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Two-dimensional electronic spectroscopy (2DES) has proven to be a highly effective technique in studying the properties of excited states and the process of excitation energy transfer in complex molecular assemblies, particularly in biological light-harvesting systems. However, the accurate simulation of 2DES for large systems still poses a challenge because of the heavy computational demands it entails. In an effort to overcome this limitation, we devised a coarse-grained 2DES method. This method encompasses the treatment of the entire system by dividing it into distinct weakly coupled segments, which are assumed to communicate predominantly through incoherent exciton transfer. We first demonstrate the efficiency of this method through simulation on a model dimer system, which demonstrates a marked improvement in calculation efficiency, with results that exhibit good concordance with reference spectra calculated with less approximate methods. Additionally, the application of this method to the light-harvesting antenna 2 (LH2) complex of purple bacteria showcases its advantages, accuracy, and limitations. Furthermore, simulating the anisotropy decay in LH2 induced by energy transfer and its comparison with experiments confirm that the method is capable of accurately describing dynamical processes in a biologically relevant system. This method presented lends itself to an extension that accounts for the effect of intrasegment relaxation processes on the 2DES spectra, which for computational efficiency are ignored in the implementation reported here. It is envisioned that the method will be employed in the future to accurately and efficiently calculate 2D spectra of more extensive systems, such as photosynthetic supercomplexes.
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Diatoms, unicellular marine organisms, harness short peptide repeats of the protein silaffin to transform silicic acid into biosilica nanoparticles. This process has been a white whale for material scientists due to its potential in biomimetic applications, ranging from medical to microelectronic fields. Replicating diatom biosilicification will depend on a thorough understanding of the silaffin peptide structure during the reaction, yet existing models in the literature offer conflicting views on peptide folding during silicification. In our study, we employed two-dimensional infrared spectroscopy (2DIR) within the amide I region to determine the secondary structure of the silaffin repeat unit 5 (R5), both pre- and post-interaction with silica. The 2DIR experiments are complemented by molecular dynamics (MD) simulations of pure R5 reacting with silicate. Subsequently, theoretical 2DIR spectra calculated from these MD trajectories allowed us to compare calculated spectra with experimental data, and to determine the diverse structural poses of R5. Our findings indicate that unbound R5 predominantly forms ß-strand structures alongside various atypical secondary structures. Post-silicification, there's a noticeable shift: a decrease in ß-strands coupled with an increase in turn-type and bend-type configurations. We theorize that this structural transformation stems from silicate embedding within R5's hydrogen-bond network, prompting the peptide backbone to contract and adapt around the biosilica precursors.
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Diatomeas , Simulación de Dinámica Molecular , Espectrofotometría Infrarroja , Diatomeas/química , Estructura Secundaria de Proteína , Péptidos/química , Fragmentos de Péptidos , Precursores de ProteínasRESUMEN
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.
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Describing long-range energy transport is a crucial step, both toward deepening our knowledge on natural light-harvesting systems and toward developing novel photoactive materials. Here, we combine experiment and theory to resolve and reproduce energy transport on pico- to nanosecond time scales in single H-type supramolecular nanofibers based on carbonyl-bridged triarylamines (CBT). Each nanofiber shows energy transport dynamics over long distances up to â¼1 µm, despite exciton trapping at specific positions along the nanofibers. Using a minimal Frenkel exciton model including disorder, we demonstrate that spatial correlations in the normally distributed site energies are crucial to reproduce the experimental data. In particular, we can observe the long-range and subdiffusive nature of the exciton dynamics as well as the trapping behavior of excitons in specific locations of the nanofiber. This trapping behavior introduces a net directionality or asymmetry in the exciton dynamics as observed experimentally.
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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.
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Bacterioclorofilas , Chlorobi , Chlorobi/genética , Chlorobi/metabolismo , Bacterioclorofilas/química , Mutación , Complejos de Proteína Captadores de Luz/química , Complejos de Proteína Captadores de Luz/metabolismo , Complejos de Proteína Captadores de Luz/genética , Microscopía por Crioelectrón , Proteínas Bacterianas/química , Proteínas Bacterianas/genética , Proteínas Bacterianas/metabolismoRESUMEN
Diatoms are one of the most abundant photosynthetic organisms on earth and contribute largely to atmospheric oxygen production. They contain fucoxanthin and chlorophyll-a/c binding proteins (FCPs) as light-harvesting complexes with a remarkable adaptation to the fluctuating light on ocean surfaces. To understand the basis of the photosynthetic process in diatoms, the excitation energy funneling within FCPs must be probed. A state-of-the-art multiscale analysis within a quantum mechanics/molecular mechanics framework has been employed. To this end, the chlorophyll (Chl) excitation energies within the FCP complex from the diatom Phaeodactylum tricornutum have been determined. The Chl-c excitation energies were found to be 5-fold more susceptible to electric fields than those of Chl-a pigments and thus are significantly lower in FCP than in organic solvents. This finding challenges the general belief that the excitation energy of Chl-c is always higher than that of Chl-a in FCP proteins and reveals that Chl-c molecules are much more sensitive to electric fields within protein scaffolds than in Chl-a pigments. The analysis of the linear absorption spectrum and the two-dimensional electronic spectra of the FCP complex strongly supports these findings and allows us to study the excitation transfer within the FCP complex.
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Diatomeas , Diatomeas/metabolismo , Clorofila/química , Clorofila A/metabolismo , Fotosíntesis , Proteínas de Unión a Clorofila/química , Complejos de Proteína Captadores de Luz/químicaRESUMEN
Photosystem II (PSII) is an integral part of the photosynthesis machinery, in which several light-harvesting complexes rely on inter-complex excitonic energy transfer (EET) processes to channel energy to the reaction center. In this paper, we report on a direct observation of the inter-complex EET in a minimal PSII supercomplex from plants, containing the trimeric light-harvesting complex II (LHCII), the monomeric light-harvesting complex CP26, and the monomeric PSII core complex. Using two-dimensional (2D) electronic spectroscopy, we measure an inter-complex EET timescale of 50 picoseconds for excitations from the LHCII-CP26 peripheral antenna to the PSII core. The 2D electronic spectra also reveal that the transfer timescale is nearly constant over the pump spectrum of 600 to 700 nanometers. Structure-based calculations reveal the contribution of each antenna complex to the measured inter-complex EET time. These results provide a step in elucidating the full inter-complex energy transfer network of the PSII machinery.
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Clorofila , Complejo de Proteína del Fotosistema II , Complejo de Proteína del Fotosistema II/química , Clorofila/metabolismo , Fotosíntesis , Tilacoides/metabolismo , Plantas/metabolismo , Transferencia de EnergíaRESUMEN
The aim of this study is to investigate the photophysical properties of a cyanine dye analogue by performing first-principles calculations based on density functional theory (DFT) and time dependent-DFT. Cationic cyanine dyes are the subject of great importance due to their versatile applications and the tunability of their photophysical properties, such as by modifying their end groups and chain length. An example of this is the vinylene shift, which is experimentally known for these molecules, and it consists of a bathochromic (red) shift of approximately 100 nm of the 0-0 vibronic transition when a vinyl group is added to the polymethine chain. Our study shows that when the saturated moiety C2H4 of the cyclopentene ring is added to the chain, it interacts with the conjugated π-system, resulting in a smaller HOMO-LUMO gap. Here, we demonstrate the origin of this interaction and how it can be used to fine tune the absorption energies of this class of dyes.
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The manipulation of the ultrafast quantum dynamics of a molecular system can be achieved through the application of tailored light fields. This has been done in many ways in the past. In our present investigation, we show that it is possible to exert specific control over the nonadiabatic dynamics of a generic model system describing ultrafast charge-transfer within a condensed dissipative environment by using frequency-chirped pulses. By adjusting the external photoexcitation conditions, such as the chirp parameter, we show that the final population of the excitonic and charge-transfer states can be significantly altered, thereby influencing the elementary steps controlling the transfer process. In addition, we introduce an excitation scheme based on double-pump time-resolved fluorescence spectroscopy using chirped-pulse excitations. Here, our findings reveal that chirped excitations enhance the vibrational system dynamics as evidenced by the simulated spectra, where a substantial signal intensity dependence on the chirp is observed. Our simulations show that chirped pulses are a promising tool for steering the dynamics of the charge-transfer process toward a desired target outcome.
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Molecular self-assembly is a fundamental process in nature that can be used to develop novel functional materials for medical and engineering applications. However, their complex mechanisms make the short-lived stages of self-assembly processes extremely hard to reveal. In this article, we track the self-assembly process of a benchmark system, double-walled molecular nanotubes, whose structure is similar to that found in biological and synthetic systems. We selectively dissolved the outer wall of the double-walled system and used the inner wall as a template for the self-reassembly of the outer wall. The reassembly kinetics were followed in real time using a combination of microfluidics, spectroscopy, cryogenic transmission electron microscopy, molecular dynamics simulations, and exciton modeling. We found that the outer wall self-assembles through a transient disordered patchwork structure: first, several patches of different orientations are formed, and only on a longer time scale will the patches interact with each other and assume their final preferred global orientation. The understanding of patch formation and patch reorientation marks a crucial step toward steering self-assembly processes and subsequent material engineering.
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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.
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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 â¼3 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.
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We introduce a first-principles model of the 12-mer poly-3-hexyltiophene (P3HT) polymer system in the realistic description of an organic photovoltaic blend environment. We combine Molecular Dynamics (MD) simulations of a thin-film blend of P3HT and phenyl-C61-butyric acid methyl ester (PCBM) to model the interactions with a fluctuating environment with Time-Dependent Density Functional Theory (TDDFT) calculations to parametrize the effect of the torsional flexibility in the polymer and construct an exciton-type Hamiltonian that describes the photoexcitation of the polymer. This allows us to reveal the presence of different flexibility patterns governed by the torsional angles along the polymer chain which, in the interacting fluctuating environment, control the broadening of the spectral observables. We identify the origin of the homogeneous and inhomogeneous line shape of the simulated optical signals. This is paramount to decipher the spectroscopic nature of the ultrafast electron-transfer process occurring in organic photovoltaic (OPV) materials.
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The excitation energy transfer (EET) process for photosynthetic antenna complexes consisting of subunits, each comprised of multiple chromophores, remains challenging to describe. The multichromophoric Förster resonance energy transfer theory is a popular method to describe the EET process in such systems. This paper presents a new time-domain method for calculating energy transfer based on the combination of multichromophoric Förster resonance energy transfer theory and the Numerical Integration of the Schrödinger Equation method. After validating the method on simple model systems, we apply it to the Light-Harvesting antenna 2 (LH2) complex, a light harvesting antenna found in purple bacteria. We use a simple model combining the overdamped Brownian oscillators to describe the dynamic disorder originating from the environmental fluctuations and the transition charge from the electrostatic potential coupling model to determine the interactions between chromophores. We demonstrate that with this model, both the calculated spectra and the EET rates between the two rings within the LH2 complex agree well with experimental results. We further find that the transfer between the strongly coupled rings of neighboring LH2 complexes can also be well described with our method. We conclude that our new method accurately describes the EET rate for biologically relevant multichromophoric systems, which are similar to the LH2 complex. Computationally, the new method is very tractable, especially for slow processes. We foresee that the method can be applied to efficiently calculate transfer in artificial systems as well and may pave the way for calculating multidimensional spectra of extensive multichromophoric systems in the future.
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Two-dimensional infrared Raman spectroscopy is a powerful technique for studying the structure and interaction in molecular and biological systems. Here, we present a new implementation of the simulation of the two-dimensional infrared Raman signals. The implementation builds on the numerical integration of the Schrödinger equation approach. It combines the prediction of dynamics from molecular dynamics with a map-based approach for obtaining Hamiltonian trajectories and response function calculations. The new implementation is tested on the amide-I region for two proteins, where one is dominated by α-helices and the other by ß-sheets. We find that the predicted spectra agree well with experimental observations. We further find that the two-dimensional infrared Raman spectra at least of the studied proteins are much less sensitive to the laser polarization used compared to conventional two-dimensional infrared experiments. The present implementation and findings pave the way for future applications for the interpretation of two-dimensional infrared Raman spectra.
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Proteínas , Espectrometría Raman , Proteínas/química , Amidas/química , Simulación de Dinámica Molecular , Espectrofotometría Infrarroja/métodosRESUMEN
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.
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Hybrid inorganic-organic perovskites have attracted considerable attention over recent years as promising processable electronic materials. In particular, the rich structural dynamics of these 'soft' materials has become a subject of investigation and debate due to their direct influence on the perovskites' optoelectronic properties. Significant effort has focused on understanding the role and behaviour of the organic cations within the perovskite, as their rotational dynamics may be linked to material stability, heterogeneity and performance in (opto)electronic devices. To this end, we use two-dimensional IR spectroscopy (2DIR) to understand the effect of partial caesium alloying on the rotational dynamics of the methylammonium cation in the archetypal hybrid perovskite CH3NH3PbI3. We find that caesium incorporation primarily inhibits the slower 'reorientational jump' modes of the organic cation, whilst a smaller effect on the fast 'wobbling time' may be due to distortions and rigidisation of the inorganic cuboctahedral cage. 2DIR centre-line-slope analysis further reveals that while static disorder increases with caesium substitution, the dynamic disorder (reflected in the phase memory of the N-H stretching mode of methylammonium) is largely independent of caesium addition. Our results contribute to the development of a unified model of cation dynamics within organohalide perovskites.
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In contrast to regular J- and H-aggregates, thin film squaraine aggregates usually have broad absorption spectra containing both J-and H-like features, which are favorable for organic photovoltaics. Despite being successfully applied in organic photovoltaics for years, a clear interpretation of these optical properties by relating them to specific excited states and an underlying aggregate structure has not been made. In this work, by static and transient absorption spectroscopy on aggregated n-butyl anilino squaraines, we provide evidence that both the red- and blue-shifted peaks can be explained by assuming an ensemble of aggregates with intermolecular dipole-dipole resonance interactions and structural disorder deriving from the four different nearest neighbor alignmentsâin sharp contrast to previous association of the peaks with intermolecular charge-transfer interactions. In our model, the next-nearest neighbor dipole-dipole interactions may be negative or positive, which leads to the occurrence of J- and H-like features in the absorption spectrum. Upon femtosecond pulse excitation of the aggregated sample, a transient absorption spectrum deviating from the absorbance spectrum emerges. The deviation finds its origin in the excitation of two-exciton states by the probe pulse. The lifetime of the exciton is confirmed by the band integral dynamics, featuring a single-exponential decay with a lifetime of 205 ps. Our results disclose the aggregated structure and the origin of red- and blue-shifted peaks and explain the absence of photoluminescence in squaraine thin films. Our findings underline the important role of structural disorder of molecular aggregates for photovoltaic applications.
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Ciclobutanos , Análisis Espectral , Vibración , FenolesRESUMEN
We measure the two-dimensional electronic spectra of the LHCII(M)-CP29-CP24 complex in photosystem II (PSII) and provide the first study of the ultrafast excitation energy transfer (EET) processes of an asymmetric and native light-harvesting assembly of the antenna of PSII. With comparisons to LHCII, we observe faster energy equilibrations in the intermediate levels of the LHCII(M)-CP29-CP24 complex at 662 and 670 nm. Notably, the putative "bottleneck" states in LHCII exhibit faster effective dynamics in the LHCII(M)-CP24-CP29 complex, with the average lifetime shortening from 2.5 ps in LHCII to 1.2 ps in the bigger assembly. The observations are supported by high-level structure-based calculations, and the accelerated dynamics can be attributed to the structural change of LHCII(M) in the bigger complex. This study shows that the biological functioning structures of the complexes are important to understand the overall EET dynamics of the PSII supercomplex.
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Complejos de Proteína Captadores de Luz , Complejo de Proteína del Fotosistema II , Transferencia de Energía , Complejos de Proteína Captadores de Luz/química , Complejo de Proteína del Fotosistema II/metabolismo , Plantas/metabolismo , TilacoidesRESUMEN
Here, we present a new analysis program, AIM, that allows extracting the vibrational amide-I Hamiltonian using molecular dynamics trajectories for protein infrared spectroscopy modeling. The constructed Hamiltonians can be used as input for spectral calculations allowing the calculation of infrared absorption spectra, vibrational circular dichroism, and two-dimensional infrared spectra. These spectroscopies allow the study of the structure and dynamics of proteins. We will explain the essence of how AIM works and give examples of the information and spectra that can be obtained with the program using the Trypsin Inhibitor as an example. AIM is freely available from GitHub, and the package contains a demonstration allowing easy introduction to the use of the program.