Sandro Jurinovich

The Fenna–Matthews–Olson Protein Revisited: A Fully Polarizable (TD)DFT/MM Description†

We report a combined molecular dynamics and quantum mechanics (QM)/molecular mechanics (MM) analysis of the excitonic properties of the Fenna-Matthews-Olson (FMO) protein by using a polarizable MM model combined with a time-dependent density functional theory description. Overall, our results indicate that structural fluctuations, electrostatic interactions, and short-range quantum effects can significantly modulate the model Hamiltonian parameters (site energies and couplings). We find that the specific interactions with the axial ligand and the hydrogen-bonded residues are responsible for the energy ladder, with their effects being mainly due to electrostatic interactions, but with short-range quantum contributions that are not negligible. In addition, a striking modulation of the screening effects experienced by the BChl pairs, due to the heterogeneous polarizability of the FMO and solvent environment, is observed. Finally, we find that the exciton model gives a reliable description of the delocalized excited states in the complex.

Geometry Optimization in Polarizable QM/MM Models: The Induced Dipole Formulation.

We present the mathematical derivation and the computational implementation of the analytical geometry derivatives for a polarizable QM/MM model (QM/MMPol). In the adopted QM/MMPol model, the focused part is treated at QM level of theory, while the remaining part (the environment) is described classically as a set of fixed charges and induced dipoles. The implementation is performed within the ONIOM procedure, resulting in a polarizable embedding scheme, which can be applied to solvated and embedded systems and combined with different polarizable force fields available in the literature. Two test cases characterized by strong hydrogen-bond and dipole-dipole interactions, respectively, are used to validate the method with respect to the nonpolarizable one. Finally, an application to geometry optimization of the chromophore of Rhodopsin is presented to investigate the impact of including mutual polarization between the QM and the classical parts in conjugated systems.

A Quantum Chemical Interpretation of Two-Dimensional Electronic Spectroscopy of Light-Harvesting Complexes

Nonlinear electronic spectroscopies represent one of the most powerful techniques to study complex multichromophoric architectures. For these systems, in fact, linear spectra are too congested to be used to disentangle the many coupled vibroelectronic processes that are activated. By using a 2D approach, instead, a clear picture can be achieved, but only when the recorded spectra are combined with a proper interpretative model. So far, this has been almost always achieved through parametrized exciton Hamiltonians that necessarily introduce biases and/or arbitrary assumptions. In this study, a first-principles approach is presented that combines accurate quantum chemical descriptions with state-of-the-art models for the environment through the use of atomistic and polarizable embeddings. Slow and fast bath dynamics, along with exciton transport between the pigments, are included. This approach is applied to the 2DES spectroscopy of the Light-Harvesting 2 (LH2) complex of purple bacteria. Simulations are extended over the entire visible-near-infrared spectral region to cover both carotenoid and bacteriochlorophyll signals. Our results provide an accurate description of excitonic properties and relaxation pathways, and give an unprecedented insight into the interpretation of the spectral signatures of the measured 2D signals.

Achieving Linear Scaling in Computational Cost for a Fully Polarizable MM/Continuum Embedding

In this paper, we present a new, efficient implementation of a fully polarizable QM/MM/continuum model based on an induced-dipoles polarizable force field and on the Conductor-like Screening Model as a polarizable continuum in combination with a self-consistent field QM method. The paper focuses on the implementation of the MM/continuum embedding, where the two polarizable methods are fully coupled to take into account their mutual polarization. With respect to previous implementations, we achieve for the first time a linear scaling with respect to both the computational cost and the memory requirements without limitations on the molecular cavity shape. This is achieved thanks to the use of the recently developed ddCOSMO model for the continuum and the Fast Multipole Method for the force field, together with an efficient iterative procedure. Therefore, it becomes possible to include in the classical layer as much as several tens of thousands of atoms with a limited computational effort.

Simulation of Electronic Circular Dichroism of Nucleic Acids: From the Structure to the Spectrum

We present a quantum mechanical (QM) simulation of the electronic circular dichroism (ECD) of nucleic acids (NAs). The simulation combines classical molecular dynamics, to obtain the structure and its temperature-dependent fluctuations, with a QM excitonic model to determine the ECD. The excitonic model takes into account environmental effects through a polarizable embedding and uses a refined approach to calculate the electronic couplings in terms of full transition densities. Three NAs with either similar conformations but different base sequences or similar base sequences but different conformations have been investigated and the results were compared with experimental observations; a good agreement was seen in all cases. A detailed analysis of the nature of the ECD bands in terms of their excitonic composition was also carried out. Finally, a comparison between the QM and the DeVoe models clearly revealed the importance of including fluctuations of the excitonic parameters and of accurately determining the electronic couplings. This study demonstrates the feasibility of the ab initio simulation of the ECD spectra of NAs, that is, without the need of experimental structural or electronic data.

Plasmon enhanced light harvesting: multiscale modeling of the FMO protein coupled with gold nanoparticles.

Plasmonic systems, such as metal nanoparticles, are becoming increasingly important in spectroscopies and devices because of their ability to enhance, even by several orders of magnitude, the photophysical properties of neighboring systems. In particular, it has been shown both theoretically and experimentally that combining nanoplasmonic devices with natural light-harvesting proteins substantially increases the fluorescence and absorption properties of the system. This kind of biohybrid device can have important applications in the characterization and design of efficient light-harvesting systems. In the present work, the FMO light-harvesting protein was combined with gold nanoparticles of different sizes, and its photophysical properties were characterized using a multiscale quantum-mechanical classical-polarizable and continuum model (QM/MMPol/PCM). By optimal tuning of the plasmon resonance of the metal nanoparticles, fluorescence enhancements of up to 2 orders of magnitude were observed. Orientation effects were found to be crucial: amplifications by factors of up to 300 were observed for the absorption process, while the radiative decay of the emitting state increased at most by a factor of 10, mostly as a result of poor alignment of the emitting state with the considered metal aggregates. Despite being a limiting factor for high-fluorescence-enhancement devices, the strong orientation dependence may represent an important feature of the natural light-harvesting system that could allow selective enhancement of a specific excited state of the complex.

Integrated NMR and computational study of push-pull NLO probes: interplay of solvent and structural effects.

In this study we combined QM calculations and NMR measurements to understand at a detailed level the complex interplay of structural/electronic properties with the effects of the solvent in the NLO activity of push-pull systems, quantified in terms of variations of the static hyperpolarizability. Different parameters (bond lengths and bond length alternation, vibrational frequencies, electronic charge distribution) are introduced and tested to rationalize both the solvent sensitivity of three molecular systems (namely, p-nitroaniline, ethyl 4-ammino benzoate, and 5-nitro-1H-indole) and the differences among them. This analysis has finally allowed us to establish a clear correlation between the charge transfer behavior of the systems, their NLO properties, and NMR parameters also validating simplified but effective chemical analyses based on resonance limit forms.

EXAT: EXcitonic analysis tool

We introduce EXcitonic Analysis Tool (EXAT), a program able to compute optical spectra of large excitonic systems directly from the output of quantum mechanical calculations performed with the popular Gaussian 16 package. The software is able to combine in an excitonic scheme the single‐chromophore properties and exciton couplings to simulate energies, coefficients, and excitonic spectra (UV‐vis, CD, and LD). The effect of the environment can also be included using a Polarizable Continuum Model. EXAT also presents a simple graphical user interface, which shows on‐screen both site and exciton properties. To show the potential of the method, we report two applications on a a chiral perturbed BODIPY system and DNA G‐quadruplexes, respectively. The program is available online at http://molecolab.dcci.unipi.it/tools/.

The role of charge-transfer states in the spectral tuning of antenna complexes of purple bacteria

The LH2 antenna complexes of purple bacteria occur, depending on light conditions, in various different spectroscopic forms, with a similar structure but different absorption spectra. The differences are related to point changes in the primary amino acid sequence, but the molecular–level relationship between these changes and the resulting spectrum is still not well understood. We undertook a systematic quantum chemical analysis of all the main factors that contribute to the exciton structure, looking at how the environment modulates site energies and couplings in the B800–850 and B800–820 spectroscopic forms of LH2. A multiscale approach combining quantum chemistry and an atomistic classical embedding has been used where mutual polarization effects between the two parts are taken into account. We find that the loss of hydrogen bonds following amino acid changes can only explain a part of the observed blue-shift in the B850 band. The coupling of excitonic states to charge-transfer states, which is different in the two forms, contributes with a similar amount to the overall blue-shift.

A Strategy for the Study of the Interactions between Metal–Dyes and Proteins with QM/MM Approaches: the Case of Iron–Gall Dye

Historical textiles dyed with tannins usually show more extended degradation than fabrics dyed with other coloring materials. In order to shed light on this phenomenon we investigated the molecular interactions between tannin dyes and protein-based textiles using quantum-mechanical tools. In particular, we focused on the iron-gall complex with a fragment of α-helix wool keratin. We developed a step by step protocol which moves from the simplest ternary complexes with free amino acids (all treated quantum mechanically) to the more realistic system of the polypeptide fragment (treated at QM/MM level), passing through an intermediate model of interacting sites to evaluate the local environmental effects. The analysis of the interactions between the iron-gall complexes and free amino acids allowed us to identify possible coordination modes as well as determining their relative geometries. However, we also showed that only with the addition of the proteic environment a detailed picture of the interaction sites and binding modes can be achieved. An important role is in fact played by the microenvironment which can favor specific coordinations with respect to others due to both structural and electronic changes in the possible interaction sites.