Density Functional Theory Study of Catechol Adhesion on Silica Surfaces†

Shabeer A. Mian,‡ Leton C. Saha,‡ Joonkyung Jang,*,‡ Lu Wang,§ Xingfa Gao,§ andShigeru 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 responsiblefor its strong and versatile adhesion on various wet surfaces. To elucidate features of this adhesion, weperformed a periodic density functional theory calculation for catechol adsorption on silica surfaces. Weobtained its binding energy and geometry on two representative hydroxylated surfaces of cristobalite, whichmimic 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, whichamounts to 14 kcal/mol, was larger than that of water, irrespective of the surface. With the inclusion ofdispersion interaction, the binding energy of catechol further increased up to 33 kcal/mol, and its preferentialadsorption over water became evident. Both the hydroxyls and phenylene ring of catechol contribute to itsstrong adhesion due to hydrogen bonds and dispersion.

1. Introduction

Marine mussel (Mytilus edulis)1 has the remarkable abilityto adhere to virtually any wet surface including mineral, paraffin,Teflon, glass, tooth, and bone.2 Moreover, such a water-resistantadhesion functions over wide temperature ranges, varyingsalinities, and in tides and waves. Understanding the molecularmechanism of mussel adhesion will be invaluable for the designand synthesis of moisture-resistant adhesives that have applica-tions in surgical tissue adhesives, dental cements, and shipbuilding, to name a few.3 The adhesive proteins of mussel(Mefp-3 and -5 in particular) are well-known to have anunusually high content of L-DOPA (3,4-dihydroxy-L-phenyla-lanine). The consensus view is that the catechol functionality(1,2-dihydroxybenzene) of L-DOPA is mainly responsible forthe strong adhesion of mussels.4,5 The oxidized form of DOPA(quinone) is in charge of the cross-linking of multiple adhesiveproteins, which is called curing.6,7

Currently, the molecular origin of the strong and versatileadhesion of mussel remains largely unknown. In conventionalpull-off8 and shear bond strength9 experiments, the cohesive andadhesive effects of adhesion are entangled. Recently, an atomicforce microscopy (AFM) experiment measured the strength ofthe single-molecule adhesion of L-DOPA with a titanium surface(with a binding energy of 22.2 kcal/mol).10 A theoreticalinvestigation, by obviating complications in experimentation anddelving instead into the atomic details, can fill in the gaps inour understanding of the adhesion. In particular, it remainsunclear how mussels establish permanent adhesion in thedominant presence of surrounding water molecules, especiallyfor a hydrophilic surface that has strong affinity for water. Ifcatechol is indeed responsible for the adhesion, then it mustadhere to a surface more strongly than water does. However,

no previous report describes a study that has compared theadhesion strength of catechol and of water. Herein, we attemptsuch a comparison using the density functional theory (DFT).Prior theoretical studies of the catechol adsorption have spe-cifically examined metallic (titanium11-14 or gold4) surfaces.However, amorphous silica is expected to be more relevant tomussel adhesion in a marine environment. Amorphous silicahas often been modeled as a surface of cristobalite that has adensity and a refractive index close to those of amorphoussilica.15-17 In humid conditions, the surface silicon (Si) atomson a freshly cleaved silica react rapidly with water to formhydroxyls (OHs) named silanols.18 It is therefore reasonable tomodel the amorphous silica as a combination of hydroxylatedsurfaces of cristobalite.

This study examines two surfaces of hydroxylated silica: the(001) surface of R-cristobalite and (111) surface of �-cristobalite.These surfaces have silanols of two distinct types: geminal (twoOH groups attached to each Si atom) and isolated (single OHgroup attached to one Si atom) silanols, respectively, for the(001) and (111) surfaces.18 The silanol densities for thesesurfaces are 4.3 and 8.1 per nm2. They therefore cover the typicaldensity of amorphous silica, 5 OH per nm2.19 For these surfaces,we investigate the physicochemical nature of the catecholadhesion using the DFT. One can choose either a cluster20-22

or a periodic system15,16,18,21,23-25 to simulate the surfaces. Weopted for a periodic DFT to encompass the long-range elasticfield of an infinite surface and to overcome the size limitationin a cluster model imposed by the saturation of dangling bondsat the boundary of cluster. We chose our periodic cells assufficiently large to avoid an artificial molecular ordering typicalfor a periodic calculation using a small cell. We compare thebinding strength of catechol with that of water on the silicasurfaces. We carefully examine the geometry of catecholadsorbed onto each surface. We also investigate the structuralchange of catechol because of its adsorption and discuss thepossible origin for its versatility in adhesion.

† Part of the “Mark A. Ratner Festschrift”.* To whom correspondence should be addressed. E-mail: jkjang@

pusan.ac.kr, nagase@ims.ac.jp.‡ Pusan National University.§ Institute for Molecular Science.

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

10.1021/jp1070538 2010 American Chemical SocietyPublished on Web 10/15/2010

2. Computational Details

All DFT calculations were performed using the SIESTApackage under periodic boundary conditions.26 We used thegeneralized gradient approximation (GGA) for the exchangecorrelation functional by application of a revised Perdew-Burke-Ernzerhof (PBE) method.27 Core electrons were treatedusing norm-conserving pseudopotentials, following the schemeof Troullier and Martins.28 Valence electrons were treated usingatomic orbitals at the level of double-� with polarization (DZP).The mesh cutoff26 for our atomic orbitals was 2.72 keV. Weapplied the Monkhorst-Pack scheme29 with 3 × 3 × 3 k pointsfor sampling the Brillouin zone. We optimized the geometryusing the conjugated gradient method30 and by allowing periodiccells to vary. We took optimization to be converged if themaximal atomic force was smaller than 0.04 eV/Å. No sym-metry was assumed throughout the calculation.

The initial configuration for optimization of the bulk R-cris-tobalite was taken from the rectangular unit cell with latticeparameters of 4.97 and 6.93 Å and with the P4121 symmetry.31

Following Iarlori et al.,16 the bulk �-cristobalite was initiallytaken as a cubic unit cell with a side length of 6.02 Å and withthe I4j2d (body centered tetragonal) symmetry. We optimizedeach molecule (catechol or water) using a periodic box that wassufficiently large to ensure that no interaction occured betweenthe molecule and its periodic images.

We constructed the initial configurations for the hydroxylatedsilica surfaces as follows. For the hydroxylated (001) surface,we took a slab of bulk R-cristobalite. The slab was made of 16atomic layers along the surface normal direction and was a 3× 3 surface supercell laterally. We then terminated each Si atomin the top layer with two OHs, generating geminal silanols. TheSi atoms in the bottom layer were terminated by hydrogen (H)atoms. The total number of atoms was 198. Assuming that thelayer of Si atoms at the bottom is the same as the bulk structure,we fixed their positions in the geometry optimization. Theperiodic simulation box length along the surface normal wastaken to be more than 40 Å to remove the periodicity alongthat direction. Our hydroxylated (111) surface comprised 10atomic layers of � cristobalite. A 2 × 2 surface supercell wastaken laterally. Each Si atom in the top layer was terminatedwith a single OH group, giving isolated silanols. The totalnumber of atoms was 224. As in the (001) surface above, theSi atoms at the bottom were terminated by H and were heldfixed in the geometry optimization.

After optimizing the geometries of molecule (catechol orwater) and surface (001 or 111) separately, we placed a catecholor a water molecule on top of each surface. The catechol wasinitially positioned with its phenylene ring either parallel orperpendicular to the surface. Similarly, a water molecule wasplaced on top of the surface with its H-O-H plane parallel orperpendicular to the surface. Typically, the lowest atom ofmolecule was placed 0.8-1.9 Å above the surface plane, andthe O atom of catechol or water was placed 2.1-3.1 Å distantfromthenearestsurfaceOorH.Weoptimizedthemolecule-surfacecomplex for these two initial configurations and chose thegeometry with the lowest energy.

Upon completion of geometry optimization, we calculatedthe binding energy ∆E as

In eq 1 and all the equations below, we use a notation systemin which EB

a (C) represents the energy of system C in the

geometry of B using the basis set a. In the equation above,EMS

m+s(MS) is the energy of molecule-surface complex. Inaddition, EM

m(M) is the energy of an isolated molecule M(catechol or water), and ES

s (S) is the energy of the surface S(111 or 001). The current definition of binding energy differsfrom the conventional one in sign (a positive binding energysignifies an attraction between the molecule and surface). Thebasis set superposition error (BSSE) δBSSE(>0) was calculatedusing the counterpoise method including the deformation (inmolecule and surface) as32,33

The molecular and surface geometries in eq 2 are taken fromtheir geometries in the molecule-surface complex. Here,EMS

m (M) is calculated using the molecular basis, EMSs (S) is

obtained using the basis for the surface, and EMSm+s(M) and EMS

m+s(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

and

We calculated the dispersion interaction by using the empiricalmethod proposed by Grimme.34 Briefly, the dispersion energybetween atoms i and j, Eij

disp, is given by

Rij is the interatomic distance, and s6 is the global scaling factordepending on the functional used ()0.75 for PBE). Rr is thesum of atomic radii, and C6

ij is given by the geometric mean ofdispersive coefficients of atoms i and j, respectively. The atomicradius and dispersive coefficient for H, C, O, and Si were takento be, respectively, 1.001 Å and 33.5 Å6 kcal/mol, 1.452 Å and418.3 Å6 kcal/mol, 1.342 Å and 167.3 Å6 kcal/mol, and 1.716Å and 2206.0 Å6 kcal/mol, respectively.34 We summed eq 5over all atomic pairs by imposing two-dimensional periodicboundary conditions with minimum image convention.35

3. Results and Discussion

3.1. Geometries of Catechol, Water, and Silica. Table 1presents structural parameters for the bulk R- and �-cristobalites.Listed are the lattice parameters and the volume of unit cell,the Si-O bond length dSiO, and the bending angles for theO-Si-O and Si-O-Si triples, θOSiO and θSiOSi, respectively.The present DFT calculations show excellent agreement withresults of experiments for both R- and �-cristobalites.31,36

Figure 1 presents the optimized structure of catechol. Carbonand hydroxyl atoms are indexed so that various structuralparameters are definable as follows. The bond lengths forO1-H1, O2-H2, O1-C1, and O2-C2 pairs are designated,respectively, as d1′ , d2′ , d1, and d2. The bending angles forH1-O1-C1, H2-O2-C2, O1-C1-C6, and O2-C2-C1

∆E ) -[EMSm+s(MS) - EM

m(M) - ESs (S) + δBSSE]

(1)

δBSSE ) [EMSm (M) - EMS

m+s(M)] + [EMSs (S) - EMS

m+s(S)](2)

dEM ) EMSm (M) - EM

m(M) (3)

dES ) EMSs (S) - ES

s (S) (4)

Eijdisp )

-s6(C6ij/Rij

6)

1 + exp[-20(Rij/Rr - 1)](5)

20794 J. Phys. Chem. C, Vol. 114, No. 48, 2010 Mian et al.

triples are denoted, respectively, as θ1′ , θ2′ , θ1, and θ2. Althoughnot depicted in the figure, we also checked the dihedral anglesfor the H1-O1-C1-C2 and H2-O2-C2-C1 torsions, φ1 andφ2, respectively. All these structural parameters are calculatedand presented in Table 2. Our results show reasonable agreementwith the previous ab initio calculations using the HF/6-31G(d,p)method.37

We describe the detailed structures of isolated water, and twofree silica surfaces in Supporting Information. There, thestructural changes of catechol, water, and surfaces due toadsorption are explained as well. The surface density of OHfor 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 wasreported for precipitated silica;38 an average density of 4.9 nm-2

was reported for amorphous silica.39 Our surfaces therefore coverthe typical range of OH densities for amorphous silica.40 Weassume that an O-H interatomic distance of 1-4 Å gives riseto an H bond. In the following, we compare the adsorptiongeometry and binding energy of catechol with those of waterfor these two distinct surfaces.

3.2. Adsorption Geometry of Water on Silica Surfaces.The geometry of water adsorbed onto each surface is presentedfirst. 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 lengthsof 2.5-3.0 Å.41 Two of the H bonds of the surface vanishedbecause of the adsorption (one between an OH and a siloxanebridge, and the other between the surface OHs). Consideringthe three nascent H bonds caused by the water adsorption, anet gain of one H bond exists. Shown in Figure 3 is the geometryof a water molecule adsorbed onto the (111) surface. The watermolecule forms three H bonds of 1.99, 1.97, and 1.61 Å inlength with the surface silanols (drawn as dashed lines). TheseH bond lengths are averaged as 1.86 Å, which is similar butslightly shorter than that for the adsorption on the (001) surface(1.89 Å).

All in all, the adsorption geometry of water is similar forboth surfaces. The structures of water and surface did not changemuch 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 by21° for the (001) surface and by 44° for the (111) surface. Thebinding energy of water is also similar for both surfaces (seebelow). The previous cluster model report described that a watermolecule binds with an isolated silanol via two H bonds.42 There,

TABLE 1: Optimized Structural Parameters for Bulkr- and �-Cristobalitesa

R-cristobalitelattice parameters

(Å)dSiO

(Å)unit cell vol

(Å3)θSiOSi

(°)

present calc. 4.94, 7.03 1.66 171.9 137.3experiment31 4.97, 6.93 1.63 171.2 147

�-cristobalitelattice parameter

(Å) dSiO (Å) θOSiO (°) θSiOSi (°)

present calc. 7.25 1.65 108.7 146.0experiment36 7.16 1.61 107.8, 112.8 146.7

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 atomsare indexed to define various bond lengths and angles. The O1-H1and O1-C1 bond lengths are denoted respectively by d1and d1′ . Here,d2 and d2′, respectively, represent the O2-C2 and O2-H2 bond lengths.We also define bending angles θ1, θ1′, θ2, and θ2′ as shown in the figure.

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

d1(Å)

d1′(Å)

d2(Å)

d2′(Å)

θ1(°)

θ2(°)

θ1′(°)

θ2′(°)

φ1(°)b

φ2(°)

isolated 1.36 0.98 1.38 0.97 120.7 113.4 107.1 111.3 -1.3 1.6isolateda 1.35 0.95 1.36 0.94 119.8 115.6 109.6 111.4 0 0on (001) 1.38 0.99 1.40 0.99 119.0 119.2 110.0 108.3 -18.9 96.2on (111) 1.37 0.99 1.40 0.98 119.2 115.0 111.6 112.2 -25.1 -25.0

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

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

Catechol Adhesion on Silica Surfaces J. Phys. Chem. C, Vol. 114, No. 48, 2010 20795

water accepts an H from the OH of surface and donates an Hto the oxygen atom of a siloxane bridge. For the present periodicsurfaces, however, no siloxane bridge participated in an H bondwith water.

3.3. Adsorption Geometry of Catechol on Silica Surface.We now specifically examine the adsorption of catechol on thetwo silica surfaces above. Figure 4 portrays a side [top] andtop [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 catecholfunctions as both an H donor and acceptor. These H bonds are1.74, 1.73, 1.93, and 1.82 Å long. It is noteworthy that theaverage of these, 1.80 Å, is shorter than the average H bondlengths for the water adsorption (which were, respectively, 1.86and 1.89 Å for the (001) and (111) surfaces). The phenylenering plane is tilted from the surface normal by 17.61°. Thecatechol adsorption greatly changed its dihedral angles, φ1 andφ2, 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 andthe surface destroyed two existing H bonds between the OHsof the surface. However, the H bonds between the surface OHsand siloxane bridges remained intact with the adsorption.

In Figure 5, we show the optimized structure of a catecholmolecule adsorbed onto the (111) surface. Different from the(001) surface, the catechol molecule forms three H bonds of1.79, 1.79, and 1.89 Å in length. One OH of catechol (whichhas the O2 atom) functions solely as an H acceptor while theother OH serves as both an acceptor and a donor of H.Compared to the case of the (001) surface, the plane of thephenylene ring is tilted more from the surface normal by 32.6°.

Table 2 shows that the dihedral angles of catecholsφ1 andφ2sare nearly -25°. The distortion from the initially planargeometry of catechol is not as significant as for the (001) surface.Other structural parameters of catechol barely changed with theadsorption (see Table 2).

3.4. Surface Binding Energies of Water and Catechol.Using the optimized geometries above, we calculated the bindingenergies (∆E) of water and catechol defined as shown in eqs 1and 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 arelarger 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 thosecalculated using a cluster model for silica.21,25,42 Tielens et al.25

reported water binding energies for various silanols range from10.52 to 11.95 kcal/mol, which are close to our results. Du etal.39 calculated the heat of adsorption as 12.19 kcal/mol for anisolated silanol. Civallerin et al.45 calculated the heat ofadsorption is 11.11 and 8.96 kcal/mol for a geminal and for anisolated silanol, respectively. Pelmenschikov et al.42 estimatedthe heat of adsorption to be 9.08 and 9.32 kcal/mol for waterbinding with a geminal and an isolated silanol, respectively.

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

Figure 4. Optimized geometry of a catechol molecule adsorbed ontothe (001) surface. Only silanols are represented as balls and sticks.Lines represent siloxane bridges attached to the silanols. Hydrogenbonds are shown as dashed lines. A side and a top view are depictedrespectively in the top and bottom panels. The locations of O1 and O2atoms of catechol are indicated by arrows.

20796 J. Phys. Chem. C, Vol. 114, No. 48, 2010 Mian et al.

The ∆E values for catechol are 14.15 and 11.65 kcal/molfor the (001) and (111) surfaces, respectively (Table 3).Therefore, the adsorption of catechol is stronger than that ofwater for both surfaces. For the case of the (001) surface, ∆Eof catechol is significantly larger than that of water (by 1.98kcal/mol). The increased binding strength for catechol arisesfrom the extra H bond it makes with the surface. In contrast,for the (111) surface, with which both catechol and water formthree H bonds, the ∆E of catechol is only 0.65 kcal/mol largerthan that of water (this small difference greatly increases if weinclude the dispersion, see below). The binding energy attribut-able to a single H bond can be estimated as the ∆E divided bythe number of H bonds. Such an estimate implies an averagebinding energy of 3.79 kcal/mol per H bond, which falls withinthe range of the typical binding energy of an H bond (2.4-6.2kcal/mol41).

Table 3 shows that the BSSE is large in the present calculationof ∆E (reaching up to 77% of uncorrected binding energy). Alarge BSSE has been reported in the DFT calculation of ∆Efor a glycine adsorption on an edingtonite silica (there, the BSSE

sometimes exceeds the magnitude of uncorrected bindingenergy).46 Regarding their calculation of ∆E for NH3 on silica,Civalleri and Ugliengo18 reported that the BSSE of a periodiccalculation is larger than that of a cluster model calculation.Probably, the BSSE is overestimated in the present periodiccalculation, which modeled amorphous silica as a crystallinesurface. Large BSSEs have been also found in the SIESTAcalculation for the adsorption of C60 on Si (001) surface by usingPBE-GGA DFT with DZP basis (close to the present calcula-tion).47 There, BSSE was large (sometimes more than two timeslarger than ∆E), but the ∆E agreed with the plane wavecalculation using VASP codes.48 Large BSSEs in our calculationare presumably due to the limited size of basis. Following Hobbset. al,47 we decreased the energy shift that determines the cutoffradius of basis from 0.27 (default) to 0.054 eV. Then, by usingthe optimized geometries above, we recalculated ∆E for catecholon the (001) surface. Due to a larger basis, the BSSE is reducedfrom 22.82 to 11.70 kcal/mol, but ∆E is virtually unchanged(from 14.15 to 15.72 kcal/mol). This demonstrates the reliabilityof our calculation of ∆E.

The present PBE functional is accurate for description of Hbonds,49,50 but misses the dispersion interaction among atoms.In the B3LYP-DFT study for the adsorption of benzene-1,4-diol on hydroxylated silica, Ugliengo et. al found the dispersivecontribution to ∆E is significant, reaching up to 16.7 kcal/mol.51,52

Using the method of Grimme (see Computational Details), weempirically calculated the dispersion energy for all the geom-etries obtained above. The binding energy augmented with thisdispersion, ∆Ewdisp, is listed in Table 3. The contribution ofdispersion is substantial for all four cases, ranging from 4.13to 21.03 kcal/mol. In every case, the dispersive binding energyof catechol (13.91 and 21.03 kcal/mol for the (001) and (111)surfaces, respectively) is larger than that of water (9.01 and 4.13kcal/mol for the (001) and (111) surfaces, respectively). It ismaximal for the catechol adsorbed on the (111) surface wherethe phenylene ring is notably tilted toward the surface. Due tothe dispersion, the difference between binding energies ofcatechol and water has increased to 6.89 and 17.47 kcal/molfor the (001) and (111) surfaces, respectively. Therefore, thepreference of catehol in adsorption became evident. Interest-ingly, catechol now adsorbs more strongly onto the (111) surfacethan onto the (001) surface. Our dispersive binding energy forcatechol (13.9 and 21.0 kcal/mol) is close to the previous reportfor a benzene-diol on silica (16.5-16.7 kcal/mol).51 Ugliengoet al51,52 reported that Grimme’s method34 overestimates bindingenergies (by 4 kcal/mol for benzene-1,4-diol), and a closer matchwith experiment is achieved by using a slight modification ofGrimme’s method.53 In this modification, due to Jurecka et. al,each atomic radius is separately scaled (instead of the globalscaling factor s6 in eq 5) and more elaborate combination rulesare used for Rr and C6

ij in eq 5. We did not use these modifi-cations here because they were developed for functionals andbases different from the present ones.

The deformation energies (dEM) (for definition, see eq 3) ofwater and catechol are presented in Table 3. The dEM of catecholwere 0.834 and 0.447 kcal/mol for the (001) and (111) surfaces,respectively. The dEM values of water were 0.118 and 0.119kcal/mol for the (001) and (111) surfaces, respectively. Theincreased dEM of catechol relative to that of water is caused bythe substantial torsion of its hydroxyls. The surface deformationenergy (dES, defined in eq 4) was even greater than dEM. ThedES values of the (001) surface were 1.424 and 1.528 kcal/mol, respectively, for the adsorption of catechol and water. ThedES values of the (111) surface were 0.119 and 2.258 kcal/mol

Figure 5. Optimized adsorption geometry of catechol on the (111)surface. Only silanols are shown as balls and sticks. Lines representsiloxane bridges attached to the silanols. Hydrogen bonds are depictedas 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 DeformationEnergies (dEM) for Catechol and Water (kcal/mol)a

water on(001)

water on(111)

catechol on(001)

catechol on(111)

∆E 12.17 (19.80) 11.08 (37.98) 14.15 (22.82) 11.65 (36.40)dEM 0.12 0.17 0.83 0.45∆Ewdisp 21.17 15.21 28.06 32.68

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

Catechol Adhesion on Silica Surfaces J. Phys. Chem. C, Vol. 114, No. 48, 2010 20797

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 catecholon silica with the catechol adhesion on titanium oxide previouslystudied.12,14 There, a bidentate form of catechol yielded acovalent adsorption with a binding energy ranging from 25 to30 kcal/mol.12,14 A monodentate and a nondissociative bindinggave reduced binding energies of 7-21 kcal/mol and of 22 kcal/mol, respectively. For our silica surfaces, we have not foundany dissociative adsorption of catechol. The present ∆E ofcatechol was 14.15 kcal/mol, which is nearly half of that foundfor the bidentate adsorption on the titanium oxide. Interestingly,the present ∆Ewdisp arising from noncovalent H bonding anddispersion is comparable to this bindentate binding energy. Thespectroscopic study of Weinhold et al.4 implied the phenylenering plays a major role in the adhesion of L-DOPA on a gold(110) surface; the phenylene ring plane lies parallel to the surfaceplane. Stern et al.54 claimed that the phenylene ring of DOPAlies parallel to a platinum surface. Unlike these metallic surfaces,the present silica surface provides no charge transfer or πinteraction for the phenylene ring. The plane of the phenylenering can be characterized as a hydrophobic unit and is thereforetilted slightly from the surface normal.

In the underwater adhesion of mussel, catechol is presumablysurrounded by water molecules. To observe how the adsorptionof catechol is affected by a water solvent, we added 31 watermolecules 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 geometryof catechol did not change markedly with the addition of watermolecules (Figure 6). Catehcol did not lose any of its H bondswith the surface and therefore is not displaced by water. Thebond lengths of catechol, d1′ , d2′ , d1, and d2, were virtuallyunchanged (increased by 0.004 Å at most). The bending anglesθ1′ , θ2′ , θ1, and θ2 changed slightly by 2.6° or less. Only thetorsion angles φ1 and φ2 changed appreciably from -18.9 and96.2° to -20.5 and 99.9°, respectively. Therefore, the surround-ing water solvent does not affect the existing catechol adsorptionto the surface.

The bulk-like water as shown in Figure 6 uses most of its Hbonds for intermolecular cohesion. Only a single H bond isformed between each adsorbed water molecule and the surface.Using the strength of single H bond estimated above, the bindingenergy of water will decrease (from 12.17 and 11.08) down to3.79 kcal/mol. Therefore, catechol adhesion in marine environ-ment should be more favorable than is indicated by the bindingenergy difference between catechol and water (Table 3).Catechol molecules aggregate in principle, but this cohesionshould be insignificant for the following reason. Most of theDOPA residues in the mussel protein (e.g., in Mefp 3 or 5protein) are isolated from each other.10 A cohesion of catecholmolecules therefore requires an entanglement of protein chains.An oxidation of catechol and the complex formation with metalions are also required for such cohesion. Consequently, thecohesion of catechol molecules proceeds much slower than theadsorption onto the surface. Besides, the π-π interaction ofphenylene 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 isessential for the layering of proteins to strengthen the matrixfor adhesion.

In the adhesion of mussel under wet conditions, catecholpresumably needs to displace water molecules preadsorbed onsurface. An ab initio molecular dynamics simulation56 isdesirable for this, but it is too computationally demanding forthe present system. As an alternative, we examined the energet-ics of the water displacement by catechol. To do so, we firstconsidered an adsorption geometry where a catechol moleculelies on top of five water molecules preadsorbed on the (001)surface (Figure 7, top). The direct contact of catechol with thesurface is blocked by the intervening water molecules. Next,we simulated a geometry where catechol coadsorbs onto thesurface along with five water molecules surrounding it (Figure7, bottom). This geometry might result if the water moleculesin the top of Figure 7 are displaced by catechol. We found theenergy of the bottom geometry of Figure 7 is lower than thatof the top of Figure 7 by 11.8 kcal/mol. If the dispersion isincluded, the energy difference increases to 18.8 kcal/mol.Therefore, the geometry change mimicking the water displace-ment by catechol (from the top to the bottom of Figure 7) isenergetically favorable. There is a more systematic procedureto study the water displacement due to Ugliengo et al.57 In this

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

20798 J. Phys. Chem. C, Vol. 114, No. 48, 2010 Mian et al.

procedure, one also considers intermediate configurations forthe transition from the top to the bottom of Figure 7. That is,starting from the configuration of the bottom figure, we imaginedetaching one water molecule from the surface and inserting itbetween catechol and the surface. As a result of this process,catechol loses one of the H bonds with the surface, and onewater molecule bridges catechol and the surface. By repeatingthis process, we can get consecutive intermediate configurationsthat gradually change from the bottom to top of Figure 7. Bycalculating various energies of reactions having these configura-tions as products, one can determine whether the water dis-placement is energetically favorable. We are currently investi-gating the water displacement by using this procedure.

4. Concluding Remarks

To advance our understanding of mussel adhesion, wepresented results of a comparative study of the adhesion of

catechol and water on silica. We studied the two representativesilica surfaces with disparate densities of silanols that resembleamorphous silica under wet conditions. Catechol adhered to thecurrent hydrophilic surfaces via multiple H bonds. The hy-droxyls, not the phenylene ring, of catechol dominated itsadhesion, and the plane of the phenylene ring stood nearlyupright, rather than lying down parallel on the surface plane.The binding of catechol was noncovalent; its binding energyamounted to 14 kcal/mol, which is smaller than that for thecovalent binding with a titanium oxide. Catechol adhered toboth silica surfaces more strongly than water with a differencein binding energy of 2 kcal/mol or less. With the inclusion ofempirical dispersion interaction, the binding energy of catecholrose up to 33 kcal/mol, comparable to its bidentate binding witha titanium surface. Consequently, the preference of catechol overwater became pronounced. Catechol was also flexible inadhesion: its hydroxyls freely rotated with respect to itsphenylene ring to find an optimal geometry for adsorption.Moreover, once catechol adhered to a strongly hydrophilic silicasurface (the (001) surface of R-cristobalite), its adhesion wasunaffected by the addition of surrounding water molecules. Thedisplacement of preadsorbed water molecules by catechol wasenergetically favorable. However, to address the question of howcatechol initially establishes its adsorption in the dominantexisting water molecules on the surface, a more systematic57 ordynamical study (ab initio molecular dynamics) seems neces-sary. It would be interesting to study the cohesion effects dueto the interaction of multiple catechol molecules. To fullyaddress this cohesion, it is necessary to consider the covalentcross-linking mediated by metal ion58,59 and the physicalentanglement of protein chains. We also hope to improve thepresent calculation considering the thermal effects such asthe zero point energy and entropy. We think, however, that thepresent work captures the essential features of the catecholadsorption of marine mussels. It is expected to serve as a usefulguideline for an improved theoretical investigation of musseladhesion.

Acknowledgment. This study was supported by a KoreaResearch Foundation Grant funded by the Korean Government(MEST) (No. 2009-0089497). J. J. is thankful to IMS for hisstay as a visiting associate professor. J. J. is grateful to MarkRanter for all the support and inspiration he gave over the years.

Supporting Information Available: Optimized geometriesfor water and the (001) and (111) silica surfaces. Optimizedstructures of the (001) and (111) surfaces are drawn in FiguresS1 and S2, respectively. We also describe the structural changeof 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.

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

Catechol Adhesion on Silica Surfaces J. Phys. Chem. C, Vol. 114, No. 48, 2010 20799

(10) Lee, H.; Scherer, N. F.; Messersmith, P. B. Proc. Natl. Acad. Sci.U.S.A. 2006, 103, 12999.

(11) Rego, L. G. C.; Batista, V. S. J. Am. Chem. Soc. 2003, 125, 7989.(12) Vega-Arroyo, M.; LeBreton, P. R.; Rajh, T.; Zapol, P.; Curtiss,

L. A. Chem. Phys. Lett. 2005, 406, 306.(13) Duncan, W. R.; Prezhdo, O. V. J. Phys. Chem. B 2004, 109, 365.(14) Redfern, P. C.; Zapol, P.; Curtiss, L. A.; Rajh, T.; Thurnauer, M. C.

J. Phys. Chem. B 2003, 107, 11419.(15) Ceresoli, D.; Bernasconi, M.; Iarlori, S.; Parrinello, M.; Tosatti, E.

Phys. ReV. Lett. 2000, 84, 3887.(16) Iarlori, S.; Ceresoli, D.; Bernasconi, M.; Donadio, D.; Parrinello,

M. J. Phys. Chem. B 2001, 105, 8007.(17) Yang, J.; Meng, S.; Xu, L. F.; Wang, E. G. Phys. ReV. Lett. 2004,

92, 146102.(18) Civalleri, B.; Ugliengo, P. J. Phys. Chem. B 2000, 104, 9491.(19) Zhuravlev, L. T. Langmuir 1987, 3, 316.(20) Montero-Cabrera, L. A.; Perez-Badell, Y.; Mora-Fonz, M. J. J. Phys.

Chem. A 2008, 112, 2880.(21) Civalleri, B.; Garrone, E.; Ugliengo, P. Langmuir 1999, 15, 5829.(22) Walsh, T. R.; Wilson, M.; Sutton, A. P. J. Chem. Phys. 2000, 113,

9191.(23) Yang, J.; Wang, E. G. Phys. ReV. B 2006, 73, 035406.(24) Pedone, A.; Malavasi, G.; Menziani, M. C.; Segre, U.; Musso, F.;

Corno, M.; Civalleri, B.; Ugliengo, P. Chem. Mater. 2008, 20, 2522.(25) Tielens, F.; Gervais, C.; Lambert, J. F. O.; Mauri, F.; Costa, D.

Chem. Mater. 2008, 20, 3336.(26) Soler, J. M.; Artacho, E.; Gale, J.; Garcia, A.; Junquera, J.; Ordejon,

P.; Sanchez-Portal, D. J. Phys.: Condens. Matter 2002, 14, 2745.(27) Hammer, B.; Hansen, L. B.; Nørskov, J. K. Phys. ReV. B 1999, 59,

7413.(28) Troullier, N.; Martins, J. L. Phys. ReV. B 1991, 43, 1993.(29) Monkhorst, H. J.; Pack, J. D. Phys. ReV. B 1976, 13, 5188.(30) Hestenes, M. R.; Stiefel, E. J. Res. Nat. Bur. Stand. 1952, 49.(31) Pluth, J. J.; Smith, J. V.; Faber, J. J. J. Appl. Phys. 1985, 57, 1045.(32) Xantheas, S. S. J. Chem. Phys. 1996, 104, 8821.(33) van Duijneveldt, F. B.; van Duijneveldt-van de Rijdt, J. G. C. M.;

van Lenthe, J. H. Chem. ReV. 1994, 94, 1873.(34) Grimme, S. J. Comput. Chem. 2006, 27, 1787.(35) Smith, W.; Yong, C. W.; Rodger, P. M. Mol. Simul. 2002, 28, 385.(36) Wright, A. F.; Leadbetter, A. J. Philos. Mag. 1975, 31.

(37) Gerhards, M.; Perl, W.; Schumm, S.; Henrichs, U.; Jacoby, C.;Kleinermanns, K. J. Chem. Phys. 1996, 104, 9362.

(38) Anglada, E.; M. Soler, J.; Junquera, J.; Artacho, E. Phys. ReV. B2002, 66, 205101.

(39) Du, M.-H.; Kolchin, A.; Cheng, H.-P. J. Chem. Phys. 2004, 120,1044.

(40) Legrand, A. P. The Surface Properties of Silicas; Wiley: New York,1998.

(41) Kinloch, A. J. J. Mater. Sci. 1980, 15, 2141.(42) Pelmenschikov, A. G.; Morosi, G.; Gamba, A. J. Phys. Chem. A

1997, 101, 1178.(43) Bakaev, V. A.; Steele, W. A. J. Chem. Phys. 1999, 111, 9803.(44) Bolis, V.; Fubini, B.; Marchese, L.; Martra, G.; Costat, D. J. Chem.

Soc., Faraday Trans. 1991, 87, 497.(45) Civalleri, B.; Garrone, E.; Ugliengo, P. Chem. Phys. Lett. 1999,

299, 443.(46) Rimola, A.; Sodupe, M.; Tosoni, S.; Civalleri, B.; Ugliengo, P.

Langmuir 2006, 22, 6593.(47) Hobbs, C.; Kantorovich, L.; Gale, J. D. Surf. Sci. 2005, 591, 45.(48) Kresse, G.; Furthmuller, J. Phys. ReV. B 1996, 54, 11169.(49) Zhao, Y.; Truhlar, D. G. Theo. Chem. Acc. 2008, 120, 215.(50) van der Wijst, T.; Guerra, C. F.; Swart, M.; Bickelhaupt, F. M.

Chem. Phys. Lett. 2006, 426, 415.(51) Rimola, A.; Civalleri, B.; Uglieno, P. Phys. Chem. Chem. Phys.

2010, 12, 6357.(52) Civalleri, B.; Zicovich-Wilson, C. M.; Valenzano, L.; Ugliengo,

P. Cryst. Eng. Comm. 2008, 10, 405.(53) Jurecka, P.; Cerny, J.; Hobza, P.; Salahub, D. J. Comput. Chem.

2007, 28, 555.(54) Stern, D. A.; Salaita, G. N.; Lu, F.; McCargar, J. W.; Batina, N.;

Frank, D. G.; Laguren-Davidson, L.; Lin, C. H.; Walton, N. Langmuir 1988,4, 711.

(55) Sinnokro, M. O.; Sherrill, C. D. J. Phys. A 2004, 108, 10200.(56) Car, R.; Parrinello, M. Phys. ReV. Lett. 1985, 55, 2471.(57) Rimola, A.; Corno, M.; Zicovich-Wilson, C. M.; Ugliengo, P. Phys.

Chem. Chem. Phys. 2009, 11, 9005.(58) Zeng, H.; Hwang, D. S.; Israelachvili, J. N.; Waite, J. H. Proc.

Nat. Acad. Sci. 2010, 107, 12850.(59) Berglin, M.; Hedlund, J.; Fant, C.; Elwing, H. J. Adhes. Sci. 2005,

81, 805.

JP1070538

20800 J. Phys. Chem. C, Vol. 114, No. 48, 2010 Mian et al.