higher polymer molecular weights. Additionally, post hoc comparisons show that mean adhesion of polymers of 94 000 and 96 000 g/mol were not statistically different (P > 0.05) from polymers of lower molecular weights (30 000 g/mol and below). Performance may have begun to drop and an optimal balance between surface adhesive and bulk cohesive forces occurred at ∼85 000 g/mol. Analogous data for dry bonding differed somewhat, with no obvious peak and increasing molecular weights correlating to higher adhesion even over 100 000 g/mol.16 Joining two substrates requires both surface adhesive bonding as well as cohesive interactions within the bulk of the material. If one interaction, be it adhesive or cohesive, becomes too prominent, the other suffers and overall performance will decline. The degree of cross-linking is quite relevant to this adhesive-cohesive balance. Oxidized catechols (i.e., semiquinone or quinone) bring about cross-linking to generate cohesive bonds within the material.10,31 However, it is the reduced form of the DOPA catechol ring that is responsible for surface adhesive contacts.3 With too much oxidative crosslinking comes greater cohesion, diminished surface adhesion, and overall a weaker glue. Consequently, the amount of catechol within the polymer will influence overall performance. Figure 2b presents a study in which several poly(catecholstyrene) derivatives were made, each with differing amounts of the catechol-containing 3,4-dihydroxystrene monomer (Table S2). Polymer molecular weights were maintained at 75 000− 101 000 g/mol in keeping with the results from Figure 2a for optimal bonding. Maximum underwater adhesion was found with a polymer of ∼22% 3,4-dihydroxystyrene and ∼78% styrene (Figure 2b). Here, too, results for underwater bonding differed somewhat versus dry conditions, which maximized at ∼33% 3,4-dihydroxystyrene and ∼67% styrene.13 These results show that, once the polymer exceeds ∼22% 3,4-dihydroxystyrene content, this excess catechol may be available to provide enhanced cross-linking and cohesion at the expense of surface binding. Overall, such a scenario leads to a decrease of adhesion. The exact mechanism of adhesion in DOPA proteins and catechol-containing polymers is not clear. There are several interactions possible including hydrogen bonding, metal chelation, and covalent cross-linking brought about by oxidation reactions.2,3,10,31,32 Although no oxidizing agents were added in the study here, after curing under salt water, the final polymers were seen to be darker than prior to use (Figure S3). Such darkening is typical when catechol compounds oxidize, cross-link, and generate conjugated organics. The polymers were delivered in an organic solvent, which then dissipated, potentially providing exposure to water at a pH able to deprotonate the catechols and begin oxidative cross-linking. Low molecular weight species are best at wetting to create surface adhesion.26,33,34 High molecular weight polymers provide cohesion via chain entanglements.26,33,34 In the case of underwater adhesion, it may be surface bonding that is the most difficult to achieve. Different derivatives of poly(catechol-

Figure 3. Underwater bonding of poly(catechol-styrene) compared to commercial products. Lap shear joints were between polished aluminum substrates.

indicating that poly(catechol-styrene) outperformed every product tested, usually by quite large margins. Standard adhesives such as Elmer’s Glue-All (polyvinyl acetate) and Super Glue (ethyl cyanoacrylate) failed to bond at even modest levels, likely a result of not being able to cure underwater or the water inducing curing too rapidly to allow interaction with the substrates, respectively. We now have what appears to be the strongest underwater adhesive reported to date. For providing a broader context of underwater bonding capability, poly(catechol-styrene) adhesion on a range of different substrates was compared to some of the strongest 7868

DOI: 10.1021/acsami.7b00270 ACS Appl. Mater. Interfaces 2017, 9, 7866−7872

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Figure 4. Comparing the adhesion of live mussels and a biomimetic system. (a) Mussels seen depositing adhesive plaques onto the side of an aquarium tank as well as upon each other. (b) Testing the adhesion strength of mussel adhesive. The inset shows how grips pull up on the thread while the adhesive plaque is bound to the substrate. (c) Aluminum rods held underwater and bonded together in a tensile joint with poly(catecholstyrene). (d) Measuring adhesion after an underwater cure. The substrates were first underwater, poly(catechol-styrene) was applied, both substrates were joined together, and the assembly cured for 72 h. The joint was then removed from the water for immediate testing.

large quantities of quite consistent data.38 Specific to this current study, we needed a means of obtaining direct comparisons between adhesion of mussel plaques and synthetic polymers. Tensile pulling at 90° was thus best to use in both cases. Average mussel adhesion in this tensile mode was 0.13 ± 0.01 MPa. For a direct comparison, polished aluminum rods were held under salt water and then bonded together into tensile joints using poly(catechol-styrene) (Figure 4c). The rods were pulled apart (Figure 4d) to reveal bonding at 2.2 ± 0.9 MPa, a 17-fold increase over the animal’s adhesion. Synthetic systems can mimic nature, but seldom outperform biological materials. Despite a large degree of effort, biomimetic properties similar to, for example, sea shells, bone, or wood have not yet been achieved.5 Our work described here has been aimed at creating the strongest underwater glue possible. A living mussel, by contrast, need only attach strongly enough to deter the forces exerted by waves and predators. Perhaps such differences in end goals can, at least partially, explain how poly(catechol-styrene) outperformed mussel adhesive. Role of Charges. Several recent reports have been contributing to our understanding of how mussels bond to rocks so well. Catechols may have a special ability to penetrate through surface-bound waters for enabling wet attachment. Having two adjacent alcohol groups might allow for

commercial glues from Figure 3. Table S3 shows that these selected commercial products performed best with polyvinyl chloride (PVC), etched aluminum, and sanded steel substrates. On polytetrafluoroethylene (Teflon), wood (red oak), and polished aluminum, poly(catechol-styrene) displayed the highest adhesion. With Teflon, only the biomimetic polymer and a single commercial product provided any bonding at all. For wood, poly(catechol-styrene) was the single system capable of creating a measurable bond underwater. Given that the commercial glues have been around for up to decades, we are excited to report superior performance for a relatively young system. Live Animal Adhesive. A new material that can, at times, outperform established products is quite exciting.5 Perhaps even more daunting is direct comparison of a biomimetic system against the true biological counterpart. Live mussels (Figure 4a) were placed atop sheets of polished aluminum for deposition of their adhesive. Using an established method (Figure 4b) and several animals, adhesive plaques were pulled up from the surfaces until failure.38 Mussel plaques and threads are deposited at several angles relative to the surface (Figure 4a). A custom built system has been used by others with success to pull threads and plaques from surfaces at the same angles used by the animals.39 Practically speaking, we find that pulling up the plaque and thread 90° from the surface provides 7869

DOI: 10.1021/acsami.7b00270 ACS Appl. Mater. Interfaces 2017, 9, 7866−7872

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ACS Applied Materials & Interfaces cooperative binding, analogous to an entropic “chelate effect.”40 Hydrogen bonding and metal chelation at the substrate appear likely to be contributing surface adhesion.40 Oxidative crosslinking generates cohesive forces.2,31,32 Cationic charges within mussel adhesive proteins have been proposed recently to aid this bonding in salt water.18,41 Positively charged amino acids could help outcompete surface-bound cations such as sodium, thereby allowing proteins to gain access onto mildly anionic surfaces including rocks.18,41 In order to address potential roles for charges11,18,42 and salts,11,17−19,37,41 we examined the bonding of poly[(3,4dihydroxystyrene)28%-co-(styrene)72%] (Mw = 95 000 g/mol) in deionized water (pH = 7.9) and found a value of 0.4 ± 0.1 MPa. When the same experiment was carried out under artificial seawater (pH = 7.9), adhesion was at 1.8 ± 0.2 MPa. The polymer used for this experiment was from the same synthesis as that used in the molecular weight study (Figure 2a), thus identical adhesion values are reported. However, another polymer with similar catechol content in Figure 2b gave rise to different adhesion owing to a lower molecular weight. Poly(catechol-styrene) is a neutral polymer and we might expect improved adhesion under deionized versus salt water. This unexpected finding could be a function of the current study using a bulk, macroscopic adhesion method versus prior efforts examining interactions of small molecules on the nanometer scale.18 Nonetheless, such data indicate that charged molecules disrupting ions atop submerged surfaces may not be of primary importance for adhesion in the seas.

After being allowed to settle, the excess hydrochloric acid was decanted. This procedure was repeated 3 times. The solid was dissolved into dichloromethane and acetone then dried via rotary evaporator. The final white solid was placed under vacuum overnight. Polymer Characterization. Polymers were characterized primarily with proton nuclear magnetic resonance (1H NMR) spectroscopy and gel permeation chromatography (GPC). The 1H NMR spectra were recorded on a Varian Inova-300 MHz spectrometer and provided compositions. Gel permeation chromatography was performed in THF mobile phase on a Polymer Laboratories PLC-GPC20 to yield molecular weights (Mn and Mw) and dispersities (i.e., Đ, polydispersity indices, PDI’s). Water Preparation. Artificial seawater was prepared using Marine Environment dual phase formula and reverse osmosis water to a final salinity of 35 g/L. Deionized water was prepared using a Barnstead Nanopure Infinity Ultrapure water system with a final resistivity of 18 MΩ. All water was prepared immediately prior to use. Deionized water was at pH = 8.0 directly from the purifier and at pH = 7.9 after 24 h. The salt water was pH = 7.9 at both the beginning and end of the 24 h experimental periods. Lap Shear Adhesion Testing. Lap shear adhesive bonding was carried out with a modified version13 of the ASTM D1002 standard method.43 Derivatives of poly[(3,4-dihydroxystyrene)-co-(styrene)] were dissolved at 0.3 g/mL in chloroform with 45 μL dispensed onto each completely submerged substrate. An additional 15 μL of chloroform was then deposited. Another substrate was placed on top of the first to form a lap shear joint of 1.2 × 1.2 cm2. The bonds were cured at room temperature for 24 h, completely submerged. Samples were then removed from the water and measured immediately on an Instron 5544 materials testing system. Measurements used a 2000 N load cell and a crosshead speed of 2 mm/min. The maximum force at joint failure divided by the overlap area provided the adhesion strength. Each sample was tested a minimum of 5 times and averaged. The molecular weight and catechol percent graphs of Figure 2 show averages of 10 samples. Error bars indicate 90% confidence intervals. Preparation of Substrates. Substrates were fabricated by methods described previously.13,20 Briefly, aluminum, type 6061 T6, was purchased and prepared either by mirror polishing with Mibro no. 3 and Mibro no. 5. polish or an ASTM D2651-01 method for adherend cleaning (etching).44 Red oak was purchased locally and had a surface roughness equivalent to that of treatment with 220 grit sandpaper. Steel adherends were sanded with 50 grit sandpaper prior to testing and then washed with ethanol, acetone, and hexanes. Teflon (PTFE) and PVC were obtained from Rideout Plastics. Testing of Commercial Adhesives. Eleven different commercial glues were tested underwater using similar conditions to poly[(3,4dihydroxystyrene)-co-(styrene)]. Each product was measured 5 times using a mass of 13.5 mg to match the mass of poly[(3,4dihydroxystyrene)-co-(styrene)] in each trial (0.3 g/mL and 45 μL). Drying experiments noted no significant loss of mass or solvent from any of the commercial glues. Samples were cured for 24 h while underwater and then tested immediately. Animal Handling. Blue mussels (Mytilus edulis) were maintained in an aquarium system described previously,38 with growth conditions of 4 °C, 35 g/L salinity, and constant aeration. Each mussel was held in place with a rubber band on one 10 × 10 cm2 polished aluminum panel. The adhesive plaques of nine adult mussels were examined. All mussels were deemed to be healthy during these experiments. One indication of viability is that the animals close their gaping shells immediately upon tapping them. Another sign is a high number of adhesive plaques formed when the animals are placed upon a new substrate. The mussels used here passed both tests well. Live Mussel Adhesion Data Collection. Removal force was collected on an Instron 5544 materials testing system. Adhesion testing was carried out 3 days after placement of mussels and panels into the aquarium. Three separate trials were conducted whereby a total of 9 animals were examined to yield 48 plaques. Adhesion measurements were all averaged per animal. These average values per animal were then averaged to get an overall mean adhesion

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CONCLUSIONS Results presented here show that man-made materials can, indeed, bring about quite significant underwater adhesion. In a rare instance of biomimetics, this synthetic system outperformed the reference biological counterpart. These findings are helping to reveal which aspects of mussel adhesion are most important when managing attachment within their wet and salty environment. All that is needed for high strength bonding underwater appears to be a catechol-containing polymer. Charged groups and other features specific to proteins might be providing secondary functional aspects. Catechol groups may have a special ability for “drilling down” through surface waters in order to bind substrates.

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EXPERIMENTAL SECTION

Polymer Synthesis. The poly[(3,4-dimethoxystyrene)-co-(styrene)] precursor copolymers were synthesized using a prior method.13 Briefly, styrene, 3,4-dimethoxystyrene, and toluene were combined in a flame-dried Schlenk flask. The flask was then cooled in a dry ice/ isopropanol bath. After 10 min, n-butyl lithium was added to initiate polymerization. The reaction mixture was kept on dry ice for 8 h and then allowed to warm up to room temperature gradually. After 24 h of total time, the reaction was quenched and the polymer precipitated by addition of methanol. The polymer was redissolved into chloroform and then reprecipitated with methanol. This purification procedure was repeated three times. The polymer was dried via rotary evaporator and placed under vacuum overnight. Polymer Deprotection. Poly[(3,4-dimethoxystyrene)-co-(styrene)] was converted to poly[(3,4-dihydroxystyrene)-co-(styrene)] by dissolving the former into dichloromethane in a flame-dried Schlenk flask.13 The flask was placed into an ice bath for 10 min after which boron tribromide was added. This reaction proceeded overnight, was quenched with methanol, and allowed to stir for 15 min. The mixture was then poured into 1% hydrochloric acid and stirred for 15 min. 7870

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ACS Applied Materials & Interfaces measurement. This method minimizes the effect of one shellfish biasing data too much by providing a different number of plaques as well as particularly weak or strong bonding. Tensile Adhesion Testing of Polymers. Polished aluminum rods of 1.5 cm diameter were completely submerged underwater. Poly[(3,4-dihydroxystyrene)-co-(styrene)], 45 μL at 0.3 g/mL in chloroform, was applied to one adherend and overlapped with the second rod. These joint assemblies cured for 3 days underwater in order to mimic conditions of the live mussel testing. Samples were then removed from the water and measured immediately on an Instron 5544 materials testing system. Measurements used a 2000 N load cell and a crosshead speed of 2 mm/min. The maximum force at joint failure divided by the overlap area provided the adhesion strength. Ten samples were measured and averaged. The error provided is a 90% confidence interval.

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(9) Wei, W.; Petrone, L.; Tan, Y.; Cai, H.; Israelachvili, J. N.; Miserez, A.; Waite, J. H. An Underwater Surface-Drying Peptide Inspired by a Mussel Adhesive Protein. Adv. Funct. Mater. 2016, 26, 3496−3507. (10) Faure, E.; Falentin-Daudré, C.; Jérôme, C.; Lyskawa, J.; Fournier, D.; Woisel, P.; Detrembleur, C. Catechols as Versatile Platforms in Polymer Chemistry. Prog. Polym. Sci. 2013, 38, 236−270. (11) White, J. D.; Wilker, J. J. Underwater Bonding with Charged Polymer Mimics of Marine Mussel Adhesive Proteins. Macromolecules 2011, 44, 5085−5088. (12) Glass, P.; Chung, H. Y.; Washburn, N. R. Enhanced Reversible Adhesion of Dopamine Methacrylamide-Coated Elastomer Microfibrillar Structures under Wet Conditions. Langmuir 2009, 25, 6607− 6612. (13) Matos-Pérez, C. R.; White, J. D.; Wilker, J. J. Polymer Composition and Substrate Influences on the Adhesive Bonding of a Biomimetic, Cross-Linking Polymer. J. Am. Chem. Soc. 2012, 134, 9498−9505. (14) Kaur, S.; Weerasekare, G. M.; Stewart, R. J. Multiphase Adhesive Coacervates Inspired by the Sandcastle Worm. ACS Appl. Mater. Interfaces 2011, 3 (4), 941−944. (15) Li, A.; Jia, M.; Mu, Y.; Jiang, W.; Wan, X. Humid Bonding with a Water-Soluble Adhesive Inspired by Mussels and Sandcastle Worms. Macromol. Chem. Phys. 2015, 216, 450−459. (16) Jenkins, C. L.; Meredith, H. J.; Wilker, J. J. Molecular Weight Effects upon the Adhesive Bonding of a Mussel Mimetic Polymer. ACS Appl. Mater. Interfaces 2013, 5, 5091−5096. (17) Li, A.; Mu, Y.; Jiang, W.; Wan, X. A Mussel-Inspired Adhesive with Stronger Bonding Strength Under Underwater Conditions than Under Dry Conditions. Chem. Commun. 2015, 51, 9117−9120. (18) Maier, G. P.; Rapp, M. V.; Waite, J. H.; Israelachvili, J. N.; Butler, A. Adaptive Synergy Between Catechol and Lysine Promotes Wet Adhesion by Surface Salt Displacement. Science 2015, 349, 628− 632. (19) Wei, W.; Yu, J.; Gebbie, M. A.; Tan, Y.; Martinez Rodriguez, N. R.; Israelachvili, J. N.; Waite, J. H. Bridging adhesion of musselinspired peptides: Role of charge, chain length, and surface type. Langmuir 2015, 31 (3), 1105−1112. (20) Meredith, H. J.; Jenkins, C. L.; Wilker, J. J. Enhancing the Adhesion of a Biomimetic Polymer Yields Performance Rivaling Commercial Glues. Adv. Funct. Mater. 2014, 24, 3259−3267. (21) Mu, Y.; Wan, X. Simple but Strong: A Mussel-Inspired Hot Curing Adhesive Based on Polyvinyl Alcohol Backbone. Macromol. Rapid Commun. 2016, 37, 545−550. (22) Fan, C.; Fu, J.; Zhu, W.; Wang, D.-A. A Mussel-Inspired Double-Crosslinked Tissue Adhesive Intended for Internal Medical Use. Acta Biomater. 2016, 33, 51−63. (23) Li, L.; Yan, B.; Yang, J.; Chen, L.; Zeng, H. Novel MusselInspired Injectable Self-Healing Hydrogel with Anti-Biofouling Property. Adv. Mater. 2015, 27 (7), 1294−1299. (24) Waite, J. H. Adhesion à la Moule. Integr. Comp. Biol. 2002, 42, 1172−1180. (25) Lin, Q.; Gourdon, D.; Sun, C.; Holten-Andersen, N.; Anderson, T. A.; Waite, J. H.; Israelachvili, J. N. Adhesion Mechanisms of the Mussel Foot Proteins Mfp-1 and Mfp-3. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 3782−3786. (26) Choi, G. Y.; Zurawsky, W.; Ulman, A. Molecular Weight Effects in Adhesion. Langmuir 1999, 15, 8447−8450. (27) Deruelle, M.; Leger, L.; Tirrell, M. Adhesion at the SolidElastomer Interface: Influence of the Interfacial Chains. Macromolecules 1995, 28, 7419−7428. (28) Baker, H. R.; Leach, P. B.; Singleterry, C. R.; Zisman, W. A. Cleaning by Surface Displacement of Water and Oils. Ind. Eng. Chem. 1967, 59, 29−40. (29) Hodgson, A.; Haq, S. Water Adsorption and the Wetting of Metal Surfaces. Surf. Sci. Rep. 2009, 64, 381−451. (30) Thiel, P. A.; Madey, T. E. The Interaction of Water with Solid Surfaces: Fundamental Aspects. Surf. Sci. Rep. 1987, 7, 211−385.

ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsami.7b00270. 1 NMR spectra, GPC traces, tables of polymer characterization, and adhesion strength of poly(catechol-styrene)on various substrates compared against commercial glues (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected] (J.J.W.). ORCID

Jonathan J. Wilker: 0000-0002-7602-9892 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We appreciate helpful discussions with Heather J. Meredith and Courtney L. Jenkins. This work was generously supported by the Office of Naval Research (Grants N000141010105 and N000141310327).

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REFERENCES

(1) Stewart, R. J.; Ransom, T. C.; Hlady, V. Natural Underwater Adhesives. J. Polym. Sci., Part B: Polym. Phys. 2011, 49, 757−771. (2) Hagenau, A.; Suhre, M. H.; Scheibel, T. R. Nature as a Blueprint for Polymer Material Concepts: Protein Fiber-Reinforced Composites as Holdfasts of Mussels. Prog. Polym. Sci. 2014, 39, 1564−1583. (3) Yu, J.; Wei, W.; Danner, E.; Ashley, R. K.; Israelachvili, J.; Waite, J. W. Mussel Protein Adhesion Depends on Interprotein ThiolMediated Redox Modulation. Nat. Chem. Biol. 2011, 7, 588−590. (4) Yang, B.; Lim, C.; Hwang, D. S.; Cha, H. J. Switch of Surface Adhesion to Cohesion by Dopa-Fe3+ Complexation, in Response to Microenvironment at the Mussel Plaque/Substrate Interface. Chem. Mater. 2016, 28, 7982−7989. (5) Meyers, M. A.; McKittrick, J.; Chen, P.-Y. Structural Biological Materials: Critical Mechanics-Materials Connections. Science 2013, 339, 773−779. (6) Sparks, B. J.; Hoff, E. F. T.; Hayes, L. P.; Patton, D. L. MusselInspired Thiol−Ene Polymer Networks: Influencing Network Properties and Adhesion with Catechol Functionality. Chem. Mater. 2012, 24, 3633−3642. (7) Moulay, S. DOPA/Catechol-Tethered Polymers: Bioadhesives and Biomimetic Adhesive Materials. Polym. Rev. 2014, 54, 436−513. (8) Lee, H.; Lee, B. P.; Messersmith, P. B. A Reversible Wet/Dry Adhesive Inspired by Mussels and Geckos. Nature 2007, 448, 338− 341. 7871

DOI: 10.1021/acsami.7b00270 ACS Appl. Mater. Interfaces 2017, 9, 7866−7872

Research Article

ACS Applied Materials & Interfaces (31) Sagert, J.; Sun, C.; Waite, J. H., Chemical Subtleties of Mussel and Polychaete Holdfasts. In Biological Adhesives; Smith, A. M., Callow, J. A., Eds.; Springer-Verlag: Berlin, 2006; pp 125−143. (32) Lee, H.; Scherer, N. F.; Messersmith, P. B. Single-Molecule Mechanics of Mussel Adhesion. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 12999−13003. (33) Nielsen, L. E.; Landel, R. F., In Mechanical Properties of Polymers and Composites; Faulker, L. L., Ed. Marcel Dekker, Inc.: New York, 1994. (34) Hon, D. N. S. Analysis of Adhesives; Taylor and Francis: New York, 2003. (35) Lee, S.-B.; Gonzalez-Cabezas, C.; Kim, K.-M.; Kim, K.-N.; Kuroda, K. Catechol-Functionalized Synthetic Polymer as a Dental Adhesive to Contaminated Dentin Surface for a Composite Restoration. Biomacromolecules 2015, 16, 2265−2275. (36) Ahn, Y.; Jang, Y.; Selvapalam, N.; Yun, G.; Kim, K. Supramolecular Velcro for Reversible Underwater Adhesion. Angew. Chem., Int. Ed. 2013, 52 (11), 3140−3144. (37) Dolez, P.; Love, B., Adhesive Bonding As an Alternative For Underwater Structural Repair. In The Eleventh International Offshore and Polar Engineering Conference; International Society of Offshore and Polar Engineers: Stavanger, Norway, 2001; pp 17−22. (38) Burkett, J. R.; Wojtas, J. L.; Cloud, J. L.; Wilker, J. J. A Method for Measuring the Adhesion Strength of Marine Mussels. J. Adhes. 2009, 85, 601−615. (39) Desmond, K. W.; Zacchia, N. A.; Waite, J. H.; Valentine, M. T. Dynamics of Mussel Plaque Detachment. Soft Matter 2015, 11, 6832− 6839. (40) Mian, S. A.; Yang, L.-M.; Saha, L. C.; Ahmed, E.; Ajmal, M.; Ganz, E. A fundamental understanding of catechol and water adsorption on a hydrophilic silica surface: Exploring the underwater adhesion mechanism of mussels on an atomic scale. Langmuir 2014, 30 (23), 6906−6914. (41) Rapp, M. V.; Maier, G. P.; Dobbs, H. A.; Higdon, N. J.; Waite, J. H.; Butler, A.; Israelachvili, J. N. Defining the Catechol-Cation Synergy for Enhanced Wet Adhesion to Mineral Surfaces. J. Am. Chem. Soc. 2016, 138, 9013−9016. (42) Clancy, S. K.; Sodano, A.; Cunningham, D. J.; Huang, S. S.; Zalicki, P. J.; Shin, S.; Ahn, B. K. Marine Bioinspired Underwater Contact Adhesion. Biomacromolecules 2016, 17, 1869−1874. (43) American Society for Testing and Materials (ASTM) Standard D1002-10, Apparent Shear Strength of Single-Lap-Joint Adhesively Bonded Metal Specimens by Tension Loading (Metal-to-Metal); ASTM International: West Conshohocken, PA, 2010. (44) American Society for Testing and Materials (ASTM) Standard D2651, Preparation of Metal Surfaces for Adhesive Bonding; ASTM International, West Conshohocken, PA, 2008.

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DOI: 10.1021/acsami.7b00270 ACS Appl. Mater. Interfaces 2017, 9, 7866−7872