Letter pubs.acs.org/JPCL
Probing the Nature of Charge Transfer at Nano−Bio Interfaces: Peptides on Metal Oxide Nanoparticles Pilarisetty Tarakeshwar,*,† Julio L. Palma,‡ Gregory P. Holland,§ Petra Fromme,† Jeffery L. Yarger,† and Vladimiro Mujica† †
Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, United States Center for Biosensors and Bioelectronics, Biodesign Institute, Arizona State University, Tempe, Arizona 85287-5001, United States § Department of Chemistry and Biochemistry, San Diego State University, 5500 Campanile Drive, San Diego, California 92182-1030, United States ‡
S Supporting Information *
ABSTRACT: Characterizing the nano−bio interface has been a long-standing endeavor in the quest for novel biosensors, biophotovoltaics, and biocompatible electronic devices. In this context, the present computational work on the interaction of two peptides, A6K (Ac-AAAAAAK-NH2) and A7 (Ac-AAAAAAA-NH2) with semiconducting TiO2 nanoparticles is an effort to understand the peptide−metal oxide nanointerface. These investigations were spurred by recent experimental observations that nanostructured semiconducting metal oxides templated with A6K peptides not only stabilize large proteins like photosystem-I (PS-I) but also exhibit enhanced charge-transfer characteristics. Our results indicate that α-helical structures of A6K are not only energetically more stabilized on TiO2 nanoparticles, but the resulting hybrids also exhibit enhanced electron transfer characteristics. This enhancement can be attributed to substantial changes in the electronic characteristics at the peptide-TiO2 interface. Apart from understanding the mechanism of electron transfer (ET) in peptide-stabilized PS-I on metal oxide nanoparticles, the current work also has implications in the development of novel solar cells and photocatalysts. SECTION: Physical Processes in Nanomaterials and Nanostructures
B
nanostructured semiconductors is interesting because a small α-helical peptide was found to aid the functioning of PS-I both as a light-harvester and charge separator in solar cells.10 Although the exact role of the peptide in enhancing the photocurrent of PS-I adsorbed on nanostructured ZnO or TiO2 is not known, it is intriguing that a small cationic peptide surfactant Ac-AAAAAAK-NH2 (A6K) consisting of six alanines and a lysine at the amidated C-terminus can play such a vital role in both stabilizing dry PS-I on nanostructured semiconductors and enhancing its photocurrent.10,11 Since there is a parallel between our recent work in understanding the role of semiconducting oxide nanoparticles in enhancing the Raman activities of molecules adsorbed on them12−15 and the characteristics of peptide−metal oxide nanointerfaces,16−19 we thought it would be interesting to investigate them. In our work on surface enhanced Raman scattering (SERS) on semiconducting nanoparticles, we have shown that the enhancement of Raman activities arises from a large increase in polarizability due to charge transfer from the molecule to the semiconducting nanoparticle.14,15 Furthermore,
iological systems provide useful cues in directing the assembly of nanoscale components into controlled and advanced structures. Most of the early efforts were predominantly based on using the exquisite recognition capabilities of DNA and RNA in the design and development of novel selfassembled structures.1−6 However, recent studies have shown that polypeptides could be employed as templates in directing the assembly of π-conjugated oligomers.5 Interestingly, the characteristics of these biologically templated oligomers were found to depend on the size, geometry, and the electronic properties of the biological template.5 It has been shown in previous photophysical studies of photoinduced electron transfer that chromophores placed at different locations of a α-helical peptide could be used to investigate distance-dependent excitonic coupling.5,7−9 These couplings can also be investigated by employing different sizes of α-helical peptides as bridges between the chromophores.5,7−9 The hierarchical self-assembly of α-helical peptides also leads to the formation of 3D organogels with high dielectric constant. The unique properties of these peptide-based organogels has recently been harnessed in the development of novel organic bulk-heterojunction photovoltaic devices.5 In this context, a recent study of dry photosystem-I (PS-I) stabilized by surfactant peptides and self-assembled on © XXXX American Chemical Society
Received: September 2, 2014 Accepted: October 3, 2014
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Figure 1. Schematic of the (Au electrode)−Peptide−{TiO2 cluster}−(Au electrode) model used to calculate the electron transfer rates reported in this work.
The MSINDO-optimized structures were used as inputs for calculations carried out at the density functional level of theory (DFT) using the Becke gradient-corrected exchange functional and Lee−Yang−Parr correlation functional with three parameters (B3LYP) and the 6-31G* basis set.27−31 The Gaussian suite of programs were employed to carry out the DFT calculations.32 Full geometry optimizations were followed by an evaluation of the vibrational frequencies for some of the smaller cluster complexes. Given the importance of the solvent, the calculations were carried out in water wherein the solvent effects were modeled using the polarizable continuum (PCM) model.33−35 Several recent studies carried out by us on systems containing TiO2 clusters reveal that calculations carried out at this level of theory yield geometries and vibrational frequencies in good agreement with experimental infrared and Raman spectra.13−15 The main objective of the current work was to understand the role of the structure and properties of the peptide−(TiO2) cluster interface on the observed ET rates. Therefore, the relation between the low voltage conductance of a molecular system connected to two metal electrodes and the electrontransfer rate of the same molecular system in solution, was used to calculate the ET rate.20 Under certain assumptions, Marcus theory can be reformulated to yield the following connection between the molecular conductance and the ET rate (kET).20
we have delineated the specific role of factors like metal oxide composition, nanoparticle size, solvent, and pH on the observed Raman activities.14 One of the interesting results obtained in the course of our work is that an increase in the positive charge of the hybrid molecule-metal oxide nanoparticle system preferentially lowers the energies of the bands of the metal oxide.14 Consequently, the highest occupied molecular orbital (HOMO) lies much closer to the conduction band edge of the metal oxide, and this leads to an enhancement of the Raman activities due to enhanced charge transfer.14 In very recent work, we used the relationship between zero-bias molecular conductance and electron transfer (ET) rate to show that the magnitude of Raman enhancement of molecules adsorbed on semiconducting nanoparticles can be correlated to the ET rate from the molecule to the semiconducting nanoparticle.15 Given the recent interest in biophotovoltaic devices and the necessity of understanding the role played by small polypeptide chains adsorbed on semiconducting nanoparticles in directing and controlling rates of electron transfer,5,10 we directed our attention to investigating the nature of charge transfer at peptide−metal oxide nanointerfaces.16−19 Our focus is to examine the role of both peptide secondary structure and the presence of cationic amino acids in the peptide in influencing both the binding energetics and the interfacial electronic characteristics. In order to address these twin issues, we carried out calculations on the A6K and A7 (Ac-AAAAAAA-NH2) peptides. Though these small peptides exhibit an α-helical secondary structure, we also carried out calculations on the corresponding extended structures. Given the relation between electron transport at low bias in a junction and nonadiabatic ET,20,21 we then calculated the conductance of the peptide− metal oxide nanointerfaces. Apart from providing an alternative to using the classical Marcus theory to calculate the ET rates, this approach also allows us to incorporate the role of quantum effects and provides another method to determine the rates of electron transfer via conductance measurements. We initially carried out calculations on both the bare peptides and the peptide−metal oxide cluster complexes using the semiempirical molecular orbital MSINDO method.22 This method, which is based on the intermediate neglect of the differential overlap (INDO) approximation has been extensively used in calculations of several metal oxide containing systems.23−25 Calculations were also carried out using the conductor-like screening model (COSMO) to take into account the effect of a water solvent.26 In the gas-phase, the adsorption of extended structures of peptides on the TiO2 cluster is energetically more stabilized than the adsorption of the corresponding α-helical structures. However, the energetic trend is reversed when calculations are carried out in the presence of a water solvent.
kET =
2π ρFC g ℏg0 ρA ρD
In the above equation, g0 is the quantum of conductance, ρFC is the Franck−Condon weighted density of states, ρD/A is the density of electronic states at the Fermi level for each electrode, and g is the Landauer conductance. To evaluate the conductance, the DFT-optimized structures of the hybrid peptide−TiO2 cluster complexes were initially tethered between two gold electrodes (Figure 1), and the electronic transport properties, based on the Landauer− Büttiker formalism, were obtained from TRANSIESTA.36−38 The transport calculations were carried out using a local density approximation and a single-ζ basis set.36 The density matrix was obtained from the Green’s function by carrying out 30 points of contour integration on the imaginary plane. A 300 Ry energy cutoff for the grid mesh was used, to have convergence in the transmission values. The transmission coefficients at zero bias T, is related to the conductance (g) through the relation (g = g0T). In all the transmission calculations, the connection to the right gold electrode was mediated through the oxygen atom of the metal oxide cluster because it shows a higher transmission value than the corresponding Au−Ti motif (Figure 1).15 The attachment of peptides containing amino acids like lysine (K) with positively charged NH3+ groups to metal oxide clusters can be mediated either through the cationic side-chain or the negatively charged C-terminus carboxyl group of the 3556
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peptide. Although earlier Raman spectral measurements and work carried out by us on the attachment of positively charged dopamine to small TiO2 clusters indicated that the binding is not mediated through the cationic side-chain of dopamine,14 we carried out calculations on the binding of bare lysine to (TiO2)10 clusters. The B3LYP/6-31G* calculations carried out in the presence of a water solvent indicated that peptide−metal oxide binding mediated through the cationic side-chain is nearly 14 kcal/mol higher in energy than that mediated through the negatively charged carboxyl group. Furthermore, since the ET rate is nearly 3 orders of magnitude larger when the binding is mediated through the carboxyl group, calculations of the larger peptide-metal oxide clusters were carried out on structures exhibiting this binding motif. Our results indicate that the binding of α-helical structure of A6K to a TiO2 cluster is nearly 19.4 kcal/mol energetically more stable than the binding of an extended structure of A6K (Figure 2, Table 1). It can be seen that, compared to an isolated peptide, the binding to the metal oxide nanoparticle stabilizes the α-helical structure by an additional 2.2 kcal/mol (Table 1). This enhanced energetic stabilization is accompanied by an increase in the magnitude of the dipole moment of A6K from 29D to 42D. Calculations of the binding of A6K to a larger Ti36O90H36 cluster also indicate a qualitatively similar trend (Figure S1, Supporting Information). In the complex associated with the α-helical structure of A6K and TiO2, the Ti atom of the metal oxide cluster is 2.540 Å away from the carboxyl carbon of the peptide. However, in the corresponding complex of extended structure of A6K, the Ti atom is 2.579 Å away from the carboxyl carbon of the peptide. The fact that this small increase in the intermolecular peptide− TiO2 distances leads to a dramatic change in the electronic characteristics of the interface can be noted from the profiles of the electrostatic potential mapped on the electron density in Figure 2. In contrast to the (TiO2)10 complex of the extended structure, the complex of α-helical A6K exhibits an enhanced electrostatic potential at the interface. The fact that this enhanced electrostatic potential leads to enhanced electron transfer characteristics can also be inferred from our earlier work on electrode−molecule interfaces.39−41 Before we discuss the ET data, it is important to note that the method employed for estimating ET rates in this work is valid under the assumption that both ET and conductance occur via a tunneling mechanism.20 This is the underlying physical reason why the electronic factor is approximately the same in both Marcus theory and the expression for conductance.20 Extensive work over the last several decades clearly shows that ET in small peptides is predominantly due to tunneling.42−48 While the solvent plays a key role in ET via the reorganization energy, the relative magnitude of ET rates arising from changes in the electronic structures of the molecular bridge can be estimated through gas phase conductance calculations at the molecular geometries that are obtained in the presence of the solvent.44 These considerations are relevant, because solvent effects have been found to be important in the energetic stabilization of α-helical structures. While this is always the case for the stabilization of a particular conformation of a biological molecule, it has been found in some extreme cases that even at room temperatures, the presence of a solvent has a negligible effect on ET mediated through tunneling mechanisms.48 The solvent however influences the ET mechanism and the corresponding rate,
Figure 2. B3LYP/6-31G* optimized structures of the (TiO2)10 complexes of (a) α-helical A6K and (b) extended A6K. Contour plots (isovalue: 0.005 au) of electrostatic potential mapped on the electron density of the (TiO2)10 complexes of (c) α-helical A6K and (d) extended A6K.
Table 1. Calculated Relative Energies and Electron Transfer Rates of Different Structural Forms of A7, A6K, and the (TiO2)10, Ti36O90H36 Complexes of A6K kET (s−1)
ΔE (kcal/mol)a system
α-helix
extended
α-helix
extended
A7 A6K A6K−(TiO2)10 A6K−Ti36O90H36
0 0 0 0
9.8 17.2 19.4 8.1
8.6 × 105 2.0 × 106 1.2 × 107
2.9 × 101 1.7 × 101 2.4 × 101
a
The structures and energies for the A6K and A6K−(TiO2)10 were obtained from geometry optimizations carried out at the B3LYP/631G* level of theory, those for A6K−Ti36O90H36 were obtained at the MSINDO level.
when measurements are carried out in high-dielectric solvents at low temperatures.48 3557
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of recent studies on the use of α-helical systems as spin filters in the development of chiral-based spintronic devices,49−52 and to clarify the origin of the enhancement of the spin−orbit interaction in intramolecular electron transfer,52 which is essential for the filtering effect to occur. It is envisioned that the method described in the current work would be combined with experiments wherein nuclear magnetic resonance (NMR) techniques are used to determine the binding modes and conformational structure of peptides on metal oxide nanoparticle surfaces. Work in this direction is currently in progress in our laboratories.
With this background, it can be noted from Table 1, that αhelical structures are more conducive to electron transfer with the ET rates (kET) being nearly 6 orders of magnitude larger than those of the corresponding extended structures. It is interesting to note that the calculated rates are of nearly the same order of magnitude as those observed in experimental measurements of ET in α-helical peptides.8,44 It can also be seen that the A6K-(TiO2)10 complexes exhibit higher ET rates than the corresponding bare peptides. In the optimized structure of the α-helical A6K-(TiO2)10 complex, the lysine (K) side chain forms an hydrogen bond to the peptide backbone. To examine the influence of this hydrogen bond on the calculated ET rates, we also carried out a calculation on a (TiO2)10 complex of α-helical A6K, wherein the lysine (K) side-chain does not form an hydrogen bond with the peptide backbone (Figure S2, Supporting Information). The calculated ET rate (kET = 1.3 × 107 s−1), for this structure indicates that the formation of a side-chain/backbone hydrogen bond in the lowest-energy optimized structure leads to little changes in the calculated rates. In recent work, we have shown that the magnitude of bond currents involving the interfacial atoms is a useful indicator of ET characteristics.15 It can be seen from (Figure S3, Supporting Information) that the magnitude of bond currents at the peptide-(TiO2)10 interface are much higher for the (TiO2)10 complex of α-helical A6K. While the preceding data seem to indicate that certain peptide structural motifs are more conducive to binding and ET, it is interesting to examine the role of the cationic amino acid (K) in influencing both the energies and the electron transfer rates. Calculations carried out on the related A7 peptide, wherein the lysine (K) is replaced by alanine (A), indicate that α-helical structures are also stabilized in case of A7. While the ET rates of the bare A7 peptide is only an order of magnitude smaller that of the corresponding A6K peptide, the calculated (kET = 1.1 × 104 s−1) for the A7−(TiO2)10 complex indicates that the absence of a cationic (K) residue leads to a decrease in ET rate by nearly 3 orders of magnitude. Given the importance of the presence of K on the ET rates, it is useful to examine how an increase in the alanine (A) content would influence the observed rates. It can be seen from Figure 3, that beyond four residues, the size of the peptide has little influence on the observed ET rate.
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ASSOCIATED CONTENT
S Supporting Information *
MSINDO-optimized structures of the larger Ti36O 90H36 complexes of A6K, optimized structure of another conformer of the (TiO2)10 complex of A6K, and visualization of bond currents at the (TiO2)10 interface of A6K. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS We thank Professor Dr. Thomas Bredow (Universität Bonn) for providing us a copy of the MSINDO program. We thank Dr. Henrik Löfås for providing the python scripts to visualize the bond currents.
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REFERENCES
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Figure 3. Calculated electron transfer rates (kET) of (TiO2)10 complexes of α-helical structures of AnK (n = 1,...,6) peptides.
We believe that the results of the current work not only allow us to obtain unparalleled insight on the role of interfacial charge transfer in influencing both the structure and nature of binding of peptides to metal oxide nanoparticles, but also help the development of novel biophotovoltaic systems based on biomolecules. Our work may also be interesting in the context 3558
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