Correlated intermolecular coupling fluctuations in photosynthetic complexes

The functioning and efficiency of natural photosynthetic complexes is strongly influenced by their embedding in a noisy protein environment, which can even serve to enhance the transport efficiency. Interactions with the environment induce fluctuations of the transition energies and couplings between the chlorophyll molecules, and due to the fact that different fluctuations will partially be caused by the same environmental factors, correlations between the various fluctuations will occur. We argue that fluctuations of the couplings should, in general, not be neglected, as these have a considerable impact on population transfer rates, decoherence rates, and the efficiency of photosynthetic complexes. Furthermore, while correlations between transition energy fluctuations have been studied, we provide the first quantitative study of the effect of correlations between coupling fluctuations and transition energy fluctuations, and of correlations between the various coupling fluctuations. It is shown that these additional correlations typically lead to changes in interchromophore transfer rates and population oscillations and can lead to a limited enhancement of the light harvesting efficiency.     

Hydration free energies and entropies for water in protein interiors

Free energy calculations for the transfer of a water molecule from the pure liquid to an interior cavity site in a protein are presented. Two different protein cavities, in bovine pancreatic trypsin inhibitor (BPTI) and in the I76A mutant of barnase, represent very different environments for the water molecule: one which is polar, forming four water-protein hydrogen bonds, and one which is more hydrophobic, forming only one water-protein hydrogen bond. The calculations give very different free energies for the different cavities, with only the polar BPTI cavity predicted to be hydrated. The corresponding entropies for the transfer to the interior cavities are calculated as well and show that the transfer to the polar cavity is significantly entropically unfavorable while the transfer to the nonpolar cavity is entropically favorable. For both proteins an analysis of the fluctuations in the positions of the protein atoms shows that the addition of a water molecule makes the protein more flexible. This increased flexibility appears to be due to an increased length and weakened strength of protein-protein hydrogen bonds near the cavity.     

Influence of environment induced correlated fluctuations in electronic coupling on coherent excitation energy transfer dynamics in model photosynthetic systems

Two-dimensional photon-echo experiments indicate that excitation energy transfer between chromophores near the reaction center of the photosynthetic purple bacterium Rhodobacter sphaeroides occurs coherently with decoherence times of hundreds of femtoseconds, comparable to the energy transfer time scale in these systems. The original explanation of this observation suggested that correlated fluctuations in chromophore excitation energies, driven by large scale protein motions could result in long lived coherent energy transfer dynamics. However, no significant site energy correlation has been found in recent molecular dynamics simulations of several model light harvesting systems. Instead, there is evidence of correlated fluctuations in site energy-electronic coupling and electronic coupling-electronic coupling. The roles of these different types of correlations in excitation energy transfer dynamics are not yet thoroughly understood, though the effects of site energy correlations have been well studied. In this paper, we introduce several general models that can realistically describe the effects of various types of correlated fluctuations in chromophore properties and systematically study the behavior of these models using general methods for treating dissipative quantum dynamics in complex multi-chromophore systems. The effects of correlation between site energy and inter-site electronic couplings are explored in a two state model of excitation energy transfer between the accessory bacteriochlorophyll and bacteriopheophytin in a reaction center system and we find that these types of correlated fluctuations can enhance or suppress coherence and transfer rate simultaneously. In contrast, models for correlated fluctuations in chromophore excitation energies show enhanced coherent dynamics but necessarily show decrease in excitation energy transfer rate accompanying such coherence enhancement. Finally, for a three state model of the Fenna-Matthews-Olsen light harvesting complex, we explore the influence of including correlations in inter-chromophore couplings between different chromophore dimers that share a common chromophore. We find that the relative sign of the different correlations can have profound influence on decoherence time and energy transfer rate and can provide sensitive control of relaxation in these complex quantum dynamical open systems.     

Photophysics of Acetophenone Interacting with DNA: Why the Road to Photosensitization is Open

Deoxyribonucleic acid photosensitization, i.e. the photoinduced electron‐ or energy‐transfer of chromophores interacting with DNA, is a crucial phenomenon that triggers important DNA lesions such as pyrimidine dimerization, even upon absorption of relatively low‐energy radiation. Oxidative lesions may also be produced via the photoinduced production of reactive oxygen species. Aromatic ketones, and acetophenone in particular, are well known for their sensitization effects. In this contribution we model the structural and dynamical properties of the acetophenone/DNA aggregates as well as their spectroscopic and photophysical properties using high‐level hybrid quantum mechanics/molecular mechanics methods. We show that the key steps of the photochemistry of acetophenone in gas phase are conserved in the macromolecular environment and thus an ultrafast singlet–triplet conversion of acetophenone is expected prior to the transfer to DNA.     

Polarons in DNA: transition from guanine to adenine transport

Experiments on hole transport in DNA have been interpreted as showing that a hole introduced onto a guanine (G) followed by a series of adenines (As) in a DNA duplex travels through the first three As by tunneling and then, with thermal energy, makes the transition onto the bridge of As. It has been widely believed that, once on the bridge, the hole is localized on a single A and proceeds by hopping between As. In the experiments, the holes on the A bridge diffuse, with little attenuation, until trapped by a GGG sequence. Recently, it has been discovered by Bixon and Jortner that the model of tunneling followed by hopping between As cannot account for the very weak dependence on bridge size of the relative chemical yields and the ratios of the rates for the two processes. In earlier calculations, we have shown that interaction with water results in the hole becoming a polaron spread over approximately four As. According to these calculations, the energy of the hole on the polaron is decreased so much that it is lower than that of the hole on G and even that of GGG. Estimates of energy fluctuations, due to fluctuations in the environment and conformational changes of the DNA, find them to be large enough so that GGG, and even G, can still act as hole traps, but trapping on the former is still very much more likely because of its lower energy.     

pH-dependent x-ray absorption spectra of aqueous boron oxides

Near edge x-ray absorption fine structure (NEXAFS) spectra at the boron K-edge were measured for aqueous boric acid, borate, and polyborate ions, using liquid microjet technology, and compared with simulated spectra calculated from first principles density functional theory in the excited electron and core hole (XCH) approximation. Thermal motion in both hydrated and isolated molecules was incorporated into the calculations by sampling trajectories from quantum mechanics∕molecular mechanics simulations at the experimental temperature. The boron oxide molecules exhibit little spectral change upon hydration, relative to mineral samples. Simulations reveal that water is arranged nearly isotropically around boric acid and sodium borate, but the calculations also indicate that the boron K-edge NEXAFS spectra are insensitive to hydrogen bonding, molecular environment, or salt interactions.     

What governs the charge transfer in DNA? The role of DNA conformation and environment

Charge transfer in DNA has received much attention in the last few years due to its role in oxidative damage and repair in DNA and also due to possible applications of DNA in nanoelectronics. Despite intense experimental and theoretical efforts, the mechanism underlying long-range hole transport is still unresolved. This is in particular due to the sensitive dependence of charge transfer on the complex structure and dynamics of DNA and the interaction with the solvent, which could not be addressed adequately in the modeling approaches up to now. In this work, we study the factors governing hole transfer in detail, using a DFT-based fragment-orbital method, which allows to compute the charge transfer parameters along multinanosecond molecular dynamics simulations. Environmental effects are captured using a hybrid quantum mechanics-molecular mechanics (QM/MM) coupling scheme. This methodology allows to analyze several factors responsible for charge transfer in DNA in detail. The fluctuation of counterions, strongly counterbalanced by the surrounding water, leads to large oscillations of onsite energies, which govern the energetics of hole propagation along the DNA strand. In contrast, the electronic couplings depend only on DNA conformation and are not affected by the solvent. In particular, the onsite energies are strongly correlated between neighboring nucleobases, indicating that a conformational-gating type of mechanism may be induced by the collective environmental degrees of freedom.     

Spectral properties of polypyridyl ruthenium complexes intercalated in DNA: theoretical insights into the surrounding effects of [Ru(dppz)(bpy)(2)](2+)

The UV/Visible absorption properties of a polypyridyl ruthenium complex upon intercalation on DNA are studied at the mixed quantum mechanics molecular mechanics level of theory. Vertical excitation transitions are computed by time dependent density functional theory. Particular emphasis is put on the different levels at which the macromolecular environment is treated, and in particular on the analysis of the effect of mechanical, electrostatic and polarizable embedding. We show that with the highest level of theory the experimental absorption wavelengths are reproduced with a difference of only 2 or 3 nm for the low energy bands. The systematic analysis of the individual vertical transitions allows us to get much more insights into the role played by the environment, in particular, in metal to ligand and intra ligand charge transfer transitions that can lead to the production of DNA oxidative lesions exploitable in phototherapy.     

Double-helical --> ladder structural transition in the B-DNA is induced by a loss of dispersion energy

The role of the dispersion energy and electrostatic energy on the geometry and stability of the B-DNA helix was investigated. Both molecular dynamics simulations with empirical force field and hybrid quantum mechanical/molecular mechanics molecular dynamics simulations, where the dispersion or electrostatics term is suppressed/increased, on the one hand and an ab initio minimization procedure on the other have shown that the lack of the dispersion term leads to an increase of the vertical separation of the bases as well as to a loss of helicity, thus resulting in a ladder-like structure. A decrease of the electrostatic term produces a separation of the DNA strands. The biological consequences of both electrostatic and dispersion forces in DNA are enormous, and without either of them, DNA would become unstable and unable to provide the storage and transfer of genetic information.     

Ab initio integrated multi-center molecular orbitals method for large cluster systems: total energy and normal vibration

A new computational scheme integrating multi-center ab initio molecular orbitals for determining total energy and normal vibration of large cluster systems is presented. This method can be used to treat large cluster systems such as solvents by quantum mechanics. The geometry parameters, the total energies, the relative energies, and the normal vibrations for four models of water cluster, the hydrated hydronium ion complex, and the transition state of proton transfer are calculated by the present method and are compared with those obtained by the full ab initio MO method. The results agree very well. The scheme proposed in this article is also intended to be used in modeling computer cluster systems using parallel algorithms.     

PNA versus DNA: effects of structural fluctuations on electronic structure and hole-transport mechanisms

The effects of structural fluctuations on charge transfer in double-stranded DNA and peptide nucleic acid (PNA) are investigated. A palindromic sequence with two guanine bases that play the roles of hole donor and acceptor, separated by a bridge of two adenine bases, was analyzed using combined molecular dynamics (MD) and quantum-chemical methods. Surprisingly, electronic structure calculations on individual MD snapshots show significant frontier orbital electronic population on the bridge in approximately 10% of the structures. Electron-density delocalization to the bridge is found to be gated by fluctuations of the covalent conjugated bond structure of the aromatic rings of the nucleic bases. It is concluded, therefore, that both thermal hopping and superexchange should contribute significantly to charge transfer even in short DNA/PNA fragments. PNA is found to be more flexible than DNA, and this flexibility is predicted to produce larger rates of charge transfer.     

DNA Nucleobase under Ionizing Radiation: Unexpected Proton Transfer by Thymine Cation in Water Nanodroplets

The effect of ionizing radiation on DNA constituents is a widely studied fundamental process using experimental and computational techniques. In particular, radiation effects on nucleobases are usually tackled by mass spectrometry in which the nucleobase is embedded in a water nanodroplet. Here, we present a multiscale theoretical study revealing the effects and the dynamics of water droplets towards neutral and ionized thymine. In particular, by using both hybrid quantum mechanics/molecular mechanics and full ab initio molecular dynamics, we reveal an unexpected proton transfer from thymine cation to a nearby water molecule. This leads to the formation of a neutral radical thymine and a Zundel structure, while the hydrated proton localizes at the interface between the deprotonated thymine and the water droplet. This observation opens entirely novel perspectives concerning the reactivity and further fragmentation of ionized nucleobases.     

Electronic couplings and on-site energies for hole transfer in DNA: systematic quantum mechanical/molecular dynamic study

The electron hole transfer (HT) properties of DNA are substantially affected by thermal fluctuations of the pi stack structure. Depending on the mutual position of neighboring nucleobases, electronic coupling V may change by several orders of magnitude. In the present paper, we report the results of systematic QM/molecular dynamic (MD) calculations of the electronic couplings and on-site energies for the hole transfer. Based on 15 ns MD trajectories for several DNA oligomers, we calculate the average coupling squares V(2) and the energies of basepair triplets XG(+)Y and XA(+)Y, where X, Y=G, A, T, and C. For each of the 32 systems, 15,000 conformations separated by 1 ps are considered. The three-state generalized Mulliken-Hush method is used to derive electronic couplings for HT between neighboring basepairs. The adiabatic energies and dipole moment matrix elements are computed within the INDO/S method. We compare the rms values of V with the couplings estimated for the idealized B-DNA structure and show that in several important cases the couplings calculated for the idealized B-DNA structure are considerably underestimated. The rms values for intrastrand couplings G-G, A-A, G-A, and A-G are found to be similar, approximately 0.07 eV, while the interstrand couplings are quite different. The energies of hole states G(+) and A(+) in the stack depend on the nature of the neighboring pairs. The XG(+)Y are by 0.5 eV more stable than XA(+)Y. The thermal fluctuations of the DNA structure facilitate the HT process from guanine to adenine. The tabulated couplings and on-site energies can be used as reference parameters in theoretical and computational studies of HT processes in DNA.     

Charge transfer in DNA: hole charge is confined to a single base pair due to solvation effects

We include solvation effects in tight-binding Hamiltonians for hole states in DNA. The corresponding linear-response parameters are derived from accurate estimates of solvation energy calculated for several hole charge distributions in DNA stacks. Two models are considered: (A) the correction to a diagonal Hamiltonian matrix element depends only on the charge localized on the corresponding site and (B) in addition to this term, the reaction field due to adjacent base pairs is accounted for. We show that both schemes give very similar results. The effects of the polar medium on the hole distribution in DNA are studied. We conclude that the effects of polar surroundings essentially suppress charge delocalization in DNA, and hole states in (GC)(n) sequences are localized on individual guanines.     

A multi-scale method for the calculation of charge transfer rates through the Pi-stack of DNA: application to DNA dynamics

We describe an ultra-fast, multi-scale method for calculating charge transfer rates through the pi-stack of DNA using a simple charge hopping model in conjunction with the Marcus equation. The calculation of the parameters required as input to the Marcus equation, such as the electronic coupling and the driving force, are calculated with a combination of quantum mechanical methods and conformations sampled from classical molecular dynamics (MD) simulations. The resulting set of time dependent rate equations are then solved stochastically using Monte Carlo (MC) methods. We have applied this model to investigate the importance of thermal fluctuations in DNA conformation over picosecond and nanosecond timescales, and have identified the timescales of most relevance to hole transfer through DNA.     

Excited Electron–Hole States in Molecular Chains

The eigenvalues and the eigenfunctions of molecular excitons, charge-transfer excitons, and electron–hole pairs have been found in the approximation of electron and hole transfer between the lowest unoccupied and highest occupied orbitals in a rigid molecular chain of identical photosensitive molecules, the recognized model of organic solar cells. It has been shown that as the Coulomb binding energy decreases, the wave functions become superposition of functions of the increasing number of sites and the decay time, determined by electron or hole transitions, is shorter that the transfer time of the exciton as a whole, so that energy transfer and charge transfer become interrelated processes.     

Energetics of proton transfer in liquid water. I. Ab initio study for origin of many-body interaction and potential energy surfaces

The energetics of proton transfer in liquid water investigated by using ab initio calculation. The molecular electronic interaction of hydrated proton clusters in classified into many-body interaction elements by a new energy decomposition method. It is found that up to three-body molecular interaction is essential to describe the potential energy surface. The three-body effect mainly arises from the (non-classical) charge transfer and strongly depends on their configuration. Higher than three-body effects are small enough to be neglected. To simulate the liquid state reactions, two cluster models including all water molecules up to the second shell in the proton transfer reactions are employed. It is shown that these proton transfer reactions only involve small potential energy barriers of a few kcal/mol or less when structural rearrangement of the solvent is induced along the proton movement.     

Statistical mechanics of hydrated electron recombination in liquid and supercritical water

The photochemical yield of hydrated electrons as a function of temperature in liquid and supercritical water is treated in terms of energy fluctuations of the medium. The geminate pair, consisting of a positive ion and a hydrated electron, is regarded as a H-like atom embedded in a completely relaxed dielectric continuum. If the local medium energy is larger than the ionization energy of this atom, the electron escapes its geminate partner. By making use of the classical theory of energy fluctuations, escape probability is described by a simple explicit function, the variable of which is a combination of temperature, relative permittivity, and specific heat. First our earlier calculations on the recombination of solvated electrons, produced by ionizing radiation in a number of polar liquids, are improved and then the theory is compared with the experimental results on temperature dependent electron survival by Kratz et al. [S. Kratz, J. Torres-Alcan, J. Urbanek, J. Lindner, and P. Vo?hringer, Phys. Chem. Chem. Phys. 12, 12169 (2010)]. Two adjustable parameters are needed to achieve reasonable quantitative agreement.     

Solution structure of papain as studied by molecular mechanics and molecular dynamics techniques

In this paper, we report the molecular mechanics and molecular dynamics studies of the hydration of papain using the AMBER and CHARMm programs. We studied papain in an environment with minimal hydration involving only the X-ray waters and also in the hydrated environment by adding an extra 9 Å layer of water around the residues. The effect of nonbond cutoff was studied by performing minimizations with 8 Å and 15 Å nonbond cutoffs using the program AMBER. Two different solvent models—a constant dielectric and a distance-dependent dielectric—were considered. The AMBER-minimized structure and the average structure obtained from the CHARMm simulations for papain solvated with X-ray waters are presented and compared with the X-ray crystal structure results. Results of a similar comparison of the hydrated structures were also presented. The calculated root mean square deviation between the minimized structure and the X-ray structure is smaller for the hydrated system than for the system hydrated with only the X-ray waters. Results of the molecular mechanics and molecular dynamics simulations were presented for the various regions of papain. The hydration of the active site of papain and the effect of hydration on the torsional motion of the active site residues are presented. © 1996 by John Wiley & Sons, Inc.