An integrated approach towards extracting structural characteristics of chlorosomes from a bchQ mutant of Chlorobaculum tepidum.

Chlorosomes, the photosynthetic antenna complexes of green sulfur bacteria, are paradigms for light-harvesting elements in artificial designs, owing to their efficient energy transfer without protein participation. We combined magic angle spinning (MAS) NMR, optical spectroscopy and cryogenic electron microscopy (cryo-EM) to characterize the structure of chlorosomes from a bchQ mutant of Chlorobaculum tepidum. The chlorosomes of this mutant have a more uniform composition of bacteriochlorophyll (BChl) with a predominant homolog, [8Ethyl, 12Ethyl] BChl c, compared to the wild type (WT). Nearly complete 13C chemical shift assignments were obtained from well-resolved homonuclear 13C-13C RFDR data. For proton assignments heteronuclear 13C-1H (hCH) data sets were collected at 1.2 GHz spinning at 60 kHz. The CHHC experiments revealed intermolecular correlations between 132/31, 132/32, and 121/31, with distance constraints of less than 5 Å. These constraints indicate the syn-anti parallel stacking motif for the aggregates. Fourier transform cryo-EM data reveal an axial repeat of 1.49 nm for the helical tubular aggregates, perpendicular to the inter-tube separation of 2.1 nm. This axial repeat is different from WT and is in line with BChl syn-anti stacks running essentially parallel to the tube axis. Such a packing mode is in agreement with the signature of the Qy band in circular dichroism (CD). Combining the experimental data with computational insight suggests that the packing for the light-harvesting function is similar between WT and bchQ, while the chirality within the chlorosomes is modestly but detectably affected by the reduced compositional heterogeneity in bchQ.

Ligand Rigidity Steers the Selectivity and Efficiency of the Photosubstitution Reaction of Strained Ruthenium Polypyridyl Complexes.

While photosubstitution reactions in metal complexes are usually thought of as dissociative processes poorly dependent on the environment, they are, in fact, very sensitive to solvent effects. Therefore, it is crucial to explicitly consider solvent molecules in theoretical models of these reactions. Here, we experimentally and computationally investigated the selectivity of the photosubstitution of diimine chelates in a series of sterically strained ruthenium(II) polypyridyl complexes in water and acetonitrile. The complexes differ essentially by the rigidity of the chelates, which strongly influenced the observed selectivity of the photosubstitution. As the ratio between the different photoproducts was also influenced by the solvent, we developed a full density functional theory modeling of the reaction mechanism that included explicit solvent molecules. Three reaction pathways leading to photodissociation were identified on the triplet hypersurface, each characterized by either one or two energy barriers. Photodissociation in water was promoted by a proton transfer in the triplet state, which was facilitated by the dissociated pyridine ring acting as a pendent base. We show that the temperature variation of the photosubstitution quantum yield is an excellent tool to compare theory with experiments. An unusual phenomenon was observed for one of the compounds in acetonitrile, for which an increase in temperature led to a surprising decrease in the photosubstitution reaction rate. We interpret this experimental observation based on complete mapping of the triplet hypersurface of this complex, revealing thermal deactivation to the singlet ground state through intersystem crossing.

MetalDock: An Open Access Docking Tool for Easy and Reproducible Docking of Metal Complexes.

Despite the proven potential of metal complexes as therapeutics, the lack of computational tools available for the high-throughput screening of their interactions with proteins is a limiting factor toward clinical developments. To address this challenge, we introduce MetalDock, an easy-to-use, open access docking software for docking metal complexes to proteins. Our tool integrates the AutoDock docking engine with three well-known quantum software packages to automate the docking of metal-organic complexes to proteins. We used a Monte Carlo sampling scheme to obtain the missing Lennard-Jones parameters for 12 metal atom types and demonstrated that these parameters generalize exceptionally well. Our results show that the poses obtained by MetalDock are highly accurate, as they predict the binding geometries experimentally determined by crystal structures with high spatial reproducibility. Three different case studies are presented that demonstrate the versatility of MetalDock for the docking of diverse metal-organic compounds to different biomacromolecules, including nucleic acids.

Correction: Automated assessment of redox potentials for dyes in dye-sensitized photoelectrochemical cells.

Correction for 'Automated assessment of redox potentials for dyes in dye-sensitized photoelectrochemical cells' by Jelena Belic et al., Phys. Chem. Chem. Phys., 2022, 24, 197-210, https://doi.org/10.1039/D1CP04218A.

Efficient workflow for the investigation of the catalytic cycle of water oxidation catalysts: Combining GFN-xTB and density functional theory.

Photocatalytic water oxidation remains the bottleneck in many artificial photosynthesis devices. The efficiency of this challenging process is inherently linked to the thermodynamic and electronic properties of the chromophore and the water oxidation catalyst (WOC). Computational investigations can facilitate the search for favorable chromophore-catalyst combinations. However, this remains a demanding task due to the requirements on the computational method that should be able to correctly describe different spin and oxidation states of the transition metal, the influence of solvation and the different rates of the charge transfer and water oxidation processes. To determine a suitable method with favorable cost/accuracy ratios, the full catalytic cycle of a molecular ruthenium based WOC is investigated using different computational methods, including density functional theory (DFT) with different functionals (GGA, Hybrid, Double Hybrid) as well as the semi-empirical tight binding approach GFN-xTB. A workflow with low computational cost is proposed that combines GFN-xTB and DFT and provides reliable results. GFN-xTB geometries and frequencies combined with single-point DFT energies give free energy changes along the catalytic cycle that closely follow the full DFT results and show satisfactory agreement with experiment, while significantly decreasing the computational cost. This workflow allows for cost efficient determination of energetic, thermodynamic and dynamic properties of WOCs.

Automated assessment of redox potentials for dyes in dye-sensitized photoelectrochemical cells.

Sustainable solutions for hydrogen production, such as dye-sensitized photoelectrochemical cells (DS-PEC), rely on the fundamental properties of its components whose modularity allows for their separate investigation. In this work, we design and execute a high-throughput scheme to tune the ground state oxidation potential (GSOP) of perylene-type dyes by functionalizing them with different ligands. This allows us to identify promising candidates which can then be used to improve the cell's efficiency. First, we investigate the accuracy of different theoretical approaches by benchmarking them against experimentally determined GSOPs. We test different methods to calculate the vertical oxidation potential, including GW with different levels of self-consistency, Kohn-Sham (KS) orbital energies and total energy differences. We find that there is little difference in the performance of these methods. However, we show that it is crucial to take into account solvent effects as well as the structural relaxation of the dye after oxidation. Other thermodynamic contributions are negligible. Based on this benchmark, we decide on an optimal strategy, balancing computational cost and accuracy, to screen more than 1000 dyes and identify promising candidates which could be used to construct more robust DS-PECs.

Systematic Computational Design and Optimization of Light Absorbing Dyes.

We present a workflow to aid the discovery of new dyes for the role of a photosensitive unit in the dye-sensitized photo-electrochemical cells (DS-PECs). New structures are generated in a fully automated way using the Compound Attachment Tool (CAT) introduced in this work. These structures are characterized with efficient approximate density functional theory (DFT) methods, and molecules with favorable optical properties are suggested for possible further use in DS-PECs. As around 2500 structures are generated in this work, and as we aim for still larger volumes of compounds to screen in subsequent applications, we have assessed the reliability of low-cost screening methods and show that simplified time-dependent density functional theory (sTDDFT) provides a satisfying accuracy/cost ratio. From the dyes considered, we propose a set that can be suitable for panchromatic sensitization of the photoelectrode in DS-PECs to further increase DS-PEC efficiency.

A Hybrid Solid-State NMR and Electron Microscopy Structure-Determination Protocol for Engineering Advanced para-Crystalline Optical Materials.

Hybrid magic-angle spinning (MAS) NMR spectroscopy and TEM were demonstrated for de novo structure determination of para-crystalline materials with a bioinspired fused naphthalene diimide (NDI)-salphen-phenazine prototype light-harvesting compound. Starting from chiral building blocks with C2 molecular symmetry, the asymmetric unit was determined by MAS NMR spectroscopy, index low-resolution TEM diffraction data, and resolve reflection conditions, and for the first time the ability to determine the space group from reciprocal space data using this hybrid approach was shown. Transfer of molecular C2 symmetry into P2/c packing symmetry provided a connection across length scales to overcome both lack of long-range order and missing diffraction-phase information. Refinement with heteronuclear distance constraints confirmed the racemic P2/c packing that was scaffolded by molecular recognition of salphen zinc in a pseudo-octahedral environment with bromide and with alkyl chains folding along the phenazine. The NDI light-harvesting stacks ran orthogonal to the intermolecular electric dipole moment present in the solid. Finally, the orientation of flexible lamellae on an electrode surface was determined.

Introducing a closed system approach for the investigation of chemical steps involving proton and electron transfer; as illustrated by a copper-based water oxidation catalyst.

The investigation of the catalytic mechanism of homogeneous water oxidation catalysts remains an active field of research. When examining catalytic steps theoretically, it is often difficult to account for the transfer of protons and electrons from step to step. To this end, a closed system approach is proposed which includes both proton and electron acceptors in the simulation box to allow for the description of proton-coupled electron transfer processes. Using Car-Parrinello Molecular Dynamics, a mononuclear copper water oxidation catalyst Cu(bpy)(OH)2 was used as a model system to explore this closed system approach. The exploration of this model system shows that, compared to traditional methods, this approach offers extra insight into proposed catalytic steps and allows for the clear identification of preferred reaction paths.

Design and synthesis of aromatic molecules for probing electric fields at the nanoscale.

We propose using halogenated organic dyes as nanoprobes for electric fields and show their greatly enhanced Stark coefficients using density functional theory (DFT) calculations. We analyse halogenated variants of three molecules that have been of interest for cryogenic single molecule spectroscopy: perylene, terrylene, and dibenzoterrylene, with the zero-phonon optical transitions at blue, red, and near-infrared. Out of all the combinations of halides and binding sites that are calculated, we have found that fluorination of the optimum binding site induces a dipole difference between the ground and excited states larger than 0.5 D for all three molecules with the highest value of 0.69 D for fluoroperylene. We also report on the synthesis of 3-fluoroterrylene and the bulk spectroscopy of this compound in liquid and solid organic environments.

Real-time simulations of photoinduced coherent charge transfer and proton-coupled electron transfer.

Photoinduced electron transfer (ET) and proton-coupled electron transfer (PCET) are fundamental processes in natural phenomena, most noticeably in photosynthesis. Time-resolved spectroscopic evidence of coherent oscillatory behavior associated with these processes has been reported both in complex biological environments, as well as in biomimetic models for artificial photosynthesis. Here, we consider a few biomimetic models to investigate these processes in real-time simulations based on ab initio molecular dynamics and Ehrenfest dynamics. This allows for a detailed analysis on how photon-to-charge conversion is promoted by a coupling of the electronic excitation with specific vibrational modes and with proton displacements. The ET process shows a characteristic coherence that is linked to the nuclear motion at the interface between donor and acceptor. We also show real-time evidence of PCET in a benzimidazole-phenol redox relay.

Effect of Anchoring Dynamics on Proton-Coupled Electron Transfer in the Ru(bda) Coordination Oligomer on a Graphitic Surface.

The oligomeric ruthenium-based water oxidation catalyst, Ru(bda), is known to be experimentally anchored on graphitic surfaces through CH-π stacking interactions between the auxiliary bda ([2,2'-bipyridine]-6,6'-dicarboxylate) ligand bonded to ruthenium and the hexagonal rings of the surface. This anchoring provides control over their molecular coverage and enables efficient catalysis of water oxidation to dioxygen. The oligomeric nature of the molecule offers multiple anchoring sites at the surface, greatly enhancing the overall stability of the hybrid catalyst-graphitic surface anode through dynamic bonding. However, the impact of this dynamic anchoring on the overall catalytic mechanism is still a topic of debate. In this study, a crucial proton-coupled electron transfer event in the catalytic cycle is investigated using DFT-based molecular dynamics simulations plus metadynamics. The CH-π stacking anchoring plays a critical role not only in stabilizing this hybrid system but also in facilitating the proton-coupled electron transfer event with possible vibronic couplings between the anchoring bonds motion and charge fluctuations at the catalyst - graphitic surface interface. Furthermore, this computational investigation displays the presence of a quartet spin state intermediate that can lead to the experimentally observed and thermodynamically more stable doublet spin state.

Covalent Benzenesulfonic Functionalization of a Graphene Nanopore for Enhanced and Selective Proton Transport.

A fundamental understanding of proton transport through graphene nanopores, defects, and vacancies is essential for advancing two-dimensional proton exchange membranes (PEMs). This study employs ReaxFF molecular dynamics, metadynamics, and density functional theory to investigate the enhanced proton transport through a graphene nanopore. Covalently functionalizing the nanopore with a benzenesulfonic group yields consistent improvements in proton permeability, with a lower activation barrier (≈0.15 eV) and increased proton selectivity over sodium cations. The benzenesulfonic functionality acts as a dynamic proton shuttle, establishing a favorable hydrogen-bonding network and an efficient proton transport channel. The model reveals an optimal balance between proton permeability and selectivity, which is essential for effective proton exchange membranes. Notably, the benzenesulfonic-functionalized graphene nanopore system achieves a theoretically estimated proton diffusion coefficient comparable to or higher than the current state-of-the-art PEM, Nafion. Ergo, the benzenesulfonic functionalization of graphene nanopores, firmly holds promise for future graphene-based membrane development in energy conversion devices.

Observation of Dark States in Two-Dimensional Electronic Spectra of Chlorosomes.

Observations of low-lying dark states in several photosynthetic complexes challenge our understanding of the mechanisms behind their efficient energy transfer processes. Computational models are necessary for providing novel insights into the nature and function of dark states, especially since these are not directly accessible in spectroscopy experiments. Here, we will focus on signatures of dark-type states in chlorosomes, a light-harvesting complex from green sulfur bacteria well-known for uniting a broad absorption band with very efficient energy transfer. In agreement with experiments, our simulations of two-dimensional electronic spectra capture the ultrafast exciton transfer occurring in 100s of femtoseconds within a single chlorosome cylinder. The sub-100 fs process corresponds to relaxation within the single-excitation manifold in a single chlorosome tube, where all initially created populations in the bright exciton states are quickly transferred to dark-type exciton states. Structural inhomogeneities on the local scale cause a redistribution of the oscillator strength, leading to the emergence of these dark-type exciton states, which dominate ultrafast energy transfer. The presence of the dark-type exciton states suppresses energy loss from an isolated chlorosome via fluorescence quenching, as observed experimentally. Our results further question whether relaxation to dark-exciton states is a leading process or merely competes with transfer to the baseplate within the photosynthetic apparatus of green sulfur bacteria.

Elucidation of the Electrocatalytic Nitrite Reduction Mechanism by Bio-Inspired Copper Complexes.

Mononuclear copper complexes relevant to the active site of copper nitrite reductases (CuNiRs) are known to be catalytically active for the reduction of nitrite. Yet, their catalytic mechanism has thus far not been resolved. Here, we provide a complete description of the electrocatalytic nitrite reduction mechanism of a bio-inspired CuNiR catalyst Cu(tmpa) (tmpa = tris(2-pyridylmethyl)amine) in aqueous solution. Through a combination of electrochemical studies, reaction kinetics, and density functional theory (DFT) computations, we show that the protonation steps take place in a stepwise manner and are decoupled from electron transfer. The rate-determining step is a general acid-catalyzed protonation of a copper-ligated nitrous acid (HNO2) species. In view of the growing urge to convert nitrogen-containing compounds, this work provides principal reaction parameters for efficient electrochemical nitrite reduction. This contributes to the investigation and development of nitrite reduction catalysts, which is crucial to restore the biogeochemical nitrogen cycle.

Challenges in Elucidating the Free Energy Scheme of the Laccase Catalyzed Reduction of Oxygen.

Artificial redox catalysts are typically limited by unfavorable scaling relations of reaction intermediates leading to a significant overpotential in multi-electron redox reactions such as for example the oxygen reduction reaction (ORR). The multicopper oxidase laccase is able to catalyze the ORR in nature. In particular the high-potential variants show a remarkably low overpotential for the ORR and apparently do not suffer from such unfavorable scaling relations. Although laccases are intensively studied, it is presently unknown why the overpotential for ORR is so low and a clear description regarding the thermodynamics of the catalytic cycle and the underlying design principles is lacking. In order to understand the laccase catalyzed ORR from an electrochemical perspective, elucidation of the free energy scheme would be of high value. This article reviews the energetics of the proposed laccase catalyzed ORR mechanisms based on experimental and computational studies. However, there are still remaining challenges to overcome to elucidate the free energy scheme of laccase. Obtaining thermodynamic data on intermediates is hard or even impossible with analytical techniques. On the other hand, several computational studies have been performed with significantly different parameters and conditions, thus making a direct comparison difficult. For these reasons, a consensus on a clear free energy scheme is still lacking. We anticipate that ultimately conquering these challenges will result in a better understanding of laccase catalyzed ORR and will allow for the design of low overpotential redox catalysts.

Ultrafast Anisotropy Decay Reveals Structure and Energy Transfer in Supramolecular Aggregates.

Chlorosomes from green bacteria perform the most efficient light capture and energy transfer, as observed among natural light-harvesting antennae. Hence, their unique functional properties inspire developments in artificial light-harvesting and molecular optoelectronics. We examine two distinct organizations of the molecular building blocks as proposed in the literature, demonstrating how these organizations alter light capture and energy transfer, which can serve as a mechanism that the bacteria utilize to adapt to changes in light conditions. Spectral simulations of polarization-resolved two-dimensional electronic spectra unravel how changes in the helicity of chlorosomal aggregates alter energy transfer. We show that ultrafast anisotropy decay presents a spectral signature that reveals contrasting energy pathways in different chlorosomes.

In vivo metallophilic self-assembly of a light-activated anticancer drug.

Self-assembling molecular drugs combine the easy preparation typical of small-molecule chemotherapy and the tumour-targeting properties of drug-nanoparticle conjugates. However, they require a supramolecular interaction that survives the complex environment of a living animal. Here we report that the metallophilic interaction between cyclometalated palladium complexes generates supramolecular nanostructures in living mice that have a long circulation time (over 12 h) and efficient tumour accumulation rate (up to 10.2% of the injected dose per gram) in a skin melanoma tumour model. Green light activation leads to efficient tumour destruction due to the type I photodynamic effect generated by the self-assembled palladium complexes, as demonstrated in vitro by an up to 96-fold cytotoxicity increase upon irradiation. This work demonstrates that metallophilic interactions are well suited to generating stable supramolecular nanotherapeutics in vivo with exceptional tumour-targeting properties.

Manifestation of Hydrogen Bonding and Exciton Delocalization on the Absorption and Two-Dimensional Electronic Spectra of Chlorosomes.

Chlorosomes are supramolecular aggregates that contain thousands of bacteriochlorophyll molecules. They perform the most efficient ultrafast excitation energy transfer of all natural light-harvesting complexes. Their broad absorption band optimizes light capture. In this study, we identify the microscopic sources of the disorder causing the spectral width and reveal how it affects the excited state properties and the optical response of the system. We combine molecular dynamics, quantum chemical calculations, and response function calculations to achieve this goal. The predicted linear and two-dimensional electronic spectra are found to compare well with experimental data reproducing all key spectral features. Our analysis of the microscopic model reveals the interplay of static and dynamic disorder from the molecular perspective. We find that hydrogen bonding motifs are essential for a correct description of the spectral line shape. Furthermore, we find that exciton delocalization over tens to hundreds of molecules is consistent with the two-dimensional electronic spectra.

Photon Energy-Dependent Ultrafast Exciton Transfer in Chlorosomes of Chlorobium tepidum and the Role of Supramolecular Dynamics.

The antenna complex of green sulfur bacteria, the chlorosome, is one of the most efficient supramolecular systems for efficient long-range exciton transfer in nature. Femtosecond transient absorption experiments provide new insight into how vibrationally induced quantum overlap between exciton states supports highly efficient long-range exciton transfer in the chlorosome of Chlorobium tepidum. Our work shows that excitation energy is delocalized over the chlorosome in <1 ps at room temperature. The following exciton transfer to the baseplate occurs in ∼3 to 5 ps, in line with earlier work also performed at room temperature, but significantly faster than at the cryogenic temperatures used in previous studies. This difference can be attributed to the increased vibrational motion at room temperature. We observe a so far unknown impact of the excitation photon energy on the efficiency of this process. This dependency can be assigned to distinct optical domains due to structural disorder, combined with an exciton trapping channel competing with exciton transfer toward the baseplate. An oscillatory transient signal damped in <1 ps has the highest intensity in the case of the most efficient exciton transfer to the baseplate. These results agree well with an earlier computational finding of exciton transfer driven by low-frequency rotational motion of molecules in the chlorosome. Such an exciton transfer process belongs to the quantum coherent regime, for which the Förster theory for intermolecular exciton transfer does not apply. Our work hence strongly indicates that structural flexibility is important for efficient long-range exciton transfer in chlorosomes.