Density Functional Theory Study of Catechol Adhesion on Silica

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J. Phys. Chem. C 2010, 114, 20793–20800

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Density Functional Theory Study of Catechol Adhesion on Silica Surfaces† Shabeer A. Mian,‡ Leton C. Saha,‡ Joonkyung Jang,*,‡ Lu Wang,§ Xingfa Gao,§ and Shigeru Nagase*,§ Department of Nanomaterials Engineering, Pusan National UniVersity, Miryang, 627-706, Republic of Korea, and Department of Theoretical and Computational Molecular Science, Institute for Molecular Science, Myodaiji, Okazaki 444-8585, Japan ReceiVed: July 28, 2010; ReVised Manuscript ReceiVed: October 2, 2010

It has been speculated that the catechol (1,2-dihydroxybenzene) functionality of marine mussels is responsible for its strong and versatile adhesion on various wet surfaces. To elucidate features of this adhesion, we performed a periodic density functional theory calculation for catechol adsorption on silica surfaces. We obtained its binding energy and geometry on two representative hydroxylated surfaces of cristobalite, which mimic amorphous silica. Catechol strongly adhered to both surfaces by making three or four hydrogen bonds. Catechol achieved versatility in adhesion via torsion of its hydroxyls. The binding energy of catechol, which amounts to 14 kcal/mol, was larger than that of water, irrespective of the surface. With the inclusion of dispersion interaction, the binding energy of catechol further increased up to 33 kcal/mol, and its preferential adsorption over water became evident. Both the hydroxyls and phenylene ring of catechol contribute to its strong adhesion due to hydrogen bonds and dispersion. 1. Introduction 1

Marine mussel (Mytilus edulis) has the remarkable ability to adhere to virtually any wet surface including mineral, paraffin, Teflon, glass, tooth, and bone.2 Moreover, such a water-resistant adhesion functions over wide temperature ranges, varying salinities, and in tides and waves. Understanding the molecular mechanism of mussel adhesion will be invaluable for the design and synthesis of moisture-resistant adhesives that have applications in surgical tissue adhesives, dental cements, and ship building, to name a few.3 The adhesive proteins of mussel (Mefp-3 and -5 in particular) are well-known to have an unusually high content of L-DOPA (3,4-dihydroxy-L-phenylalanine). The consensus view is that the catechol functionality (1,2-dihydroxybenzene) of L-DOPA is mainly responsible for the strong adhesion of mussels.4,5 The oxidized form of DOPA (quinone) is in charge of the cross-linking of multiple adhesive proteins, which is called curing.6,7 Currently, the molecular origin of the strong and versatile adhesion of mussel remains largely unknown. In conventional pull-off8 and shear bond strength9 experiments, the cohesive and adhesive effects of adhesion are entangled. Recently, an atomic force microscopy (AFM) experiment measured the strength of the single-molecule adhesion of L-DOPA with a titanium surface (with a binding energy of 22.2 kcal/mol).10 A theoretical investigation, by obviating complications in experimentation and delving instead into the atomic details, can fill in the gaps in our understanding of the adhesion. In particular, it remains unclear how mussels establish permanent adhesion in the dominant presence of surrounding water molecules, especially for a hydrophilic surface that has strong affinity for water. If catechol is indeed responsible for the adhesion, then it must adhere to a surface more strongly than water does. However, †

Part of the “Mark A. Ratner Festschrift”. * To whom correspondence should be addressed. E-mail: jkjang@ pusan.ac.kr, [email protected]. ‡ Pusan National University. § Institute for Molecular Science.

no previous report describes a study that has compared the adhesion strength of catechol and of water. Herein, we attempt such a comparison using the density functional theory (DFT). Prior theoretical studies of the catechol adsorption have specifically examined metallic (titanium11-14 or gold4) surfaces. However, amorphous silica is expected to be more relevant to mussel adhesion in a marine environment. Amorphous silica has often been modeled as a surface of cristobalite that has a density and a refractive index close to those of amorphous silica.15-17 In humid conditions, the surface silicon (Si) atoms on a freshly cleaved silica react rapidly with water to form hydroxyls (OHs) named silanols.18 It is therefore reasonable to model the amorphous silica as a combination of hydroxylated surfaces of cristobalite. This study examines two surfaces of hydroxylated silica: the (001) surface of R-cristobalite and (111) surface of β-cristobalite. These surfaces have silanols of two distinct types: geminal (two OH groups attached to each Si atom) and isolated (single OH group attached to one Si atom) silanols, respectively, for the (001) and (111) surfaces.18 The silanol densities for these surfaces are 4.3 and 8.1 per nm2. They therefore cover the typical density of amorphous silica, 5 OH per nm2.19 For these surfaces, we investigate the physicochemical nature of the catechol adhesion using the DFT. One can choose either a cluster20-22 or a periodic system15,16,18,21,23-25 to simulate the surfaces. We opted for a periodic DFT to encompass the long-range elastic field of an infinite surface and to overcome the size limitation in a cluster model imposed by the saturation of dangling bonds at the boundary of cluster. We chose our periodic cells as sufficiently large to avoid an artificial molecular ordering typical for a periodic calculation using a small cell. We compare the binding strength of catechol with that of water on the silica surfaces. We carefully examine the geometry of catechol adsorbed onto each surface. We also investigate the structural change of catechol because of its adsorption and discuss the possible origin for its versatility in adhesion.

10.1021/jp1070538  2010 American Chemical Society Published on Web 10/15/2010

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2. Computational Details All DFT calculations were performed using the SIESTA package under periodic boundary conditions.26 We used the generalized gradient approximation (GGA) for the exchange correlation functional by application of a revised PerdewBurke-Ernzerhof (PBE) method.27 Core electrons were treated using norm-conserving pseudopotentials, following the scheme of Troullier and Martins.28 Valence electrons were treated using atomic orbitals at the level of double-ζ with polarization (DZP). The mesh cutoff26 for our atomic orbitals was 2.72 keV. We applied the Monkhorst-Pack scheme29 with 3 × 3 × 3 k points for sampling the Brillouin zone. We optimized the geometry using the conjugated gradient method30 and by allowing periodic cells to vary. We took optimization to be converged if the maximal atomic force was smaller than 0.04 eV/Å. No symmetry was assumed throughout the calculation. The initial configuration for optimization of the bulk R-cristobalite was taken from the rectangular unit cell with lattice parameters of 4.97 and 6.93 Å and with the P4121 symmetry.31 Following Iarlori et al.,16 the bulk β-cristobalite was initially taken as a cubic unit cell with a side length of 6.02 Å and with the I4j2d (body centered tetragonal) symmetry. We optimized each molecule (catechol or water) using a periodic box that was sufficiently large to ensure that no interaction occured between the molecule and its periodic images. We constructed the initial configurations for the hydroxylated silica surfaces as follows. For the hydroxylated (001) surface, we took a slab of bulk R-cristobalite. The slab was made of 16 atomic layers along the surface normal direction and was a 3 × 3 surface supercell laterally. We then terminated each Si atom in the top layer with two OHs, generating geminal silanols. The Si atoms in the bottom layer were terminated by hydrogen (H) atoms. The total number of atoms was 198. Assuming that the layer of Si atoms at the bottom is the same as the bulk structure, we fixed their positions in the geometry optimization. The periodic simulation box length along the surface normal was taken to be more than 40 Å to remove the periodicity along that direction. Our hydroxylated (111) surface comprised 10 atomic layers of β cristobalite. A 2 × 2 surface supercell was taken laterally. Each Si atom in the top layer was terminated with a single OH group, giving isolated silanols. The total number of atoms was 224. As in the (001) surface above, the Si atoms at the bottom were terminated by H and were held fixed in the geometry optimization. After optimizing the geometries of molecule (catechol or water) and surface (001 or 111) separately, we placed a catechol or a water molecule on top of each surface. The catechol was initially positioned with its phenylene ring either parallel or perpendicular to the surface. Similarly, a water molecule was placed on top of the surface with its H-O-H plane parallel or perpendicular to the surface. Typically, the lowest atom of molecule was placed 0.8-1.9 Å above the surface plane, and the O atom of catechol or water was placed 2.1-3.1 Å distant fromthenearestsurfaceOorH.Weoptimizedthemolecule-surface complex for these two initial configurations and chose the geometry with the lowest energy. Upon completion of geometry optimization, we calculated the binding energy ∆E as m+s m ∆E ) -[EMS (MS) - EM (M) - ESs(S) + δBSSE]

(1) In eq 1 and all the equations below, we use a notation system in which EBa(C) represents the energy of system C in the

geometry of B using the basis set a. In the equation above, m+s EMS (MS) is the energy of molecule-surface complex. In m (M) is the energy of an isolated molecule M addition, EM (catechol or water), and ESs(S) is the energy of the surface S (111 or 001). The current definition of binding energy differs from the conventional one in sign (a positive binding energy signifies an attraction between the molecule and surface). The basis set superposition error (BSSE) δBSSE(>0) was calculated using the counterpoise method including the deformation (in molecule and surface) as32,33 m m+s s m+s δBSSE ) [EMS (M) - EMS (M)] + [EMS (S) - EMS (S)] (2)

The molecular and surface geometries in eq 2 are taken from their geometries in the molecule-surface complex. Here, m s (M) is calculated using the molecular basis, EMS (S) is EMS (M) and Em+s obtained using the basis for the surface, and Em+s MS MS (S) are calculated using the basis for the molecule-surface complex. The deformation energies of the molecule and the surface, dEM and dES, respectively, are defined as m m dEM ) EMS (M) - EM (M)

(3)

s dES ) EMS (S) - ESs(S)

(4)

and

We calculated the dispersion interaction by using the empirical method proposed by Grimme.34 Briefly, the dispersion energy between atoms i and j, Edisp ij , is given by

Eijdisp )

-s6(Cij6 /Rij6 ) 1 + exp[-20(Rij /Rr - 1)]

(5)

Rij is the interatomic distance, and s6 is the global scaling factor depending on the functional used ()0.75 for PBE). Rr is the sum of atomic radii, and C6ij is given by the geometric mean of dispersive coefficients of atoms i and j, respectively. The atomic radius and dispersive coefficient for H, C, O, and Si were taken to be, respectively, 1.001 Å and 33.5 Å6 kcal/mol, 1.452 Å and 418.3 Å6 kcal/mol, 1.342 Å and 167.3 Å6 kcal/mol, and 1.716 Å and 2206.0 Å6 kcal/mol, respectively.34 We summed eq 5 over all atomic pairs by imposing two-dimensional periodic boundary conditions with minimum image convention.35 3. Results and Discussion 3.1. Geometries of Catechol, Water, and Silica. Table 1 presents structural parameters for the bulk R- and β-cristobalites. Listed are the lattice parameters and the volume of unit cell, the Si-O bond length dSiO, and the bending angles for the O-Si-O and Si-O-Si triples, θOSiO and θSiOSi, respectively. The present DFT calculations show excellent agreement with results of experiments for both R- and β-cristobalites.31,36 Figure 1 presents the optimized structure of catechol. Carbon and hydroxyl atoms are indexed so that various structural parameters are definable as follows. The bond lengths for O1-H1, O2-H2, O1-C1, and O2-C2 pairs are designated, respectively, as d1′, d2′, d1, and d2. The bending angles for H1-O1-C1, H2-O2-C2, O1-C1-C6, and O2-C2-C1

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TABLE 1: Optimized Structural Parameters for Bulk r- and β-Cristobalitesa R-cristobalite

lattice parameters (Å)

dSiO (Å)

unit cell vol (Å3)

θSiOSi (°)

present calc. experiment31

4.94, 7.03 4.97, 6.93

1.66 1.63

171.9 171.2

137.3 147

β-cristobalite

lattice parameter (Å)

dSiO (Å)

θOSiO (°)

θSiOSi (°)

present calc. experiment36

7.25 7.16

1.65 1.61

108.7 107.8, 112.8

146.0 146.7

a dSiO ) Si-O distance, θOSiO ) O-Si-O bending angle, θSiOSi ) Si-O-Si bending angle.

Figure 1. Optimized geometry of catechol. Carbon and hydroxyl atoms are indexed to define various bond lengths and angles. The O1-H1 and O1-C1 bond lengths are denoted respectively by d1and d1′. Here, d2 and d′, 2 respectively, represent the O2-C2 and O2-H2 bond lengths. We also define bending angles θ1, θ′, 1 θ2, and θ′2 as shown in the figure.

TABLE 2: Structural Parameters of Catechol and of a Catechol Molecule Adsorbed on a Silica Surface

isolated isolateda on (001) on (111)

d1 (Å)

d1′ (Å)

d2 (Å)

d2′ (Å)

θ1 (°)

θ2 (°)

θ1′ (°)

1.36 1.35 1.38 1.37

0.98 0.95 0.99 0.99

1.38 1.36 1.40 1.40

0.97 0.94 0.99 0.98

120.7 119.8 119.0 119.2

113.4 115.6 119.2 115.0

107.1 109.6 110.0 111.6

θ2′ (°)

φ1 (°)b

φ2 (°)

111.3 -1.3 1.6 111.4 0 0 108.3 -18.9 96.2 112.2 -25.1 -25.0

a Previous calculation by Gearhards et al.37 b A negative (positive) angle represents a clockwise (counterclockwise) rotation.

triples are denoted, respectively, as θ′, 1 θ′, 2 θ1, and θ2. Although not depicted in the figure, we also checked the dihedral angles for the H1-O1-C1-C2 and H2-O2-C2-C1 torsions, φ1 and φ2, respectively. All these structural parameters are calculated and presented in Table 2. Our results show reasonable agreement with the previous ab initio calculations using the HF/6-31G(d,p) method.37 We describe the detailed structures of isolated water, and two free silica surfaces in Supporting Information. There, the structural changes of catechol, water, and surfaces due to adsorption are explained as well. The surface density of OH for the (001) surface was 8.1 nm-2: nearly twice that of the (111) surface, 4.3 nm-2. A high OH density of 7 nm-2 was reported for precipitated silica;38 an average density of 4.9 nm-2 was reported for amorphous silica.39 Our surfaces therefore cover the typical range of OH densities for amorphous silica.40 We assume that an O-H interatomic distance of 1-4 Å gives rise to an H bond. In the following, we compare the adsorption geometry and binding energy of catechol with those of water for these two distinct surfaces.

Figure 2. Optimized geometry of a water molecule adsorbed onto the (001) surface. Only silanols are represented as balls and sticks. Lines represent siloxane bridges attached to the silanols. Hydrogen bonds are drawn as dashed lines. A side [top] and a top [bottom] view are shown together.

3.2. Adsorption Geometry of Water on Silica Surfaces. The geometry of water adsorbed onto each surface is presented first. Figure 2 shows that a water molecule forms three H bonds (which is the maximal number) with the surface OHs of the (001) surface. The bond lengths for these H bonds are 2.07, 1.64, and 1.96 Å, which are shorter than typical H bond lengths of 2.5-3.0 Å.41 Two of the H bonds of the surface vanished because of the adsorption (one between an OH and a siloxane bridge, and the other between the surface OHs). Considering the three nascent H bonds caused by the water adsorption, a net gain of one H bond exists. Shown in Figure 3 is the geometry of a water molecule adsorbed onto the (111) surface. The water molecule forms three H bonds of 1.99, 1.97, and 1.61 Å in length with the surface silanols (drawn as dashed lines). These H bond lengths are averaged as 1.86 Å, which is similar but slightly shorter than that for the adsorption on the (001) surface (1.89 Å). All in all, the adsorption geometry of water is similar for both surfaces. The structures of water and surface did not change much after adsorption (see Supporting Information for details). A water molecule formed three H bonds with both surfaces. The H-O-H plane of water is tilted from the surface plane by 21° for the (001) surface and by 44° for the (111) surface. The binding energy of water is also similar for both surfaces (see below). The previous cluster model report described that a water molecule binds with an isolated silanol via two H bonds.42 There,

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Figure 3. Optimized geometry of water adsorbed onto the (111) surface. Only silanols are represented as balls and sticks. Lines represent siloxane bridges attached to the silanols. Hydrogen bonds are shown as dashed lines. A side [top] and a top [bottom] view are drawn together.

water accepts an H from the OH of surface and donates an H to the oxygen atom of a siloxane bridge. For the present periodic surfaces, however, no siloxane bridge participated in an H bond with water. 3.3. Adsorption Geometry of Catechol on Silica Surface. We now specifically examine the adsorption of catechol on the two silica surfaces above. Figure 4 portrays a side [top] and top [bottom] view of a catechol molecule adsorbed onto the (001) surface. The catechol molecule forms four H bonds (dashed lines) with the surface OHs, and each OH of catechol functions as both an H donor and acceptor. These H bonds are 1.74, 1.73, 1.93, and 1.82 Å long. It is noteworthy that the average of these, 1.80 Å, is shorter than the average H bond lengths for the water adsorption (which were, respectively, 1.86 and 1.89 Å for the (001) and (111) surfaces). The phenylene ring plane is tilted from the surface normal by 17.61°. The catechol adsorption greatly changed its dihedral angles, φ1 and φ2, from near zero to -18.9 and 96.2°, respectively (Table 2). Other structural parameters of catechol were almost unchanged. The creation of H bonds between the catechol molecule and the surface destroyed two existing H bonds between the OHs of the surface. However, the H bonds between the surface OHs and siloxane bridges remained intact with the adsorption. In Figure 5, we show the optimized structure of a catechol molecule adsorbed onto the (111) surface. Different from the (001) surface, the catechol molecule forms three H bonds of 1.79, 1.79, and 1.89 Å in length. One OH of catechol (which has the O2 atom) functions solely as an H acceptor while the other OH serves as both an acceptor and a donor of H. Compared to the case of the (001) surface, the plane of the phenylene ring is tilted more from the surface normal by 32.6°.

Figure 4. Optimized geometry of a catechol molecule adsorbed onto the (001) surface. Only silanols are represented as balls and sticks. Lines represent siloxane bridges attached to the silanols. Hydrogen bonds are shown as dashed lines. A side and a top view are depicted respectively in the top and bottom panels. The locations of O1 and O2 atoms of catechol are indicated by arrows.

Table 2 shows that the dihedral angles of catecholsφ1 and φ2sare nearly -25°. The distortion from the initially planar geometry of catechol is not as significant as for the (001) surface. Other structural parameters of catechol barely changed with the adsorption (see Table 2). 3.4. Surface Binding Energies of Water and Catechol. Using the optimized geometries above, we calculated the binding energies (∆E) of water and catechol defined as shown in eqs 1 and 2. In Table 3, ∆E values are listed for both surfaces. The ∆E values of water are 12.17 and 11.08 kcal/mol for the (001) and (111) surfaces, respectively. Because these ∆E values are larger than the heat of liquefaction of water (10.51 kcal/mol43,44), the present surface is categorizable as a hydrophilic surface. The present ∆E values of water are comparable to those calculated using a cluster model for silica.21,25,42 Tielens et al.25 reported water binding energies for various silanols range from 10.52 to 11.95 kcal/mol, which are close to our results. Du et al.39 calculated the heat of adsorption as 12.19 kcal/mol for an isolated silanol. Civallerin et al.45 calculated the heat of adsorption is 11.11 and 8.96 kcal/mol for a geminal and for an isolated silanol, respectively. Pelmenschikov et al.42 estimated the heat of adsorption to be 9.08 and 9.32 kcal/mol for water binding with a geminal and an isolated silanol, respectively.

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Figure 5. Optimized adsorption geometry of catechol on the (111) surface. Only silanols are shown as balls and sticks. Lines represent siloxane bridges attached to the silanols. Hydrogen bonds are depicted as dashed lines. A side [top] and a top [bottom] view are drawn together. The locations of O1 and O2 atoms of catechol are indicated by arrows.

TABLE 3: Surface Binding Energies (∆E) and Deformation Energies (dEM) for Catechol and Water (kcal/mol)a

∆E dEM ∆Ewdisp

water on (001)

water on (111)

catechol on (001)

catechol on (111)

12.17 (19.80) 0.12 21.17

11.08 (37.98) 0.17 15.21

14.15 (22.82) 0.83 28.06

11.65 (36.40) 0.45 32.68

a BSSE correction for each binding energy (δBSSE) appears in parentheses.

The ∆E values for catechol are 14.15 and 11.65 kcal/mol for the (001) and (111) surfaces, respectively (Table 3). Therefore, the adsorption of catechol is stronger than that of water for both surfaces. For the case of the (001) surface, ∆E of catechol is significantly larger than that of water (by 1.98 kcal/mol). The increased binding strength for catechol arises from the extra H bond it makes with the surface. In contrast, for the (111) surface, with which both catechol and water form three H bonds, the ∆E of catechol is only 0.65 kcal/mol larger than that of water (this small difference greatly increases if we include the dispersion, see below). The binding energy attributable to a single H bond can be estimated as the ∆E divided by the number of H bonds. Such an estimate implies an average binding energy of 3.79 kcal/mol per H bond, which falls within the range of the typical binding energy of an H bond (2.4-6.2 kcal/mol41). Table 3 shows that the BSSE is large in the present calculation of ∆E (reaching up to 77% of uncorrected binding energy). A large BSSE has been reported in the DFT calculation of ∆E for a glycine adsorption on an edingtonite silica (there, the BSSE

sometimes exceeds the magnitude of uncorrected binding energy).46 Regarding their calculation of ∆E for NH3 on silica, Civalleri and Ugliengo18 reported that the BSSE of a periodic calculation is larger than that of a cluster model calculation. Probably, the BSSE is overestimated in the present periodic calculation, which modeled amorphous silica as a crystalline surface. Large BSSEs have been also found in the SIESTA calculation for the adsorption of C60 on Si (001) surface by using PBE-GGA DFT with DZP basis (close to the present calculation).47 There, BSSE was large (sometimes more than two times larger than ∆E), but the ∆E agreed with the plane wave calculation using VASP codes.48 Large BSSEs in our calculation are presumably due to the limited size of basis. Following Hobbs et. al,47 we decreased the energy shift that determines the cutoff radius of basis from 0.27 (default) to 0.054 eV. Then, by using the optimized geometries above, we recalculated ∆E for catechol on the (001) surface. Due to a larger basis, the BSSE is reduced from 22.82 to 11.70 kcal/mol, but ∆E is virtually unchanged (from 14.15 to 15.72 kcal/mol). This demonstrates the reliability of our calculation of ∆E. The present PBE functional is accurate for description of H bonds,49,50 but misses the dispersion interaction among atoms. In the B3LYP-DFT study for the adsorption of benzene-1,4diol on hydroxylated silica, Ugliengo et. al found the dispersive contribution to ∆E is significant, reaching up to 16.7 kcal/mol.51,52 Using the method of Grimme (see Computational Details), we empirically calculated the dispersion energy for all the geometries obtained above. The binding energy augmented with this dispersion, ∆Ewdisp, is listed in Table 3. The contribution of dispersion is substantial for all four cases, ranging from 4.13 to 21.03 kcal/mol. In every case, the dispersive binding energy of catechol (13.91 and 21.03 kcal/mol for the (001) and (111) surfaces, respectively) is larger than that of water (9.01 and 4.13 kcal/mol for the (001) and (111) surfaces, respectively). It is maximal for the catechol adsorbed on the (111) surface where the phenylene ring is notably tilted toward the surface. Due to the dispersion, the difference between binding energies of catechol and water has increased to 6.89 and 17.47 kcal/mol for the (001) and (111) surfaces, respectively. Therefore, the preference of catehol in adsorption became evident. Interestingly, catechol now adsorbs more strongly onto the (111) surface than onto the (001) surface. Our dispersive binding energy for catechol (13.9 and 21.0 kcal/mol) is close to the previous report for a benzene-diol on silica (16.5-16.7 kcal/mol).51 Ugliengo et al51,52 reported that Grimme’s method34 overestimates binding energies (by 4 kcal/mol for benzene-1,4-diol), and a closer match with experiment is achieved by using a slight modification of Grimme’s method.53 In this modification, due to Jurecka et. al, each atomic radius is separately scaled (instead of the global scaling factor s6 in eq 5) and more elaborate combination rules are used for Rr and C6ij in eq 5. We did not use these modifications here because they were developed for functionals and bases different from the present ones. The deformation energies (dEM) (for definition, see eq 3) of water and catechol are presented in Table 3. The dEM of catechol were 0.834 and 0.447 kcal/mol for the (001) and (111) surfaces, respectively. The dEM values of water were 0.118 and 0.119 kcal/mol for the (001) and (111) surfaces, respectively. The increased dEM of catechol relative to that of water is caused by the substantial torsion of its hydroxyls. The surface deformation energy (dES, defined in eq 4) was even greater than dEM. The dES values of the (001) surface were 1.424 and 1.528 kcal/ mol, respectively, for the adsorption of catechol and water. The dES values of the (111) surface were 0.119 and 2.258 kcal/mol

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when catechol and water were adsorbed, respectively. Therefore, adsorption of water caused a larger dES than that of catechol. It is interesting to compare the present adhesion of catechol on silica with the catechol adhesion on titanium oxide previously studied.12,14 There, a bidentate form of catechol yielded a covalent adsorption with a binding energy ranging from 25 to 30 kcal/mol.12,14 A monodentate and a nondissociative binding gave reduced binding energies of 7-21 kcal/mol and of 22 kcal/ mol, respectively. For our silica surfaces, we have not found any dissociative adsorption of catechol. The present ∆E of catechol was 14.15 kcal/mol, which is nearly half of that found for the bidentate adsorption on the titanium oxide. Interestingly, the present ∆Ewdisp arising from noncovalent H bonding and dispersion is comparable to this bindentate binding energy. The spectroscopic study of Weinhold et al.4 implied the phenylene ring plays a major role in the adhesion of L-DOPA on a gold (110) surface; the phenylene ring plane lies parallel to the surface plane. Stern et al.54 claimed that the phenylene ring of DOPA lies parallel to a platinum surface. Unlike these metallic surfaces, the present silica surface provides no charge transfer or π interaction for the phenylene ring. The plane of the phenylene ring can be characterized as a hydrophobic unit and is therefore tilted slightly from the surface normal. In the underwater adhesion of mussel, catechol is presumably surrounded by water molecules. To observe how the adsorption of catechol is affected by a water solvent, we added 31 water molecules around a catechol molecule adsorbed onto the (001) surface. Because of the large number of atoms in this case (305), we used only the Γ point in the integration of the Brillouin zone. Furthermore, the mesh cutoff for atomic orbitals was 2.04 keV. Further geometry optimization showed the adsorption geometry of catechol did not change markedly with the addition of water molecules (Figure 6). Catehcol did not lose any of its H bonds with the surface and therefore is not displaced by water. The bond lengths of catechol, d1′, d2′, d1, and d2, were virtually unchanged (increased by 0.004 Å at most). The bending angles θ1′, θ2′, θ1, and θ2 changed slightly by 2.6° or less. Only the torsion angles φ1 and φ2 changed appreciably from -18.9 and 96.2° to -20.5 and 99.9°, respectively. Therefore, the surrounding water solvent does not affect the existing catechol adsorption to the surface. The bulk-like water as shown in Figure 6 uses most of its H bonds for intermolecular cohesion. Only a single H bond is formed between each adsorbed water molecule and the surface. Using the strength of single H bond estimated above, the binding energy of water will decrease (from 12.17 and 11.08) down to 3.79 kcal/mol. Therefore, catechol adhesion in marine environment should be more favorable than is indicated by the binding energy difference between catechol and water (Table 3). Catechol molecules aggregate in principle, but this cohesion should be insignificant for the following reason. Most of the DOPA residues in the mussel protein (e.g., in Mefp 3 or 5 protein) are isolated from each other.10 A cohesion of catechol molecules therefore requires an entanglement of protein chains. An oxidation of catechol and the complex formation with metal ions are also required for such cohesion. Consequently, the cohesion of catechol molecules proceeds much slower than the adsorption onto the surface. Besides, the π-π interaction of phenylene rings is small relative to its H bonding with surface (only up to 2.7 kcal/mol55). After the initial adhesion, however, the cohesion of catechol molecules in the mussel protein is essential for the layering of proteins to strengthen the matrix for adhesion.

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Figure 6. Optimized geometry of catechol adsorbed onto the (001) surface in the presence of surrounding water molecules. The geometry is optimized after adding 31 water molecules to the catechol adsorbed onto the surface. The optimized geometry is shown as side [top] and top [bottom] views. Catechol, water, and silanols are depicted as balls and sticks. Lines represent siloxane bridges attached to the silanols. Dashed lines denote hydrogen bonds.

In the adhesion of mussel under wet conditions, catechol presumably needs to displace water molecules preadsorbed on surface. An ab initio molecular dynamics simulation56 is desirable for this, but it is too computationally demanding for the present system. As an alternative, we examined the energetics of the water displacement by catechol. To do so, we first considered an adsorption geometry where a catechol molecule lies on top of five water molecules preadsorbed on the (001) surface (Figure 7, top). The direct contact of catechol with the surface is blocked by the intervening water molecules. Next, we simulated a geometry where catechol coadsorbs onto the surface along with five water molecules surrounding it (Figure 7, bottom). This geometry might result if the water molecules in the top of Figure 7 are displaced by catechol. We found the energy of the bottom geometry of Figure 7 is lower than that of the top of Figure 7 by 11.8 kcal/mol. If the dispersion is included, the energy difference increases to 18.8 kcal/mol. Therefore, the geometry change mimicking the water displacement by catechol (from the top to the bottom of Figure 7) is energetically favorable. There is a more systematic procedure to study the water displacement due to Ugliengo et al.57 In this

Catechol Adhesion on Silica Surfaces

J. Phys. Chem. C, Vol. 114, No. 48, 2010 20799 catechol and water on silica. We studied the two representative silica surfaces with disparate densities of silanols that resemble amorphous silica under wet conditions. Catechol adhered to the current hydrophilic surfaces via multiple H bonds. The hydroxyls, not the phenylene ring, of catechol dominated its adhesion, and the plane of the phenylene ring stood nearly upright, rather than lying down parallel on the surface plane. The binding of catechol was noncovalent; its binding energy amounted to 14 kcal/mol, which is smaller than that for the covalent binding with a titanium oxide. Catechol adhered to both silica surfaces more strongly than water with a difference in binding energy of 2 kcal/mol or less. With the inclusion of empirical dispersion interaction, the binding energy of catechol rose up to 33 kcal/mol, comparable to its bidentate binding with a titanium surface. Consequently, the preference of catechol over water became pronounced. Catechol was also flexible in adhesion: its hydroxyls freely rotated with respect to its phenylene ring to find an optimal geometry for adsorption. Moreover, once catechol adhered to a strongly hydrophilic silica surface (the (001) surface of R-cristobalite), its adhesion was unaffected by the addition of surrounding water molecules. The displacement of preadsorbed water molecules by catechol was energetically favorable. However, to address the question of how catechol initially establishes its adsorption in the dominant existing water molecules on the surface, a more systematic57 or dynamical study (ab initio molecular dynamics) seems necessary. It would be interesting to study the cohesion effects due to the interaction of multiple catechol molecules. To fully address this cohesion, it is necessary to consider the covalent cross-linking mediated by metal ion58,59 and the physical entanglement of protein chains. We also hope to improve the present calculation considering the thermal effects such as the zero point energy and entropy. We think, however, that the present work captures the essential features of the catechol adsorption of marine mussels. It is expected to serve as a useful guideline for an improved theoretical investigation of mussel adhesion.

Figure 7. Optimized geometry of catechol lying on top of five water molecules preadsorbed on the (001) surface [top]. Optimized geometry of catechol directly adsorbed on the (001) surface with five surrounding water molecules that are coadsorbed [bottom]. Catechol, water, and silanols are depicted as balls and sticks. Lines represent siloxane bridges attached to the silanols. Dashed lines denote hydrogen bonds.

procedure, one also considers intermediate configurations for the transition from the top to the bottom of Figure 7. That is, starting from the configuration of the bottom figure, we imagine detaching one water molecule from the surface and inserting it between catechol and the surface. As a result of this process, catechol loses one of the H bonds with the surface, and one water molecule bridges catechol and the surface. By repeating this process, we can get consecutive intermediate configurations that gradually change from the bottom to top of Figure 7. By calculating various energies of reactions having these configurations as products, one can determine whether the water displacement is energetically favorable. We are currently investigating the water displacement by using this procedure. 4. Concluding Remarks To advance our understanding of mussel adhesion, we presented results of a comparative study of the adhesion of

Acknowledgment. This study was supported by a Korea Research Foundation Grant funded by the Korean Government (MEST) (No. 2009-0089497). J. J. is thankful to IMS for his stay as a visiting associate professor. J. J. is grateful to Mark Ranter for all the support and inspiration he gave over the years. Supporting Information Available: Optimized geometries for water and the (001) and (111) silica surfaces. Optimized structures of the (001) and (111) surfaces are drawn in Figures S1 and S2, respectively. We also describe the structural change of each free surface due to the adsorption of water or catechol. This material is available free of charge via the Internet at http:// pubs.acs.org. References and Notes (1) Lee, H.; Lee, B. P.; Messersmith, P. B. Nature 2007, 448, 338. (2) Waite, J. H. Int. J. Adhes. Adhes. 1987, 7, 9. (3) Ninan, L.; Monahan, J.; Stroshine, R. L.; Wilker, J. J.; Shi, R. Biomaterials 2003, 24, 4091. (4) Weinhold, M.; Soubatch, S.; Temirov, R.; Rohlfing, M.; Jastorff, B.; Tautz, F. S.; Doose, C. J. Phys. Chem. B 2006, 110, 23756. (5) Yu, M.; Hwang, J.; Deming, T. J. J. Am. Chem. Soc. 1999, 121, 5825. (6) Westwood, G.; Horton, T. N.; Wilker, J. J. Macromolecules 2007, 40, 3960. (7) Burzio, L. A.; Waite, J. H. Biochemistry 2000, 39, 11147. (8) Young, G. A.; Crisp, D. J. In Adhesion; Allen, K. W., Ed.; Applied Science: London, 1982; p 19. (9) Yu, M.; Deming, T. J. Macromolecules 1998, 31, 4739.

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