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A density functional theory study on theunderwater adhesion of catechol onto agraphite surface†

Ramesh Kumar Chitumalla, a Kiduk Kim, a Xingfa Gao *b andJoonkyung Jang *a

Mussel foot proteins (MFPs) strongly adhere to both hydrophilic and hydrophobic surfaces under wet

conditions. This water-resistant adhesion of MFP is ascribed to catechol (1,2-dihydroxybenzene) which is

highly contained in the MFP. Currently, little is known about the molecular details of the underwater

adhesion of catechol onto a nonpolar hydrophobic surface. By using the density functional theory, we

investigate the adhesion of catechol onto a wet graphite surface. We unveil the molecular geometry and

energy in the course of the wet adhesion of catechol. Catechol adheres through p–p stacking with the

underlying graphite. The surrounding water molecules further strengthen the adhesion by forming

hydrogen bonds with catechol. In addition, a significant charge transfer has been observed from wet

graphite to the catechol. Consequently, catechol adheres onto the present hydrophobic surface as

strongly as onto a hydrophilic silica surface.

1. Introduction

Amazingly, marine mussels can firmly adhere to virtually anysurface (glasses, plastics, and metal oxides) under wet and tidalconditions. This water-resistant adhesion of mussels is univer-sal, strong, and biodegradable, which is unparalleled by anysynthetic adhesive. Understanding the wet adhesion of musselscan serve as a fundamental guideline for the rational design ofa water-resistant adhesive which can be applied, for example, asa medical glue or a dental cement.1–3

Marine mussels adhere through their byssal threads4,5

which form plaques on surfaces. These plaques containseveral types of proteins called mussel foot proteins(MFPs).6,7 Noticeably, all the MFPs contain an unusually highcontent of 3,4-dihydroxy-L-phenylalanine (DOPA)8–10 in theiramino-acid sequences.8,11,12 More specifically, the catechol(1,2-dihydroxybenzene) group of DOPA9 is considered to beresponsible for the wet adhesion of MFP. There is evidence thatcatechols participate in both the initial surface anchoring andthe later cross-linking (curing) of MFPs.13,14

Catechol can adhere to both organic and inorganic surfacesby establishing reversible non-covalent or irreversible covalentbonds.15 The adhesion of catechol has been theoreticallystudied for various surfaces. A prior density functional theory(DFT) study showed that catechol binds to a titanium oxidewith an adhesion energy of 25–30 kcal mol�1.16 Another DFTstudy estimated the adhesion energy of catechol onto a hydro-xylated silica surface to be 33 kcal mol�1.17 Regarding theadhesion of catechol onto a hydrophilic surface, previousstudies18,19 revealed that catechol adheres by forming multiplehydrogen bonds with a polar surface. In contrast, little isknown at the molecular level about the underwater adhesionof catechol onto a nonpolar hydrophobic surface where theadhesion phenomenon and molecular orientation are signifi-cantly different from the adhesion onto a hydrophilic surface.On the hydrophilic (hydroxylated silica) surface, the hydroxylgroups, not the phenylene ring, of catechol dominated theadhesion by forming multiple H bonds with the hydroxylgroups of the surface. In contrast, both the hydroxyl groupsand the phenylene ring of catechol were involved in the presentadhesion onto the hydrophobic graphite surface. Herein, wepresent the first DFT study on the underwater adhesion ofcatechol onto a hydrophobic graphite surface. The dispersioninteraction should be important for the present adhesion ofcatechol onto a nonpolar surface which does not possess anypolar or hydroxyl groups. Therefore, we employ the DFT-D2method of Grimme to account for the long-range dispersion(van der Waals) interactions.20 We investigate the molecular

a Department of Nanoenergy Engineering, Pusan National University, Busan 46241,

Republic of Korea. E-mail: jkjang@pusan.ac.kr; Tel: +82-51-510-7348b College of Chemistry and Chemical Engineering, Jiangxi Normal University,

Nanchang 330022, China. E-mail: gaox@jxnu.edu.cn; Tel: +82-51-510-3983

† Electronic supplementary information (ESI) available: Optimized geometry of awater molecule adsorbed on a graphite surface (Fig. S1, ESI†). The orientation ofcatechol adhered to the dry or wet graphite surface (Fig. S2, ESI†). See DOI:10.1039/d0cp05623e

Received 28th October 2020,Accepted 7th December 2020

DOI: 10.1039/d0cp05623e

rsc.li/pccp

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geometry and energy in the course of the underwater adhesionof catechol. Our study shows that catechol strongly adheres viap–p stacking with the graphite and also via hydrogen bondsformed with the surrounding water molecules. Consequently,catechol adheres to the present hydrophobic surface as stronglyas to a hydrophilic surface.

2. Simulation methods

The present DFT calculation uses the generalized gradientapproximation (GGA)21–23 with the Perdew–Burke–Ernzerhof(PBE) functional24 to model the exchange–correlation. Projectoraugmented wave25,26 potentials are employed to describe theelectronic–ionic core interactions for carbon (C), oxygen (O), andhydrogen (H) atoms. The dispersion interaction between atoms iand j, Eij, is evaluated by using the DFT-D2 method of Grimme:20

Eij ¼�s6ðCij

6=R6ijÞ

1þ exp½�20ðRij=Rr � 1Þ�;

where Rij is the distance between atoms i and j; the global scalingparameter s6 is optimized (= 0.75) for the PBE functional; Rr

represents the sum of the atomic radii; and Cij6 is the geometric

mean of the dispersive coefficients of atoms i and j. The sum ofthe atomic radius Rr and the dispersive coefficient Cij

6 for C, H, andO are, respectively, 1.452 Å and 418.3 Å6 kcal mol�1, 1.001 Å and33.5 Å6 kcal mol�1, and 1.32 Å and 167.3 Å6 kcal mol�1.20 Theresults of the present DFT method agree with the experimentsfor benzene or phenol adsorbed on a graphite surface.27,28 All

the DFT methods described above are implemented by usingthe Vienna ab initio Simulation Package (version 5.4.1).29–31 Inaddition to the DFT-D2 method, the adsorption of catechol ongraphite is also studied employing DFT-D332 (zero damping)and DFT-D3-BJ32,33 (Becke–Jonson damping) methods toexplore various dispersion corrections on adhesion.

Graphite can adopt AB or ABC stacking.34–36 As AB-stackedgraphite is more stable,28,37–39 we model the present graphite asAB-stacked bi-layers of graphene. We use a periodic hexagonalsupercell containing 144 carbon atoms, which is a 6 � 6 surfacesupercell laterally (a = b = 14.76 Å). The simulation cell length(c) along the direction normal to the surface is taken to be 45 Å,to eliminate the periodicity along the Z-direction. The C atomsof the bottom layer of graphite are held fixed during geometryoptimization. We use the Monkhorst–Pack scheme40 with 1 �1 � 1 k-points for sampling the Brillouin zone and a plane-wavecutoff energy of 450 eV. The geometry optimization is declaredto be converged if the maximal energy difference is o10�5 eVand the force on every atom is o0.02 eV Å�1. The optimizedstructure of graphite gives an interlayer spacing of 3.35 Å and aC–C bond length of 1.42 Å. These values are in accordance withthose reported in the earlier reports.41–43

3. Results and discussion

We investigate the molecular structure of catechol by indexingselected C, H, and O atoms and by defining various structuralparameters shown in Fig. 1: the lengths of O1–C1, O2–C2,O1–H1, and O2–H2 bonds are designated, respectively, as d1,d2, d1

0, and d20. The bending angles of the O1–C1–C6, O2–C2–C1,

H1–O1–C1, and H2–O2–C2 are designated, respectively, as y1, y2,y10, and y2

0. The torsion angles of H1–O1–C1–C2 and H2–O2–C2–C3 are denoted as Ø1 and Ø2, respectively. Table 1 lists all thestructural parameters optimized for an isolated catechol andfor the catechol adsorbed on a dry or wet graphite surface. Thepresent structural parameters of an isolated catechol agree withthose reported in the previous Hartree–Fock and post-Hartree–Fock (MP2) ab initio calculations at the 6-31G(d,p) level of theory.7

Upon adhesion onto a dry graphite surface, almost all thestructural parameters of catechol are virtually unchanged. Thetorsion angles, Ø1 and Ø2, however significantly change fromnear-zero to �2.4 and �13.41, respectively (Table 1). Thissignifies that the hydroxyl (OH) groups of catechol rotate outof the phenylene ring toward the graphite surface. This torsionpresumably arises from the attraction between the partiallypositive H atoms of the OH groups and the negative electric

Fig. 1 Structural parameters of catechol. The O1–C1 and O1–H1 bondlengths are represented, respectively, by d1 and d1

0. The O2–C2 and O2–H2 bond lengths are represented by d2 and d2

0, respectively. The bendingangles of O1–C1–C6, O2–C2–C1, H1–O1–C1, and H2–O2–C2 aredenoted by y1, y1

0, y2, and y20, respectively.

Table 1 Structural parameters optimized for isolated catechol and for catechol adsorbed on a dry or wet graphite surface. All the distances and angles(defined in the main text) are listed in units of Å and degree, respectively

d1 d10 d2 d2

0 y1 y10 y2 y2

0 Ø1b Ø2

b

Isolated 1.36 0.98 1.38 0.97 119.7 107.9 115.3 109.5 �0.2 0.1Isolateda 1.35 0.95 1.36 0.94 119.8 109.6 115.6 111.4 0.0 0.0On a dry graphite 1.37 0.98 1.38 0.97 119.7 107.8 115.3 109.7 �2.4 �13.4On a wet graphite 1.38 0.99 1.38 1.03 120.4 106.4 115.3 111.2 1.4 10.6

a J. Chem. Phys., 1996, 104, 9362–9375.7 b A positive (negative) angle represents a counterclockwise (clockwise) rotation.

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charges accumulated at the centers of the hexagonal rings ofgraphite.44 This electrostatic interaction, called the OH–p inter-action, attracts the OH groups toward the graphite surface.Fig. 2a shows that the H2 atom is directly above the center of ahexagonal ring of C below. Consequently, the electrostaticattraction is stronger for the H2 atom, producing a significantchange in Ø2. The H1 atom is relatively distant from any of thecenters of the hexagonal rings of graphite. Therefore, Ø1 onlyslightly deviates from zero. The slight change in Ø1 also can beascribed to the intramolecular H bonding between H1 and O2atoms which keeps the H1 atom in the plane of the phenylene ring.

Fig. 2b shows that the ring of catechol is nearly parallel tothe underlying graphite surface with the center of mass (COM)of catechol of 3.12 Å above the surface. This parallel orientationsuggests the p–p interaction between catechol and graphite.Catechol adopts a slipped p–p stacking in which the center ofits phenylene ring is located above the bridge site betweentwo C atoms of graphite, instead of the center of a hexagonalring (Fig. 2a). In fact, the p–p interaction commonly adopts aslipped–parallel, instead of a face-to-face, alignment. The p–sattraction in the slipped–parallel alignment, which is absent inthe face-to-face alignment, additionally stabilizes the adhesionof catechol.45 As shown in Fig. 2c, the phenylene ring interactswith four hexagonal rings of C below: the centroid of thephenylene ring is 3.41, 3.41, 3.69, and 3.94 Å away from thecentroids of four hexagonal rings of C below. The corres-ponding angle between the surface normal of graphite andthe centroid–centroid vector varies as 20, 21, 30, and 351(Fig. 2c). For an effective p–p interaction, the centroid–centroiddistance should be o3.80 Å and the angle between the surfacenormal of graphite and the centroid–centroid vector should beo201.45 The two hexagonal rings of graphite are 3.41 Å awayfrom the centroid of catechol and have angles close to 201,indicative of strong p–p interactions. The other two hexagonal

rings of graphite exhibit moderate p–p interactions withcatechol because their centroid–centroid distances and anglesare larger. In addition to these p–p interactions, the OH–pinteractions between the OH groups of catechol and graphitefurther strengthen the adhesion of catechol. It is interestingto note that the phenylene ring of catechol is nearly parallel tothe surface, unlike on the hydrophilic surfaces where it standsupright.

From the geometry of catechol adhered on the dry graphitesurface (Fig. 2), we calculate the adhesion energy Ead as Ead =(ES + EM) � EMS, where ES is the energy of pristine graphite andEM and EMS represent the energies of the isolated catecholand of the catechol adhered to the graphite surface, respec-tively. Ead is found to be 12.68 kcal mol�1, which is close to thepreviously calculated values of 11.53 and 12.91 kcal mol�1 forbenzene27 and phenol28 adsorbed on a graphite surface, respec-tively. The Ead values of catechol on graphite obtained from theother two methods, viz., DFT-D3 and DFT-D3-BJ, are 11.66 and12.36 kcal mol�1, respectively. These Ead values are marginallysmaller than that obtained from the DFT-D2 method.

We investigate, for comparison, the adhesion of a water(H2O) molecule onto the dry graphite surface. An isolated watermolecule has an O–H bond length of 0.97 Å and a H–O–Hbending angle of 104.41. Upon adhesion onto the dry graphitesurface, the O–H bond length changes from 0.97 to 0.98 Å andthe H–O–H angle from 104.41 to 104.71. In order to calculate theadhesion energy of a water molecule, we consider three differ-ent locations of the O atom of water on the graphite: on top ofa C atom (top), on top of the center of a hexagonal ring of C(center), and on top of the bridge site of a C–C bond (bridge).For each of these three locations, we consider two opposingorientations in which the OH groups of water point toward(down) or away from (up) the graphite surface. The H–O–Hplane of a water molecule is always vertical to the graphitesurface (Fig. S1, ESI,† shows the optimized geometries of watermolecules adhered on different locations). In Table 2, Ead

values for water molecules adsorbed at three different locations

Fig. 2 Geometry optimized for catechol adhered on a graphite surface.Top (a), side (b), and slant (c) views are drawn. In (c), the centroids ofcatechol and of four hexagonal rings of the graphite surface are drawn asballs. The centroid–centroid distances are shown along with the anglesbetween the centroid–centroid vectors and the surface normal of thegraphite. Two different views are shown in (c). The bottom layer ofgraphite is not shown for visual clarity.

Table 2 Adhesion energy (Ead) and equilibrium distance (D0) of a watermolecule adhered on a graphite surface. Ead and D0 are calculated forthree different locations of the O atom of water on the graphite surface:on top of the center of the hexagonal ring of C (center), on top of thebridge site between two C atoms (bridge), and on top of a C atom (top). Foreach location, we consider two orientations of water in which the OHgroups point down toward (down) and up away from (up) the graphitesurface. D0 refers to the vertical distances of the O and H atoms from thetop layer of graphite for the up and down orientations, respectively

Location Orientation

Ead (kcal mol�1) D0 (Å)

This work Prior worka This work Prior worka

Center Up 3.78 1.91 3.22 3.07Down 4.13 3.21 2.69 2.60

Bottom Up 3.54 1.78 3.29 3.17Down 4.01 2.97 2.88 2.67

Top Up 3.42 1.73 3.37 3.18Down 3.94 2.95 2.65 2.65

a Phys. Chem. Chem. Phys., 2011, 13, 12041–12047.46

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with the up and down orientations of OH groups are listed. Ead

ranges from 3.42 to 4.13 kcal mol�1. The most stable is thewater molecule with its OH groups pointing down towardthe graphite and its O atom located above the center of thehexagonal ring of C, giving an Ead value of 4.13 kcal mol�1.The present Ead values are comparable to the earlier reportsusing the PBE-D2 (1.73 to 3.21 kcal mol�1)46 and DFT/CC(2.10 to 3.59 kcal mol�1)47 methods.

Fig. 3 shows the potential energy surface (PES) for theadhesion of catechol onto the dry graphite surface: the energyof the adhered catechol E is plotted vs. the vertical distance ofthe COM of catechol from the graphite surface, D. The PES iscalculated by fixing the distance of one O atom of catechol fromthe surface, while the other degrees of freedom are allowed torelax. The PES has the minimum located at D = 3.10 Å wherecatechol has its phenylene ring nearly parallel (tilted by 2.31,see Fig. S2, ESI†) to the graphite surface. With decreasingD from the minimum point, the energy steeply increases to5.38 and 19.71 kcal mol�1 at D = 2.91 and 2.69 Å, respectively.At these short D values, the ring of catechol is substantiallytilted from the parallel orientation. On the other hand, withincreasing D from 3.10 Å, E smoothly increases from theminimum and levels off for D 49 Å. In this range of D values,the ring of catechol always remains parallel to the graphitesurface. The range of the interaction between catechol andgraphite extends to 9 Å, which is typical for an intermoleculardispersion interaction. In the same figure, we have comparedthe PES for the adhesion of catechol on the dry graphite surfaceobtained from the DFT-D2 method with those obtained usingDFT-D3 and DFT-D3(BJ) methods. The three PES curves showsimilar adhesion behavior for catechol on graphite. Therefore,we have chosen only the DFT-D2 method, where the Ead value ofcatechol is the strongest, for the wet adhesion.

We now move on to investigate the adhesion of catecholonto a wet graphite surface. The wet adhesion of catechol is

emulated by adding 70 water molecules with a liquid density of1.0 g cm�3. Fig. 4a and b depict the geometry of catecholadhered on the wet graphite surface in the top and side views,respectively. The OH groups of catechol act as both acceptorsand donors of H bonds with water molecules. A H bond isconsidered to be formed if the O–H distance ranges from 1 to4 Å18 and all the established H bonds between catechol andwater molecules have shown shorter O–H distances than 4 Å.Seven H bonds form between catechol and water molecules, asdenoted by the dotted lines in Fig. 4c. Catechol develops twostrong (O–H distances o 2.2 Å) and five weak (O–H distances 43.2 Å) H bonds. In two strong H bonds, one OH group ofcatechol acts as a H bond donor (with a bond distance of 1.57 Å)and the other OH group as an acceptor (with a distance of1.79 Å). We have not observed any moderate H bonds with theH bond distance ranging from 2.2 to 3.2 Å. The longest H bonddistance that we have observed is 3.93 Å for a weak H bond,whereas the other H bonds are shorter or equal to 3.5 Å. Also, anintramolecular H bond forms between the two OH groups ofcatechol with a bond distance of 2.07 Å (not shown in the figure).

As listed in Table 1, the bond lengths of catechol, d1, d10, d2,

and d20, slightly increase upon adhesion onto the wet graphite

surface. The increase in d20 (by 0.06 Å) is quite significant

because the O2H2 group is a H bond donor to three watermolecules. The O1H1 group, on the other hand, is a H bondacceptor and d1

0 increases by 0.01 Å only. The bending anglesy1, y1

0, and y2, are virtually unchanged (change by o11).Only y2

0 (H2–O2–C2) varies from 109.71 to 111.21 due to theH bonding between the H2 atom and water molecules. Thedihedral angles Ø1 and Ø2 substantially change to 1.41 and10.61, respectively, from the negative values of �2.41 and�13.41, respectively, found for the dry graphite. The negativevalues (clockwise rotation) of Ø1 and Ø2 on the dry graphiteindicate that the H atoms are attracted and tilted toward thesurface. In contrast, the positive dihedral angles (counterclock-wise rotation) of Ø1 and Ø2 (1.41 and 10.61) on the wet graphiteindicate that the H atoms are tilted away from the graphitesurface. This arises from the fact that catechol on thewet graphite surface forms H bonds with water molecules, inaddition to the p–p stacking with the graphite surface. Here, theH bond interaction wins over, making the OH groups ofcatechol tilt away from, rather than toward, the graphitesurface. The multiple H bonds formed between catechol andthe surrounding water may contribute ca. 26 kcal mol�1 to wetadhesion energy.17

As shown in Fig. 4d, the ring of catechol interacts with fourhexagonal rings of graphite through p–p stacking, as found forthe dry graphite above. Fig. 4a shows that this p–p stackingagain adopts a slipped alignment48,49 in which the O1 atom islocated above the center of a hexagonal ring of C and the O2atom is above the center of a C–C bridge. The phenylene ring ofcatechol is tilted, however, due to the H bonds formed betweencatechol and the water molecules (Fig. 4b). We calculate the tiltangle of the phenylene ring of catechol by calculating the angleformed between the surface normal of the phenylene ringand the surface normal of the graphite surface (Z-axis). The tilt

Fig. 3 Potential energy surface for the adhesion of catechol onto agraphite surface. The energy of catechol adhered to the surface, E, isplotted vs. the vertical distance of the center of mass (COM) of catecholfrom the surface, D. E is shifted so that it is zero at the minimum. Snapshotsof the adhered catechol are shown for D values of 2.69 and 3.10 Å. Linesare drawn as a visual guide.

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angle of catechol on the wet graphite surface is 10.81, whereasthe corresponding angle on the dry graphite is only 2.31(detailed geometries are shown in Fig. S2, ESI†). Only onehexagonal ring of graphite has a significant p–p interactionwith catechol where the centroid–centroid distance and angleare 3.59 Å and 12.711, respectively. The other three centroidsweakly interact with catechol because their centroid–centroiddistances are 3.90, 4.06, and 4.20 Å and the correspondingangles are 26.2, 30.1, and 33.61, respectively.

To gain deeper insights into the adhesion process, we havealso studied the charge transfer between graphite and catecholfor the energetically most stable configurations of dry andwet adhesion. We employed the quantum theory of atoms inmolecules by Bader50 in combination with the code developedby Henkelman et al.51 to compute the charge transfer. TheBader charge analysis revealed that the charge transfer occursfrom the graphite surface to the catechol. It has been observed

that the charge transfer from graphite to the catechol is moderate;however, it is significant from wet graphite to the catechol. Theestimated charge transfer from wet graphite to the catechol is ca.five times higher than that from the graphite surface. This chargetransfer is further confirmed and visualized through chargedensity difference plots. Fig. 5 depicts the induced charge densityredistribution upon the adhesion of catechol on the graphitesurface. The charge density accumulation around catechol anddepletion from the surface are represented in yellow and cyancolors, respectively. The computed values of the transferredcharge from graphite (0.016 |e|) and wet graphite (0.075 |e|) tothe catechol are also shown in Fig. 5.

We finally study how strongly catechol adheres to the wetgraphite surface. To do so, we construct the PES by varying thevertical distance of catechol D. Fig. 6 indicates that the PES ofthe wet adhesion is qualitatively similar to that of the adhesiononto the dry graphite surface. Quantitatively, however, theenergy minimum is located at D = 3.39 Å, which is longer thanthe minimum distance found for the dry adhesion (3.10 Å).As D increases beyond 4.05 Å, we find that catechol loses itsdirect contact with the graphite surface and water moleculesintervene between catechol and graphite. Note that the mini-mum of the PES curve is much deeper than that of the dryadhesion. The adhesion energy Ead is not well defined forthe wet adhesion of catechol because of the presence of thewater solvent. Instead, the adhesion energy is estimated as thedepth of the minimum of PES relative to the energy convergedat large D values (48 Å), that is, 39.31 kcal mol�1. This is more

Fig. 4 Geometry of catechol adhered to a wet graphite surface. The top (a), side (b), and slant (c) views are drawn. The COM of catechol is 3.39 Å abovethe graphite surface. Six H bonds formed between catechol and water molecules are shown as dotted lines (c). The p–p stacking of catechol with the wetgraphite surface (d). The centroids of catechol and of four hexagonal rings of graphite are drawn as balls. The centroid–centroid distances are shownalong with the angles of centroid–centroid vectors measured from the surface normal of the graphite. In (d), two different views are shown. Watermolecules are not drawn for visual clarity.

Fig. 5 Charge density difference plots of catechol adhered to a dry (left)and a wet (right) graphite surface for the most stable adhesion structures.Yellow (cyan) regions stand for the charge accumulation (depletion).

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than three times larger than that of the dry adhesion(12.68 kcal mol�1). This is rather surprising given that watermolecules are expected to interfere and weaken the adhesion ofcatechol. Once catechol anchors on the surface by displacingthe pre-adsorbed water molecules however, the multipleH bonds formed between catechol and the water moleculesfurther strengthen the adhesion of catechol compared to thedry adhesion of catechol where only the p–p stacking drives theadhesion. The present adhesion energy of catechol onto thewet graphite is close to that found for adhesion onto a wethydrophilic silica surface (B44 kcal mol�1).18 Furthermore,the present PES curve is qualitatively similar to the potential-of-mean-force curve reported in the prior molecular dynamicssimulation of the adhesion of catechol on a wet aluminasurface.52

4. Conclusions

At present, the remarkably water-resistant adhesion of musselsonto a nonpolar hydrophobic surface is not well understoodat the molecular level. Given that the catecholic moieties ofmussels are responsible for their adhesion, we performed theDFT study on the adhesion of catechol onto a dry or wetgraphite surface. Catechol adheres to the dry graphite mainlyvia p–p stacking by making its phenylene ring parallel to thegraphite surface. The adhesion of catechol is further strength-ened by the OH–p interaction between the OH groups ofcatechol and the center of the hexagonal ring of carbonbelonging to the graphite. On the wet graphite surface coveredby water, catechol adheres with an energy of 39.31 kcal mol�1,which is more than three times larger than that found for thedry graphite. This arises from the multiple H bonds formedbetween catechol and water molecules, in addition to p–pstacking of catechol with the graphite. The strong wet adhesionis also supported by the charge transfer to the catechol which is

further confirmed by charge density difference plots. As a result,the present adhesion energy of catechol on wet graphite is close tothat found on a hydrophilic silica surface.

Conflicts of interest

There are no conflicts to declare.

Acknowledgements

This study was supported by a grant from the National ResearchFoundation of Korea (NRF) funded by the Korea government(2018R1A2A2A05019776 and 2016H1D3A1936765). X. G. was sup-ported by the National Natural Science Foundation of China(21773095).

References

1 J. Dove and P. Sheridan, J. Am. Dent. Assoc., JADA, 1986,112, 879.

2 S.-B. Lee, C. Gonzalez-Cabezas, K.-M. Kim, K.-N. Kim andK. Kuroda, Biomacromolecules, 2015, 16, 2265–2275.

3 Y. K. Jo, B.-H. Choi, C. Zhou, J.-S. Ahn, S. H. Jun andH. J. Cha, J. Mater. Chem. B, 2015, 3, 8102–8114.

4 J. H. Waite, N. H. Andersen, S. Jewhurst and C. Sun,J. Adhes., 2005, 81, 297–317.

5 C. V. Benedict and J. H. Waite, J. Morphol., 1986, 189,171–181.

6 H. Zhao and J. H. Waite, J. Biol. Chem., 2006, 281,26150–26158.

7 M. Gerhards, W. Perl, S. Schumm, U. Henrichs, C. Jacobyand K. Kleinermanns, J. Chem. Phys., 1996, 104, 9362–9375.

8 J. Waite, Chem. Indus., 1991, 2, 607–610.9 R. J. Stewart, T. C. Ransom and V. Hlady, J. Polym. Sci., Part

B: Polym. Phys., 2011, 49, 757–771.10 M. A. Matin, R. K. Chitumalla, M. Lim, X. Gao and J. Jang,

J. Phys. Chem. B, 2015, 119, 5496–5504.11 E. W. Danner, Y. Kan, M. U. Hammer, J. N. Israelachvili and

J. H. Waite, Biochemistry, 2012, 51, 6511–6518.12 W. Wei, J. Yu, C. Broomell, J. N. Israelachvili and J. H. Waite,

J. Am. Chem. Soc., 2012, 135, 377–383.13 S. Haemers, G. J. M. Koper and G. Frens, Biomacromolecules,

2003, 4, 632–640.14 L. A. Burzio and J. H. Waite, Biochemistry, 2000, 39,

11147–11153.15 P. Kord Forooshani and B. P. Lee, J. Polym. Sci., Part A:

Polym. Chem., 2017, 55, 9–33.16 P. C. Redfern, P. Zapol, L. A. Curtiss, T. Rajh and

M. C. Thurnauer, J. Phys. Chem. B, 2003, 107, 11419–11427.17 S. A. Mian, L. C. Saha, J. Jang, L. Wang, X. Gao and

S. Nagase, J. Phys. Chem. C, 2010, 114, 20793–20800.18 S. A. Mian, X. Gao, S. Nagase and J. Jang, Theor. Chem. Acc.,

2011, 130, 333–339.19 S. A. Mian, L.-M. Yang, L. C. Saha, E. Ahmed, M. Ajmal and

E. Ganz, Langmuir, 2014, 30, 6906–6914.

Fig. 6 Potential energy surface for the adhesion of catechol onto a wetgraphite surface. The energy E is plotted vs. the vertical distance of theCOM of catechol measured from the graphite surface, D (drawn assquares). The PES is shifted so that its value is zero at the minimum. Alsoplotted for comparison is the PES for the adhesion of catechol onto a drygraphite surface (circles).

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This journal is©the Owner Societies 2021 Phys. Chem. Chem. Phys., 2021, 23, 1031--1037 | 1037

20 S. Grimme, J. Comput. Chem., 2006, 27, 1787–1799.21 V. N. Staroverov, G. E. Scuseria, J. Tao and J. P. Perdew,

J. Chem. Phys., 2003, 119, 12129–12137.22 V. N. Staroverov, G. E. Scuseria, J. Tao and J. P. Perdew, Phys.

Rev. B: Condens. Matter Mater. Phys., 2004, 69, 075102.23 J. Boettger, Phys. Rev. B: Condens. Matter Mater. Phys., 1997,

55, 11202.24 J. P. Perdew, K. Burke and M. Ernzerhof, Phys. Rev. Lett.,

1996, 77, 3865–3868.25 P. E. Blochl, Phys. Rev. B: Condens. Matter Mater. Phys., 1994,

50, 17953–17979.26 G. Kresse and D. Joubert, Phys. Rev. B: Condens. Matter

Mater. Phys., 1999, 59, 1758–1775.27 S. D. Chakarova-Kack, E. Schroder, B. I. Lundqvist and

D. C. Langreth, Phys. Rev. Lett., 2006, 96, 146107.28 S. D. Chakarova-Kack, Ø. Borck, E. Schroder and

B. I. Lundqvist, Phys. Rev. B: Condens. Matter Mater. Phys.,2006, 74, 155402.

29 G. Kresse and J. Hafner, Phys. Rev. B: Condens. Matter Mater.Phys., 1994, 49, 14251–14269.

30 G. Kresse and J. Furthmuller, Comput. Mater. Sci., 1996, 6,15–50.

31 G. Kresse and J. Furthmuller, Phys. Rev. B: Condens. MatterMater. Phys., 1996, 54, 11169–11186.

32 S. Grimme, J. Antony, S. Ehrlich and H. Krieg, J. Chem. Phys.,2010, 132, 154104.

33 S. Grimme, S. Ehrlich and L. Goerigk, J. Comput. Chem.,2011, 32, 1456–1465.

34 K. S. Novoselov, A. K. Geim, S. Morozov, D. Jiang,M. Katsnelson, I. Grigorieva, S. Dubonos and A. A. Firsov,Nature, 2005, 438, 197.

35 T. Taychatanapat, K. Watanabe, T. Taniguchi and P. Jarillo-Herrero, Nat. Phys., 2011, 7, 621.

36 A. Kumar, W. Escoffier, J. M. Poumirol, C. Faugeras,D. P. Arovas, M. M. Fogler, F. Guinea, S. Roche, M. Goiranand B. Raquet, Phys. Rev. Lett., 2011, 107, 126806.

37 M. Hasegawa and K. Nishidate, Phys. Rev. B: Condens. MatterMater. Phys., 2004, 70, 205431.

38 P. H. Tan, W. P. Han, W. J. Zhao, Z. H. Wu, K. Chang,H. Wang, Y. F. Wang, N. Bonini, N. Marzari, N. Pugno,G. Savini, A. Lombardo and A. C. Ferrari, Nat. Mater., 2012,11, 294–300.

39 X. Chen, F. Tian, C. Persson, W. Duan and N.-X. Chen, Sci.Rep., 2013, 3, 3046.

40 H. J. Monkhorst and J. D. Pack, Phys. Rev. B: Solid State,1976, 13, 5188–5192.

41 Y. Baskin and L. Meyer, Phys. Rev., 1955, 100, 544.42 A. Pisanty, J. Chem. Educ., 1991, 68, 804.43 D. Chung, J. Mater. Sci., 2002, 37, 1475–1489.44 E. E. de Moraes, M. Z. Tonel, S. B. Fagan and M. C. Barbosa,

J. Mol. Model., 2019, 25, 302.45 C. Janiak, J. Chem. Soc., Dalton Trans., 2000, 3885–3896,

DOI: 10.1039/B003010O.46 E. Voloshina, D. Usvyat, M. Schutz, Y. Dedkov and B. Paulus,

Phys. Chem. Chem. Phys., 2011, 13, 12041–12047.47 M. Rubes, P. Nachtigall, J. Vondrasek and O. Bludsky,

J. Phys. Chem. C, 2009, 113, 8412–8419.48 C. Gonzalez and E. C. Lim, J. Phys. Chem. A, 2000, 104,

2953–2957.49 A. Reyes, M. A. Tlenkopatchev, L. Fomina, P. Guadarrama

and S. Fomine, J. Phys. Chem. A, 2003, 107, 7027–7031.50 R. F. W. Bader, Chem. Rev., 1991, 91, 893–928.51 G. Henkelman, A. Arnaldsson and H. Jonsson, Comput.

Mater. Sci., 2006, 36, 354–360.52 I.-C. Yeh, J. L. Lenhart and B. C. Rinderspacher, J. Phys.

Chem. C, 2015, 119, 7721–7731.

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