Adsorption Configurations and Energies of Amino Acids on Anatase

Aug 7, 2008 - Stable adsorption configurations of several amino acid monomers on anatase (101) and (001) and rutile (110) as well as (100) were found ...
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J. Phys. Chem. C 2008, 112, 13600–13606

Adsorption Configurations and Energies of Amino Acids on Anatase and Rutile Surfaces Susan Ko¨ppen, Oliver Bronkalla, and Walter Langel* Institut fu¨r Biochemie, UniVersita¨t Greifswald, 17487 Greifswald, Felix-Hausdorff-Strasse 4, Germany ReceiVed: April 17, 2008; ReVised Manuscript ReceiVed: June 19, 2008

Stable adsorption configurations of several amino acid monomers on anatase (101) and (001) and rutile (110) as well as (100) were found in Car-Parrinello simulations of aqueous solutions. Adsorption energies were calculated by averaging over trajectories of the adsorbed and desorbed configuration, taking into account thermal fluctuations of the potential energy. The small adsorption energy of the cysteine on the stoichiometric (110) rutile surface is largely enhanced by inserting the S into an oxygen vacancy. Values for glutamic acid and lysine were significantly higher in the previously identified hydroxyl contact points (160 and 110 kJ/mol, respectively) than on the stoichiometric rutile surfaces (70 and 40 kJ/mol). Adsorption of histidine and glutamic acid on anatase largely depended on the surface orientation. Glutamic acid binds strongly to (101), whereas histidine on (001) was so stably bound that no molecular desorption was achieved. These results coincide with recent experiments on the crystallization of anatase in amino acid solutions [Durupthy, O.; Bill, J.; Aldinger, F. Cryst. Growth Des. 2007, 7, 2696]. 1. Introduction Adsorption of amino acids on different titanium dioxide surfaces plays a key role in the biocompatibility of titaniumbased implant materials, which are passivated by oxide layers.2 The majority of experimental studies on titanium dioxide refer to rutile (100) and (110) since single crystals with these surface orientations are available. Titanium dioxide films and powders often contain major amounts of anatase.2 Many studies focus on the (101) orientation of anatase.2–4 Other terminations such as (001) have lower stability but seem to be more reactive and may contribute significantly to the anatase surface chemistry.5 According to the preparation conditions, epitactic growth of anatase on SrTiO3 resulted both in perfect (1 × 1) (001) surfaces6 and in a reconstructed (1 × 4) structure for which the “ad-molecule model” (adm) was developed7 on the basis of several experimental studies.8,9 Titanium dioxide typically is in contact with aqueous solution or with water vapor in air, resulting in at least partial hydroxylation.10 The interaction of amino acids with the surface controls the crystallization of titanium dioxide in solutions at low pH values.1 Glutamic acid preferentially adsorbs on anatase (101), preventing the further growth of surfaces with this orientation, and the crystallites are mainly (101) terminated, whereas in histidine solution mainly (001) is blocked by adsorption. The powder diffraction experiments of Duruphty et al.1 did not permit any distinction to be made between perfect and reconstructed (001) surfaces on the crystallites in solution. In an earlier study of the adhesion of amino acid monomers on rutile surfaces by first-principles molecular dynamics, we found several stable adsorption configurations both in vacuum and in aqueous solution.11 Mainly three types of active groups were attaching to the surface: thiol, carboxyl, and amino groups. The high chemical activity of thiol groups in the cysteine is well-known from disulfide bridges in proteins. On the perfect TiO2 surface we found a significant increase in activity, when deprotonating the side chains. A significant amount of them is * Corresponding author. Telephone: +49 (0)3834 86 4423. Fax: +49 (0)3834 86 4475. E-mail: [email protected].

deprotonated in biological solutions, with the pK ) 8.33 being close to the physiological pH of 7.4. Carboxyl and amino groups are of major importance for the adsorption process since they occur both at the terminals of each strand and in the side chains of glutamic and aspartic acids or lysine. Zwitterions of amino acid monomers with a deprotonated carboxyl and a protonated amino group have strongly polar backbones, independently of the side chain. In contrast to that, the interaction of a peptide with the surface has to pass via side chains rather than the few NH3+ and COO- groups at the N and C terminals, respectively. The side chains differ in structure, polarity, and charge; the carboxyl and amino end groups are very active, too. Most studies on the adsorption geometry and energy of the carboxyl group on anatase3,5 and rutile surfaces12–14 refer to simple aliphatic carbonic acids such as HCOOH or the most simple amino acid, glycine.15,16 Experimental studies in a vacuum indicate that amino acids also adsorb via their backbone carboxyl groups attaching to the 5-fold titanium atoms,17 quite similar to aliphatic carboxylic acids. The adhesion of proteins to titanium dioxide was studied experimentally since it is of essential interest for tissue growth on implants.18,19 Experiments20 and calculations with amino acid monomers on the hydroxylated (100) rutile surface21 agree that the interaction of charged or polar amino acid side chains with negative terminal and positive bridging OH groups is crucial. In ref 20 the adsorption of histidine and aspartic acid was compared with nonpolar species such as alanine and phenylalanine, showing very significant differences. Recent classical molecular dynamics calculations of collagen on rutile indicate that extended proteins are attached to the surface via a small number of contact points.21,22 We described contact points between peptides and partially hydroxylated titanium dioxide at physiological pH values.21 The deprotonated side chain carboxyl group of glutamic acid had a great affinity to protonated positive surface bridging oxygens, with the O-H distance being around 1.4 Å, and the protonated amino group of lysine was attached to negative surface hydroxyls with an average N-O distance of 2.8 Å. These amino acids are major

10.1021/jp803354z CCC: $40.75  2008 American Chemical Society Published on Web 08/07/2008

Amino Acids on Anatase and Rutile Surfaces constituents of important cell adhesion proteins such as collagens. In contrast to that, Carravetta and Monti studied interactions of dipeptides of Ala-Glu and Ala-Lys with stoichiometric rutile (110) surfaces and found that mainly backbone carboxyl groups are adsorbing, whereas the lysine and glutamic acid side chains experienced little attraction to the surface.22 Adhesion strength is readily characterized by the adsorption energy, which is usually calculated from energy differences of the geometry optimized adsorbed and desorbed states.16,23,24 For glycine on (110) rutile a value of 161 kJ/mol was found if the carboxyl group only is bound to the surface. By an additional hydrogen bond from the amino group to a bridging oxygen atom (BO) the energy increased only slightly to 197 kJ/mol, which indicates that the major part of the adsorption energy is due to the carboxyl group.16 Static energy calculations refer to solvent-free “vacuum” systems.16,23 We focus on aqueous systems with completely different amino acid chemistries. This especially concerns the stabilization of zwitterions, proton transfer reactions, and the competition of the amino acid and water adsorption. The latter aspect was revealed to be important for glycine on TiO2 in wet systems,25 where H2O is replaced by the amino acid which forms a multilayer composed of intact and dissociated molecules. In ref 26, a new method for the dynamic evaluation of adsorption energies in solution was applied to hydrocarbons. Here we treat the amino acids cysteine, lysine, glutamic acid, and histidine on five titanium dioxide modifications (rutile (110) and (100), as well as anatase (101) and perfect and (1 × 4) reconstructed (001)). This complements our work on the adsorption of single amino acids and of contact points of larger peptides, and gives some first explanation for the findings by Duruphty et al.1 on controlling the antase crystallization by amino acids. The paper is organized as follows: in section 2 we briefly review our calculation method. In the section 3 the results are presented in detail, and in section 4 the implications for the mentioned earlier work are discussed. 2. Method First-principles molecular dynamic simulation according to the Car-Parrinello method was employed using the program CPMD, versions 3.9 and 3.11.27 The plane-wave basis in this approach and the resulting periodic boundary conditions are well adapted to our homogeneously filled simulation cells. Troullier-Martins pseudopotentials with a cutoff of 60 Ry28 and Becke exchange gradient correction29 were used (cf. refs 11, 24, 26, and 30). In Car-Parrinello molecular dynamics the Kohn-Sham energy EKS includes the full electronic and ion potential energies and plays the role of the potential energy in classical molecular dynamics. The scheme does not provide strict conservation of Eclassic, but of the sum of Eclassic and Ekinc. Eclassic is the sum of EKS and the kinetic energies of ion motion, and Ekinc is an artificial energy which is a result of introducing additional terms into the Lagrangian, correcting the electronic density while the ions are displaced. The inertia of this correction is determined by a fictitious mass parameter µ quoted as multiples of the electron mass. In this approach any variation of Ekinc transfers into an inverse variation of Eclassic, limiting its stability. Several factors coincided here demanding the reduction of µ from 1100 in previous work to 700 for suppressing drifts of Ekinc. The number of time steps now is considerably higher than in earlier calculations and the conservation of Eclassic has to be stricter, since small energy differences are calculated, whereas in earlier work mainly adsorption geometries were reported. In addition, it is well-known that defects such as missing surface oxygen atoms introduce additional electronic states between

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Figure 1. Plot of potential energy over time for glutamic acid on the (100) rutile surface. The inset shows the energy distributions of the adsorbed and desorbed states; the adsorption energy is the difference of the maximum positions.

conduction and valence bands and affect the energy conservation in the Car-Parrinello scheme by reducing the band gap.31 We further had to use Nose´ thermostats for ions and electrons here to keep the thermal energy constant, making initial and final states comparable, and we found that the thermostats interfered with the conservation of Ekinc. All these effects are enhanced with an increasing number of water molecules in the cell. As a consequence of the modification of µ, the time step has to be reduced to 3.5 atu (atomic time units), corresponding to 12 steps/fs. Before starting CPMD runs, the structures of the simulation cells (see below) were optimized using a simple force field (cvffaug) within the discover module of cerius2. Our standard protocol for the CPMD runs provides optimization of the electronic wave functions, stepwise heating of the ionic motion during 500 molecular dynamics steps at each of the temperatures of 40, 70 120, and 200 K and 3000 steps at 300 K. At the end of NVE runs (constant Number of atoms, Volume of the cell, and total Energy) of typically 5000-10 000 steps corresponding to 0.4-0.8 ps, the temperatures fluctuated around averages in the range of 250-350 K. For the adsorption energies we added three further Nose´ controlled stages to each run (cf. ref 26), extending the total simulation time to 3-3.6 ps: (i) A molecular dynamics (MD) run of about 0.25 ps at 300 K resulted in a stable EKS for the adsorbed stage. (ii) Constraints were imposed to three distances between the atom of the adsorbed molecule binding to the surface and three surface atoms close to it, and the set point was increased by 660 m/s for about 4-8 Å reducing the interaction of the molecule with the surfaces in most cases to a negligible final value. (iii) During a final run for at least 1.25 ps with constant constraints, the system attained in most cases a desorbed state, where the energy fluctuated but did not show significant drift. In plots of EKS as a function of time (Figure 1) desorption usually results in a steep increase followed by a smaller decrease during relaxation. The adsorption energy is evaluated as the difference between the averages before and after this step. As expected from the thermodynamics of small systems,32 the fluctuation of these energies is about 40-50 kJ/mol. The distributions of the initial and final state energies values (cf. inset in Figure 1) were fitted by two Gaussians, and the difference of the centers were taken as adsorption energies. Due to noise on the energy distributions, the uncertainty of the center positions is about 10 kJ/mol, resulting in a statistical error of about 15 kJ/mol for the quoted results (Table 1). Similar to the energies, atom-atom distances within stable initial and final configurations are fluctuating around their averages with amplitudes of about 0.2 Å, resulting in a statistical error of similar magnitude for the described geometries.

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TABLE 1: Adsorption Energies (in kJ/mol) of Four Selected Amino Acids on (110) and (100) Rutile and on (101) and (001) Anatase Surfaces configuration (110) perfect (101) perfect (110) vacancy (100) perfect

S- recombination without recombination SH vacuum, recombination (S-), recombination without recombination (SH) stoichiometric contact point

cysteine

lysine

glutamic acid

80 (H+): 160

40 (OH-): 110 deprotonated: 280 (110 + 170) protonated: 220 (130 + 90) 70 (10 + 60) no stable adsorption

histidine

40 230 (unstable)11 50 280 250 330

(101) perfect (001) perfect (001) adm

Details of the description of rutile by slabs with three layers have been given in ref 24. Surfaces with 1 × 3 and 2 × 2 bridging oxygen atoms (BO) had sizes of 6.5 × 8.9 and 5.92 × 9.19 Å2 for (110) and (100), respectively. The positions of the atoms in the bottom layer are fixed in order to mimic a rigid substrate crystal. The perfect anatase (101) surface has a size of 7.736 × 10.54 Å2 with four bridging atoms, consisting of two layers with eight Ti and 16 O atoms each. Stable slabs were obtained by fixing the z coordinates of the inner 16 atoms, i.e., eight 6-fold coordinated Ti and eight 3-fold coordinated O atoms, to their ideal values. These atoms still can move in the x-y plane, and all other atoms are fully unconstrained unless explicitly stated.26 We further set up two modifications of anatase (001). For the perfect surface a (2 × 3) geometry with six bridging atoms and a cross section of 7.55 × 11.33 Å2 was chosen, similar to ref 33. A four-layer slab of this size consists of 24 Ti and 48 O atoms. As the exact structure of the (001) surface in the experiment1 is not known, a typical (1 × 4) reconstruction known as the “ad-molecule” model (adm)9 has also been modeled. The smallest slab for adsorbing an amino acid monomer on the adm surface has (2 × 4) geometry and a surface size of 7.55 × 15.11 Å2, affording 34 Ti and 68 O atoms (Figure 2). Even though the (001) surface has a higher surface energy than (101) and is considered to be less stable,2 a small number of constraints was sufficient to stabilize our slab of more than 100 atoms; i.e., only the z coordinates of the six Ti and O atoms in the second layer from the bottom had to be fixed.

Figure 2. Models of perfect (2 × 3) and reconstructed (2 × 4) anatase surfaces with (001) orientation. The cells contain six and eight bridging atoms each, respectively. The reconstruction results in “roofs” which consist of the original bridging atoms and added TiO2 units (“ad molecules”). The roofs are separated by “valleys” with widths of three lattice constants. On top of the roofs rows of bridging atoms emerge, which are vertical to the rows on the perfect surface.

650 80

Simulation cells containing the titanium oxide slabs, the amino acid zwitterions, and explicit water molecules were built using the cerius2 program package. The amino acid was positioned above the surface with a minimal atom-atom distance of 2.5-3 Å between substrate and adsorbate. The rutile (110) and (100) and the anatase (101) and (001) cells were manually filled with 15-20, 24-27, 27-34, and 18-21 (adm 23-25) H2O molecules, respectively, and the cell heights were adjusted to the standard density of the water, with the spacings between the slabs being 15 Å (110), 17 Å (100), 15 Å (101), 12 Å (001), and 9 Å (adm), respectively. In glutamic acid, the backbone COO- group has a pKa value of only 2.134 and is considered to be always deprotonated, whereas the side chain with pKa ) 4.25 is deprotonated under physiological conditions but is partially protonated at pH values around 4 as applied in ref 1. 3. Results and Discussion In this section the adsorption (i) of cysteine on (110) rutile, (ii) of lysine and glutamic acid on stoichiometric and hydroxylated titanium dioxides, and (iii) of glutamic acid and histidine on three different anatase surfaces is discussed. 3.1. Cysteine on the (110) Rutile Surface. No stable adsorption configuration had been found for the neutral thiol group of the zwitterion pointing to the perfect surface.11 A starting configuration with the thiol proton transferred on an adjacent BO resulted in adsorption, with the deprotonated sulfur forming a bond to a surface titanium atom with a Ti-S distance of 2.4 Å, close to earlier results of 2.6 Å.11 This configuration is stable for more than 1.25 ps until desorption is induced. During opening the Ti-S bond by constraints, the anion is neutralized by a proton from a BO. The adsorption energy was still small (40 kJ/mol; cf. Table 1). This result may be compared with data from two similar runs. In a vacuum on anatase (101), recombination was also observed and the energy was 50 kJ/mol. A further run in solution on rutile (110) did not result in recombination and afforded 230 kJ/mol in energy. Obviously the proton is only very weakly bound to the bridging atom, and the transfer to the sulfur atom is exothermic by about 190 kJ/mol. Inserting the S atom into an oxygen vacancy at a position close to that of the missing bridging oxygen atom resulted in stable configurations for both protonated and deprotonated thiol groups (Figure 3). In the deprotonated case no recombination of the basic sulfur ion with protons on the bridging atoms was observed during desorption. This is remarkable, since these protons should be very acidic. In a run with protons on both of the remaining BO, the zwitterion was desorbed as anion, and the adsorption energy was about 250 kJ/mol. In two runs with

Amino Acids on Anatase and Rutile Surfaces

Figure 3. Adsorption of the neutral and the anionic cysteine on an oxygen vacancy of a (110) rutile surface by insertion of the thiol group into oxygen vacancies.

one out of two BO protonated, desorption was accompanied by a proton transfer from the NH3+ group to the S- atom. The energy of 280 kJ/mol is higher than without the recombination, which might be slightly endothermic. This is consistent with the fact that the pKa value of the -NH3+ group is higher than that of the -S-H group (10.78 vs 8.33). After adsorption of the neutral zwitterion in a vacancy, the thiol proton is positioned between sulfur and titanium atoms. The distances between S and the two Ti atoms underneath the vacancy are higher for the protonated thiol group than for the deprotonated one (3.6 vs 3.1 Å), but the proton does not sterically hinder the adsorption as was observed for NH3.35 The high interatomic distance indicates weakening of the Ti-S bond by the additional proton, but the adsorption energy of 330 kJ/ mol for this configuration is even higher than for the deprotonated group. The cysteine found a very stable bridging configuration binding to the surface not only via the sulfur but also forming a hydrogen bond from the amino group to an inplane oxygen atom. We suggested earlier that the formation of a coordinative bond between an adsorbate atom with a free electron pair and a surface Ti atom might be an important mechanism for adsorption on TiO2,26 and results for cysteine seem to support this assumption. In contrast to the insertion of a stable -S-H group into the vacancy found here, transfer of the thiol proton to the NH2 group was described in ref 11. This early run started from the genuine molecule rather than from the zwitterions, and consequently the amino group was very basic. It is astonishing that the proton transfer between sulfur and ammonia could take place in both directions. Possibly this reaction is controlled by the interaction of the two groups with the surface Ti, which tends to increase the acidity of the respective protons, and by the protonation of the remaining two bridging atoms. According to this assumption transfer of the proton from -NH3+ to -S- was triggered when the molecule was desorbed by elongating the sulfur from the surface, whereas the ammonia still saw strong interaction with it. In this transient situation the ammonia was more acidic than the thiol, and proton transfer in a sense opposite that predicted by the respective pKa values took place. 3.2. Lysine and Glutamic Acid on Stoichiometric and Hydroxylated (100) Rutile. Here adsorptions of the side chains of these amino acids on hydroxyl groups of contact points and on stoichiometric rutile (100) are compared. The N-O distance between a singly coordinated hydroxyl group on the surface and lysine was only about 2.6 Å (Figure 4b), which is close to the value of 2.8 Å in the force field calculation.21 This bond from one of the amino protons to the

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Figure 4. Adsorption geometry of lysine on (a) the stoichiometric (100) surface and (b) on the surface with a single coordinated hydroxyl group. The shorter distance of the side chain N to the hydroxyl oxygen than to the bridging oxygen (2.6 vs 3.5 Å) corresponds to the higher adsorption energy on the hydroxylated surface than on the nonhydroxylated one (160 vs 80 kJ/mol).

Figure 5. Reaction schemes and snapshots of glutamic acid on rutile (100). (a,b) On the perfect surface, the glutamic acid side chain is only hydrogen bonded to a physisorbed water molecule and the adsorption energy is low (40 kJ/mol). (c,d) On the surface with protonated bridging oxygen, glutamic acid binds directly to the surface and a higher adsorption energy of 110 kJ/mol was observed. Within a few picoseconds a proton flips from the BO to the functional group.

hydroxyl O was stable for about 1.25 ps until desorption was induced by elongating the distances between the lysine N and two Ti atoms and an O atom in the surface, affording an energy of 160 kJ/mol. On the non-hydroxylated surface the side chain of lysine forms two hydrogen bonds to bridging oxygen and to molecularly adsorbed water (Figure 4a). The distance of the lysine N to the bridging oxygen increases from initially 2.8 Å to 3.5 Å after 0.6 ps, being stable until desorption is induced, and the adsorption energy was 80 kJ/mol. Thus the N-O distance was considerably longer and the adsorption energy was smaller by a factor of 2 than on the hydroxylated surface. The side chain of glutamic acid is not adsorbed directly on the stoichiometric surface but forms a hydrogen bond to a water molecule (Figure 5b), which is adsorbed on an adjacent 5-fold coordinated titanium atom. In two runs for this system with slightly different starting geometries, we saw in one case proton transfer along the hydrogen bond after 0.8 ps (Figure 5a) and desorption of the neutral zwitterions and in the second run adsorption with stable hydrogen bonding (Figure 5b). Probably the acidities of the adsorbed water and of the side chain carboxyl group are very close to each other. As the carboxyl group has a pKa ) 4.25,34 which is significantly lower than for free water molecules, this means that the adsorbed water molecules are more acidic than the free ones. We evaluated the adsorption energy for the system in which no proton transfer occurred and found a value as low as 40 kJ/mol.

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TABLE 2: Protonation State of the Anatase Surfaces for Modeling an Acid Environment bridging atoms (101) (001) perfect (001) adm

total

protonated

4 6 8

3 4 5

A similar but much faster proton transfer was observed for the side chain pointing toward a protonated bridging atom (Figure 5d), neutralizing the carboxyl group within a few femtoseconds. Probably the protonated BO has an even lower pKa than adsorbed water or the COO- group. The resulting configuration (Figure 5c) is stable for about 1.1 ps until desorption is induced. The adsorption energy of 110 kJ/mol is much higher than on the stoichiometric surface. This proton transfer as revealed by first-principles molecular dynamics is not seen in force field simulations with predefined bonds, and indicates an unexpectedly high acidity of the protonated bridging oxygen. Experiments show that the pKa of this protonation equilibrium is lower than the point of zero charge of the surface,36 which scatters between 4.2 and 6 in various measurements.37 3.3. Glutamic Acid and Histidine on Anatase Surfaces. Adhesion of histidine and glutamic acid on anatase (101) and (001) was probed here for comparison with the crystallization study by Duruphty et al.1 Our calculations provided protonrich environments corresponding to the low pH values employed in the experiments, and a major part of the 2-fold coordinated oxygen atoms on the surfaces is protonated (see Table 2). The total charge of the system was adjusted to 0 by Cl- counterions. On (101), the deprotonated side chain of the glutamic acid zwitterion forms a hydrogen bond to one of three protons on BO. The H atom nearly spontaneously flips after 0.19 ps from the surface to the carboxyl oxygen. The second side chain oxygen is hydrogen bonded to a molecularly adsorbed water as on stoichiometric (100) rutile, and a backbone oxygen atom is bonded to a surface titanium atom. As three out of the four reactive oxygen sites of glutamic acid are involved, the adsorption geometry is very stable, and the total adsorption energy is as high as 280 kJ/mol. Desorption took place in two steps. Detaching the backbone carboxyl group first afforded 110 kJ/mol. After relaxing the system for 1.25 ps, the desorption of the protonated carboxyl group from the deprotonated BO was induced by pulling the backbone for further 4 Å. The BO next to the deprotonated one was displaced in the +z direction by 0.41 Å and did not relax during the remaining simulation time of 1.2 ps. The energy of 170 kJ/mol is considerably higher than the corresponding value of 110 kJ/mol on rutile (100), where the surface was not affected at all. Protonation of the side chain only had a moderate influence on the adsorption geometry and energy. The OH is oriented away from the surface, and the carbonyl O forms a hydrogen bond to a surface proton, as in the COO- group. The desorption of backbone and side chain afforded 130 and 90 kJ/mol, respectively, and the total adsorption energy was 220 kJ/mol, which is 60 kJ/mol lower than for amino acid with the deprotonated side chain. This neutral zwitterion also was positioned on a perfect (001) surface with four out of six bridging atoms protonated. As on anatase (101), the side chain carboxyl group acts as an acceptor and forms a hydrogen bond to a protonated bridging oxygen, and the backbone COO- is bonding to a surface titanium atom with a stable Ti-O distance around 2 Å. Desorption again proceeds in two consecutive steps. The backbone desorbs first since the Ti-OCO bond is opened by constraints. No protonation of the carboxyl group is observed owing to its low pK value. Next to

Figure 6. Comparison of adsorption geometries of glutamic acid (a-c) and histidine (d-f) on the (101) perfect and reconstructed (001) anatase surfaces. Glutamic acid adsorbs in a bridging configuration with backbone and side chain at the (101) and at the perfect (001) surface. Histidine is not able to find a stable adsorption geometry with side chain and backbone at (101) but strongly adsorbs at the (001) surface in this configuration. At the adm (001) surface neither for glutamic acid nor for histidine the bridging configuration was found.

TABLE 3: Deformation of Glutamic Acid and Histidine Molecules during Adsorption: Distances between the Two Carboxyl C Atoms and between Carboxyl C and Imidazole N1, Respectively

free (101) (001)

carboxyl C-C distance/Å in Glu

carboxyl C-N1 distance/Å in His

4.6 4.3 (bridging configuration) 3.2 (bridging configuration)

3.8 3.8 (imidazole end free) 3.1 (bridging configuration)

the adsorption site, a BO at nearly its theoretical position is displaced out of the surface by 0.85 Å and one of its two Ti-O bonds is broken. Its restoration is inhibited by adsorption of a water molecule at the unsaturated Ti. We speculate that this state of the surface is energetically favorable with respect to the initial configuration and results in an energy gain compensating in part the actual desorption energy. This would explain the very low energy input of only 10 kJ/mol for this step. In a second step, the side chain is desorbed, keeping its proton. The added energy of 60 kJ/mol corresponds to the rupture of the hydrogen bond. The total adsorption energy thus amounts to about 70 kJ/mol and is significantly lower than on (101). On both perfect anatase surfaces side chain and backbone carboxyl groups of glutamic acid are adsorbed on adjacent surface sites in bridging configurations (Figure 6). The intramolecular distance of the carboxyl C atoms in free relaxed glutamic acid is 4.6 Å as compared to 4.3 Å at (101) and 3.2 Å on perfect (001), respectively (see Table 3). The value on (101) is very close to that in the free molecule, but on (001) the bridging configuration results in deformation of the molecule tending to reduce the stability of the adsorbed configuration.

Amino Acids on Anatase and Rutile Surfaces On the adm surface, the backbone carboxyl group does not form a bond to a titanium atom but both of its oxygen atoms are hydrogen bonded to protons of adjacent BO on top of the added TiO2 units. After 0.2 ps a proton flips to the backbone carboxyl oxygen atom. Within a further 0.2 ps the hydrogen bonds finally break and the group desorbs. This indicates that the bridging atoms on the ad molecule are extremely acidic and in equilibrium mostly deprotonated. The situation is different for the BO of the valley between the added molecules, to which the protonated side chain is hydrogen bonded with one oxygen atom, being an acceptor as on perfect (001). Even though the side chain has a significantly higher pK than the backbone, no recombination is observed, and the hydrogen bond is stable. In histidine on anatase (101), only the backbone carboxyl group forms a stable hydrogen bond to one of the hydrogens on a bridging atom. By steric reasons a bridging geometry as for glutamic acid is impossible, and the imidazole side chain is not binding to the surface. A hydrogen bond of the side chain to BO atoms in the same row as the carboxyl group would introduce major distortion to the molecule, and adsorption of backbone carboxyl group and side chain imidazole on two neighboring rows of BO atoms is not possible: the distance of 5.6 Å between these rows is too high. The imidazole ring orients parallel to the surface plane, and the interaction with it is weak, similar to results for benzene on TiO2.38 Consequently, no rupture of any Ti-O bond in the surface was observed. Instead, a head-to-tail hydrogen bond between the carboxyl group of the molecule and the imidazole group of its image in the adjacent cell is formed. Desorption was induced by increasing the distance constraints of one of the carboxyl oxygen atoms to three surface Ti atoms. The hydrogen bond between molecule and image is broken, and a transient hydrogen bond between an imidazole NH and an in-plane O indicates some interaction between ring and surface. The adsorption energy of 290 kJ/mol is very high for a single carboxyl group, and we speculate that the interaction between molecule and image stabilizes the adsorbed state. In the small system studied here, this is an artifact, but it might indicate the possibility of forming stable extended layers in larger systems. A perfect (001) surface with four out of six protonated bridging atoms was generated for histidine adsorption. One oxygen atom of the backbone carboxyl group is bonded to surface titanium, whereas the second one forms a hydrogen bond to a proton on a BO. In contrast to the (101) surface, the imidazole is stabilized by two hydrogen bonds between its NH group and bridging oxygen atoms with distances of 2.2 and 1.6 Å, respectively. The N acts both as donor binding to an unprotonated and as acceptor for an adjacent protonated BO. After 1.25 ps the proton flips to the nitrogen, and N-H and O-H distances of 1.04 and 1.7 Å, respectively, are found (Figure 7). In this configuration the (original) donor BO is shifted in the +z direction of about 0.5 Å with respect to the two Ti atoms to which it is bound, with the Ti-Ti-O angles increasing from 30° to 60°. An attempt to force desorption of this molecule by elongating the distance between a carboxyl O and a surface Ti resulted in a torsion of the COO- group along the axis of its C-CR bond and finally in rupture of the latter, affording an addition of 650 kJ/mol to the potential energy. A CO2 molecule was desorbed from the surface, and the decarboxylated CR was saturated by proton transfer from a molecularly adsorbed H2O. A Ti-O bond in the surface which was broken during desorption recombines afterward, since the large imidazole group is still adsorbed and hinders the adsorption of a further water molecule on the unsaturated titanium atom.

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Figure 7. BO-BO distance of 3.6 Å is the prerequisite for a double coordinated adsorption of the imidazole group of histidine on stoichiometric (001) anatase. The nitrogen atom is acceptor and donor for hydrogen bonds to a non-protonated and a protonated BO, respectively. After 1.25 ps, the proton flips from the latter O to the N atom and the O moves out of the surface opening one of its two Ti-O bonds.

Even if we cannot exclude that breaking the C-CR bond is an artifact of our special dissociation constraints, decarboxylation is a well-known dissociation channel of amino acids. In TPD and XPS experiments on proline on rutile surfaces mainly dissociative desorption was observed, since the molecule is strongly bonded to the surfaces and dissociates before desorbing at 500-550 K,39,40 and the splitting of the C-CR bond is proposed as one out of two dissociation channels.41 On the (1 × 4) reconstructed (001) surface, the backbone of histidine and the -NH group of the side chain are initially hydrogen bonded to the protonated BOad on top of the added TiO2 and to a BOreg on the regular surface, respectively. After 0.7 ps, the -NH · · · BOreg hydrogen bond breaks and the distance increases to a stable value of 3 Å. The adsorption energy of only 80 kJ/mol for this configuration corresponds to a much weaker adsorption than on the perfect (001) surface. Histidine can attain a side chain-backbone bridging configuration on the stoichiometric (001) surface without major deformations of the molecule, with the intramolecular distance between carboxyl C and imidazole N1 being reduced from 3.8 Å in the relaxed free molecule to 3.1 Å (see Table 3). In the bridging configuration the C-N1 distance is determined by the spacing between adjacent rows of BO, which is 3.6 Å on (001) (Figure 7). On the (101) surface the corresponding BO-BO distance is about 5.6 Å, and no bridging configuration is attained. The C-N1 distance probably had to be around 5 Å, and we assume that stretching the molecule by about 1.2 Å seems to be unlikely. On the reconstructed surface, the BOad is reactive and forms a strong hydrogen bond to the histidine carboxyl. The imidazole ring is attracted by the perfect surface between the ad molecules, but once the carboxyl group is trapped, it could not form stable bonds to bridging atoms by steric reasons because the distance between the BOad and the nearest BOreg is 5.3 Å. 4. Conclusion It had been shown earlier that the thiol group of cysteine preferentially adsorbs in oxygen vacancies. This has been confirmed quantitatively; the adsorption energies are around 300 kJ/mol in the vacancies vs less than 50 kJ/mol on the perfect surface. In contrast to that, the presumed high reactivity of deprotonated thiol was not established. On the perfect surface only the anion is adsorbed in our calculation but has an adsorption energy of only 40 kJ/mol, whereas in the vacancy the adsorption energy of the anion probably is even lower than of the neutral molecule. Calculations sampled a number of different configurations for the adsorption of carboxyl and amino groups. This limited number of runs does not give a complete picture, but we try to deduce characteristic reaction pathways. From force field

13606 J. Phys. Chem. C, Vol. 112, No. 35, 2008 simulations we derived the concept of contact points, saying that peptides are adsorbed by the specific interaction of a few charged side chains with oppositely charged surface hydroxyl sites only, whereas on non-hydroxylated surfaces the interaction is very small. Here this model is confirmed by Car-Parrinello simulations of the monomers on TiO2 in detail; the adsorption energies of lysine and glutamic acid in contact points are about a factor of 2 higher than those of links of these side chains to the stoichiometric (100) rutile surfaces. Force field simulations indicated only small interaction of amino groups with the stoichiometric surface. In the CarParrinello calculation the adsorption energies of lysine both on the stoichiometric and on the hydroxylated surfaces with contact points21 were even higher than the corresponding values of glutamic acid. For the carboxyl groups of glutamic acid we obtain a more detailed picture than in previous force field calculations, where mainly electrostatic interactions with the surface were seen. Here, the reactions of the side chain are systematically different from those of the backbone. In most cases a backbone COOoxygen forms a coordinative bond to a 5-fold coordinated surface Ti, without interference by adsorbed water, and independently of pH value and surface structure. The side chain COO- group binds to protons from the surface or from molecular adsorbed H2O, and proton transfer reactions occur, which cannot be seen in a force field calculation. For the observed specific termination of anatase crystals by (101) or (001) surfaces, we suggest two explanations. The amino acid may stick with high adsorption energy to one of the two surfaces and block further crystal growth on it. This is clearly the case for glutamic acid, which has nearly 4 times higher adsorption energy on (101) than on (001) and thus stabilizes the (101) surface on crystallites. For histidine we cannot quantify the difference because on (001) no molecular desorption was seen. Monomers can attain a special adsorption configuration, where both the side chain and backbone of an amino acid are adsorbed to the surface. Energetically such bridging configurations are highly favored with respect to single point adsorption of one group only. On (001) a very stable bridging configuration is obtained with both side chain and backbone binding to the surface, whereas by steric reasons only single point adsorption is possible on (101). We attribute the stabilization of (001) by histidine to this difference. In many cases opening of in-plane Ti-O bonds was induced either during the adsorption or during desorption. This often was irreversible, with no closing being achieved after desorption, but obviously this did not correlate with crystallization. The affinity of the two amino acids to the reconstructed (001) surface was very weak. Glutamic acid was not adsorbed at all, and histidine with only 60 kJ/mol. We assume, however, that under the conditions applied in the experiments by ref 1, no (1 × 4) reconstruction is obtained. If (001) was so strongly relaxed, no further crystallization would have been possible on these surfaces. Acknowledgment. We gratefully acknowledge funding of our work by the Deutsche Forschungsgemeinschaft (La 700/71, La 700/8-1), access to the packages CPMD 3.9 and 3.11 by J. Hutter, P. Ballone, M. Bernasconi, P. Focher, E. Fois, St. Goedecker, D. Marx, M. Parrinello, and M. Tuckerman, MPI

Ko¨ppen et al. fu¨r Festko¨rperforschung and IBM Zurich Research Laboratory, and assistance during some of the calculations by S. Klatt. Fruitful discussions with Joachim Bill, MPI fu¨r Metallforschung, Stuttgart, incited the simulations in section 3.3. The calculations were in part performed in the university computing centers in Rostock and Greifswald. References and Notes (1) Durupthy, O.; Bill, J.; Aldinger, F. Cryst. Growth Des. 2007, 7, 2696. (2) Diebold, U. Surf. Sci. Rep. 2003, 48, 53. (3) Vittadini, A.; Selloni, A.; Rotzinger, F. P.; Gra¨tzel, M. J. Phys. Chem. B 2000, 104, 1300. (4) Gong, X.; Selloni, A. J. Catal. 2007, 249, 134. (5) Gong, X.; Selloni, A.; Vittadini, A. J. Phys. Chem. B 2006, 110, 2804. (6) Herman, G. S.; Gao, Y.; Tran, T. T.; Osterwalder, J. Surf. Sci. 2000, 447, 201. (7) Lazzeri, M.; Selloni, A. Phys. ReV. Lett. 2001, 87, 266105. (8) Liang, Y.; Gan, S.; Chambers, S. C.; Altman, E. I. Phys. ReV. B 2001, 63, 235402. (9) Herman, G. S.; Sievers, M. R.; Gao, Y. Phys. ReV. Lett. 2000, 84, 3354. (10) Jones, F. H. Surf. Sci. 2001, 42, 75. (11) Langel, W.; Menken, L. Surf. Sci. 2003, 538, 1. (12) Ahdjoudj, J.; Minot, C. Catal. Lett. 1997, 46, 83. (13) Rotzinger, F. P.; Kesselman-Truttmann, J. M.; Hug, S. J.; Shklover, V.; Gra¨tzel, M. J. Phys. Chem. B 2004, 108, 5004. (14) Ka¨ckell, P.; Terakura, K. Surf. Sci. 2000, 461, 191. (15) Qiu, T.; Bateau, M. A. J. Colloid Interface Sci. 2006, 303, 229. (16) Ojama¨e, L.; Aulin, C.; Pedersen, H.; Ka¨ll, K. J. Colloid Interface Sci. 2006, 296, 71. (17) Schmidt, M.; Steinmann, S. G. Fresenius J. Anal. Chem. 1991, 341, 412. (18) Spencer, N. D.; Textor, M. In Materials in Medicine; Speidel, M. O., Uggowitzer, P. J., Eds.; vdf Hochschulverlag: Zurich, 1998. (19) Roessler, S.; Born, R.; Scharnweber, D.; Worch, H.; Sewing, A.; Dard, M. J. Mater. Sci.: Mater. Med. 2001, 12, 871. (20) Tran, T. H.; Nosaka, A. Y.; Nosaka, Y. J. Phys. Chem. B 2006, 110, 25525. (21) Ko¨ppen, S.; Ohler, B.; Langel, W. Z. Phys. Chem. 2007, 221, 3. (22) Carravetta, V.; Monti, S. J. Phys. Chem. B 2006, 110, 6160. (23) Bates, S. P.; Kresse, G.; Gillan, M. J. Surf. Sci. 1998, 409, 336. (24) Langel, W. Surf. Sci. 2002, 496, 141. (25) Lausmaa, J.; Lo¨fgren, P.; Kasemo, B. J. Biomed. Mater. Res. 1999, 44, 217. (26) Ko¨ppen, S.; Langel, W. Phys. Chem. Chem. Phys. 2008, 10, 1907. (27) Marx, D.; Hutter, J. Ab-initio Molecular Dynamics. Theory and Implementation. In Modern Methods and Algorithms in Quantum Chemistry; NIC Series, Vol. 1; Forschungzentrum Juelich: Juelich, 2000. (28) Troullier, N.; Martin, J. Solid State Commun. 1990, 74, 613. (29) Becke, A. Phys. ReV. A 1988, 38, 3098. (30) Langel, W. Surf. Sci. 2006, 600, 1884. (31) Pastore, G.; Smargiassi, E.; Buda, F. Phys. ReV. A 1991, 44, 6334. (32) Heermann, D. W. Computer simulations in theoretical physics; Springer: Berlin, 1986. (33) Vittadini, A.; Selloni, A.; Rotzinger, F. P.; Gra¨tzel, M. Phys. ReV. Lett. 1998, 81, 2954. (34) Nelson, D. L.; Cox, M. M. Lehninger Biochemie, 3rd ed.; Springer: Berlin, 2001. (35) Pang, C. L.; Sasahara, A.; Onishi, H. Nanotechnology 2007, 18, 044003. (36) Giacomelli, C. E.; Avena, M. J.; DePauli, C. P. Langmuir 1995, 11, 3483. (37) Kosmulski, K. Chemical Properties of Material Surfaces; Marcel Dekker: Basel, 2001. (38) Reiss, S.; Krumm, H.; Niklewski, A.; Staemmler, V.; Wo¨ll, Ch. J. Chem. Phys. 2002, 116, 7704. (39) Fleming, G. J.; Idriss, H. Langmuir 2004, 20, 7540. (40) Fleming, G. J.; Adib, K.; Rodriguez, J. A.; Barteau, M. A.; Idriss, H. Surf. Sci. 2007, 601, 5726. (41) Soria, E.; Colera, I.; Roman, E.; Williams, E. M.; de Segovia, J. L. Surf. Sci. 2000, 451, 188.

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