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.

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.

Analyzing Lipid Membrane Defects via a Coarse-Grained to Triangulated Surface Map: The Role of Lipid Order and Local Curvature in Molecular Binding.

Lipid packing defects are known to serve as quantitative indicators for protein binding to lipid membranes. This paper presents a protocol for mapping molecular lipid detail onto a triangulated continuum leaflet representation. Besides establishing the desired forward counterpart to the existing inverse TS2CG map, this coarse-grained to triangulated surface (CG2TS) map enables straightforward extraction of the defect characteristics for any membrane geometry found in nature. We have applied our protocol to investigate the role of local curvature and varying lipid packing on the defect constant π. We find that the defect size is greatly influenced by both factors, arguing strongly against the usual assignment of a single defect constant in the case of more realistic membrane conditions. An important discovery is that lipids in the gel phase produce larger defects, or a higher π, in domains of high (local) curvature than the same lipid in a liquid phase of any curvature. This finding suggests that membranes featuring very ordered lipid packing can bind proteins via large defects in curved regions. Finally, we propose a route for estimating defect constants directly from the standard membrane properties. Identifying the precise role of composition, lipid (tail) order, and (local) curvature in defects for the irregular lipid structures that are (temporally) present in many biological processes is instrumental for obtaining fundamental insight as well as for a rational design of membrane binding targets.

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.

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.

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.

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.

A Core-Shell Approach for Systematically Coarsening Nanoparticle-Membrane Interactions: Application to Silver Nanoparticles.

The continuous release of engineered nanomaterial (ENM) into the environment may bring about health concerns following human exposure. One important source of ENMs are silver nanoparticles (NPs) that are extensively used as anti-bacterial additives. The introduction of ENMs into the human body can occur via ingestion, skin uptake or the respiratory system. Therefore, evaluating how NPs translocate over bio-membranes is essential in assessing their primary toxicity. Unfortunately, data regarding membrane-NP interaction is still scarce, as is theoretical and in silico insight into what governs adhesion and translocation for the most relevant NPs and membranes. Coarse-grained (CG) molecular descriptions have the potential to alleviate this situation, but are hampered by the absence of a direct link to NP materials and membrane adhesion mechanisms. Here, we interrogate the relationship between the most common NP representation at the CG level and the adhesion characteristics of a model lung membrane. We find that this representation for silver NPs is non-transferable, meaning that a proper CG representation for one size is not suited for other sizes. We also identify two basic types of primary adhesion-(partial) NPs wrapping by the membrane and NP insertion into the membrane-that closely relate to the overall NP hydrophobicity and significantly differ in terms of lipid coatings. The proven non-transferability of the standard CG representation with size forms an inspiration for introducing a core-shell model even for bare NPs that are uniform in composition. Using existing all-atom molecular dynamics (MD) data as a reference, we show that this extension does allow us to reproduce size-dependent NP adhesion properties and lipid responses to NP binding at the CG level. The subsequent CGMD evaluation for 10 nm Ag NPs provides new insight into membrane binding for relevant NP sizes and into the role of water in trapping NPs into defected mixed monolayer-bilayer states. This development will be instrumental for simulating NP-membrane adhesion towards more experimentally relevant length and time scales for particular NP materials.

Predicted Adsorption Affinity for Enteric Microbial Metabolites to Metal and Carbon Nanomaterials.

Ingested nanomaterials are exposed to many metabolites that are produced, modified, or regulated by members of the enteric microbiota. The adsorption of these metabolites potentially affects the identity, fate, and biodistribution of nanomaterials passing the gastrointestinal tract. Here, we explore these interactions using in silico methods, focusing on a concise overview of 170 unique enteric microbial metabolites which we compiled from the literature. First, we construct quantitative structure-activity relationship (QSAR) models to predict their adsorption affinity to 13 metal nanomaterials, 5 carbon nanotubes, and 1 fullerene. The models could be applied to predict log k values for 60 metabolites and were particularly applicable to 'phenolic, benzoyl and phenyl derivatives', 'tryptophan precursors and metabolites', 'short-chain fatty acids', and 'choline metabolites'. The correlations of these predictions to biological surface adsorption index descriptors indicated that hydrophobicity-driven interactions contribute most to the overall adsorption affinity, while hydrogen-bond interactions and polarity/polarizability-driven interactions differentiate the affinity to metal and carbon nanomaterials. Next, we use molecular dynamics (MD) simulations to obtain direct molecular information for a selection of vitamins that could not be assessed quantitatively using QSAR models. This showed how large and flexible metabolites can gain stability on the nanomaterial surface via conformational changes. Additionally, unconstrained MD simulations provided excellent support for the main interaction types identified by QSAR analysis. Combined, these results enable assessing the adsorption affinity for many enteric microbial metabolites quantitatively and support the qualitative assessment of an even larger set of complex and biologically relevant microbial metabolites to carbon and metal nanomaterials.

The role of chirality and plastic crystallinity in the optical and mechanical properties of chlorosomes.

The most efficient light-harvesting antennae found in nature, chlorosomes, are molecular tubular aggregates (TMAs) assembled by pigments without protein scaffolds. Here, we discuss a classification of chlorosomes as a unique tubular plastic crystal and we attribute the robust energy transfer in chlorosomes to this unique nature. To systematically study the role of supramolecular tube chirality by molecular simulation, a role that has remained unresolved, we share a protocol for generating realistic tubes at atomic resolution. We find that both the optical and the mechanical behavior are strongly dependent on chirality. The optical-chirality relation enables a direct interpretation of experimental spectra in terms of overall tube chirality. The mechanical response shows that the overall chirality regulates the hardness of the tube and provides a new characteristic for relating chlorosomes to distinct chirality. Our protocol also applies to other TMA systems and will inspire other systematic studies beyond lattice models.

Liposome fusion with orthogonal coiled coil peptides as fusogens: the efficacy of roleplaying peptides.

Biological membrane fusion is a highly specific and coordinated process as a multitude of vesicular fusion events proceed simultaneously in a complex environment with minimal off-target delivery. In this study, we develop a liposomal fusion model system with specific recognition using lipidated derivatives of a set of four de novo designed heterodimeric coiled coil (CC) peptide pairs. Content mixing was only obtained between liposomes functionalized with complementary peptides, demonstrating both fusogenic activity of CC peptides and the specificity of this model system. The diverse peptide fusogens revealed important relationships between the fusogenic efficacy and the peptide characteristics. The fusion efficiency increased from 20% to 70% as affinity between complementary peptides decreased, (from K F ≈ 108 to 104 M-1), and fusion efficiency also increased due to more pronounced asymmetric role-playing of membrane interacting 'K' peptides and homodimer-forming 'E' peptides. Furthermore, a new and highly fusogenic CC pair (E3/P1K) was discovered, providing an orthogonal peptide triad with the fusogenic CC pairs P2E/P2K and P3E/P3K. This E3/P1k pair was revealed, via molecular dynamics simulations, to have a shifted heptad repeat that can accommodate mismatched asparagine residues. These results will have broad implications not only for the fundamental understanding of CC design and how asparagine residues can be accommodated within the hydrophobic core, but also for drug delivery systems by revealing the necessary interplay of efficient peptide fusogens and enabling the targeted delivery of different carrier vesicles at various peptide-functionalized locations.

Aggregation of Lipid A Variants: A Hybrid Particle-Field Model.

Lipid A is one of the three components of bacterial lipopolysaccharides constituting the outer membrane of Gram-negative bacteria, and is recognized to have an important biological role in the inflammatory response of mammalians. Its biological activity is modulated by the number of acyl-chains that are present in the lipid and by the dielectric medium, i.e., the type of counter-ions, through electrostatic interactions. In this paper, we report on a coarse-grained model of chemical variants of Lipid A based on the hybrid particle-field/molecular dynamics approach (hPF-MD). In particular, we investigate the stability of Lipid A bilayers for two different hexa- and tetra-acylated structures. Comparing particle density profiles along bilayer cross-sections, we find good agreement between the hPF-MD model and reference all-atom simulation for both chemical variants of Lipid A. hPF-MD models of constituted bilayers composed by hexa-acylated Lipid A in water are stable within the simulation time. We further validate our model by verifying that the phase behavior of Lipid A/counterion/water mixtures is correctly reproduced. In particular, hPF-MD simulations predict the correct self-assembly of different lamellar and micellar phases from an initially random distribution of Lipid A molecules with counterions in water. Finally, it is possible to observe the spontaneous formation and stability of Lipid A vesicles by fusion of micellar aggregates.

Unfolding the prospects of computational (bio)materials modeling.

In this perspective communication, we briefly sketch the current state of computational (bio)material research and discuss possible solutions for the four challenges that have been increasingly identified within this community: (i) the desire to develop a unified framework for testing the consistency of implementation and physical accuracy for newly developed methodologies, (ii) the selection of a standard format that can deal with the diversity of simulation data and at the same time simplifies data storage, data exchange, and data reproduction, (iii) how to deal with the generation, storage, and analysis of massive data, and (iv) the benefits of efficient "core" engines. Expressed viewpoints are the result of discussions between computational stakeholders during a Lorentz center workshop with the prosaic title Workshop on Multi-scale Modeling and are aimed at (i) improving validation, reporting and reproducibility of computational results, (ii) improving data migration between simulation packages and with analysis tools, (iii) popularizing the use of coarse-grained and multi-scale computational tools among non-experts and opening up these modern computational developments to an extended user community.

Dynamic Disorder Drives Exciton Transfer in Tubular Chlorosomal Assemblies.

Chlorosomes stand out for their highly efficient excitation energy transfer (EET) in extreme low light conditions. Yet, little is known about the EET when a chlorosome is excited to a pure state that is an eigenstate of the exciton Hamiltonian. In this work, we consider the dynamic disorder in the intermolecular electronic coupling explicitly by calculating the electronic coupling terms in the Hamiltonian using nuclear coordinates that are taken from molecular dynamics simulation trajectories. We show that this dynamic disorder is capable of driving the evolution of the exciton, being a stationary state of the initial Hamiltonian. In particular, long-distance excitation energy transfer between domains of high exciton population and oscillatory behavior of the population in the site basis are observed, in line with two-dimensional electronic spectroscopy studies. We also found that in the high exciton population domains, their population variation is correlated with their overall coupling strength. Analysis in a reference state basis shows that such dynamic disorder, originating from thermal energy, creates a fluctuating landscape for the exciton and promotes the EET process. We propose such dynamic disorder as an important microscopic origin for the high efficient EET widely observed in different types of chlorosomes, bioinspired tubular aggregates, or other light-harvesting complexes.

Power generation by reverse electrodialysis in a single-layer nanoporous membrane made from core-rim polycyclic aromatic hydrocarbons.

Nanoporous graphene and related atomically thin layered materials are promising candidates in reverse electrodialysis research owing to their remarkable ionic conductivity and high permselectivity. The synthesis of atomically thin nanoporous membranes with a narrow pore size distribution, however, remains challenging. Here, we report the fabrication of nanoporous carbon membranes via the thermal crosslinking of core-rim structured monomers, that is, polycyclic aromatic hydrocarbons. The mechanically robust, centimetre-sized membrane has a pore size of 3.6 ± 1.8 nm and a thickness of 2.0 ± 0.5 nm. When applied to reverse electrodialysis, the nanoporous carbon membrane offers a high short-circuit current with an output power density of 67 W m-2, which is about two orders of magnitude beyond that of the classic ion-exchange membranes and current prototype nanoporous membranes reported in the literature. Crosslinked and atomically thin porous polycyclic aromatic hydrocarbon membranes therefore represent new scaffolds that will revolutionize the rapidly developing fields of sustainable energy and membrane technology.

Contrasting Modes of Self-Assembly and Hydrogen-Bonding Heterogeneity in Chlorosomes of Chlorobaculum tepidum.

Chlorosome antennae form an interesting class of materials for studying the role of structural motifs and dynamics in nonadiabatic energy transfer. They perform robust and highly quantum-efficient transfer of excitonic energy while allowing for compositional variation and completely lacking the usual regulatory proteins. Here, we first cast the geometrical analysis for ideal tubular scaffolding models into a formal framework, to relate effective helical properties of the assembly structures to established characterization data for various types of chlorosomes. This analysis shows that helicity is uniquely defined for chlorosomes composed of bacteriochlorophyll (BChl) d and that three chiral angles are consistent with the nuclear magnetic resonance (NMR) and electron microscope data for BChl c, including two novel ones that are at variance with current interpretations of optical data based on perfect cylindrical symmetry. We use this information as a starting point for investigating dynamic and static heterogeneity at the molecular level by unconstrained molecular dynamics. We first identify a rotational degree of freedom, along the Mg-OH coordination bond, that alternates along the syn-anti stacks and underlies the (flexible) curvature on a larger scale. Because rotation directly relates to the formation or breaking of interstack hydrogen bonds of the O-H···O=C structural motif along the syn-anti stacks, we analyzed the relative fractions of hydrogen-bonded and the nonbonded regions, forming stripe domains in otherwise spectroscopically homogeneous curved slabs. The ratios 7:3 for BChl c and 9:1 for BChl d for the two distinct structural components agree well with the signal intensities determined by NMR. In addition, rotation with curvature-independent formation of stripe domains offers a viable explanation for the localization and dispersion of exciton states over two fractions, as observed in single chlorosome fluorescence decay studies.

Biomembrane solubilization mechanism by Triton X-100: a computational study of the three stage model.

The solubilization mechanism of lipid membranes in the presence of Triton X-100 (TX-100) is investigated at molecular resolution using molecular dynamics (MD) simulations. Thanks to the large time and length scales accessible by the hybrid particle-field formulation of the models employed here, the complex process of membrane solubilization has been studied, with the goal of verifying the three stage model reported in the literature. DPPC lipid bilayers and vesicles have been studied at different concentrations of the TX-100 detergent employing coarse grained (CG) models. Systems up to ∼600.000 beads, corresponding to more than 2 millions heavy atoms, have been simulated. Moreover, in order to clarify several experimental pieces of evidence, both slow and fast detergent partition scenarios have been investigated. Flat and curved (vesicles) lipid bilayer surfaces, interacting with TX-100, have been considered to study the curvature effects on the detergent partition rate in the membrane. Shape and conformational changes of mixed DPPC/TX-100 vesicles, as a function of TX-100 content, have also been studied. In particular, high curvature surfaces, corresponding to a higher local TX-100 content, promote a membrane rupture. In flat lipid surfaces, on the time scale simulated the detergent partition is almost absent, following a different pathway of the solubilization membrane mechanism.

Specific features of defect structure and dynamics in the cylinder phase of block copolymers.

We present a systematic study of defects in thin films of cylinder-forming block copolymers upon long-term thermal or solvent annealing. In particular, we consider in detail the peculiarities of both classical and specific topological defects, and conclude that there is a strong "defect structure-chain mobility" relationship in block copolymers. In the systems studied, representative defect configurations provide connectivity of the minority phase in the form of dislocations with a closed cylinder end or classical disclinations with incorporated alternative, nonbulk structures with planar symmetry. In solvent-annealed films with enhanced chain mobility, the neck defects (bridges between parallel cylinders) were observed. This type of nonsingular defect has not been identified in block copolymer systems before. We argue that topological arguments and 2D defect representation, sufficient for lamellar systems, are not sufficient to determine the stability and mobility of defects in the cylindrical phase. In-situ scanning force microscopy measurements are compared with the simulations based on the dynamic self-consistent mean field theory. The close match between experimental measurements and simulation results suggests that the lateral defect motion is diffusion-driven. In addition, 3D simulations demonstrated that the bottom (wetting) layer is only weakly involved into the structure ordering at the free surface. Finally, the morphological evolution is considered with the focus on the motion and interaction of the representative defect configurations.

Defect evolution in block copolymer thin films via temporal phase transitions.

We study the details of the defect dynamics in thin films of a cylinder-forming polystyrene-block-polybutadiene (SB) diblock copolymer melt. The high temporal resolution of in-situ scanning force microscopy (SFM) uncovers elementary dynamic processes of structural rearrangements on time scales not accessible so far. Short-term interfacial undulations and the formation of transient phases (spheres, perforated lamellae, and lamellae) are observed. We demonstrate that the well-known structural defects are annihilated by short-term phase transitions into what may be considered excited states. These temporary phase transitions are reproduced in simulations based on dynamic self-consistent field theory. We discuss the role of the observed structural evolution in the context of the equilibrium phase behavior in SB thin films.

Mechanism of the transition between lamellar and gyroid phases formed by a diblock copolymer in aqueous solution.

The mechanism of the transition from a lamellar phase to a gyroid phase in an aqueous solution of a diblock copolymer has been studied by time-resolved synchrotron small-angle X-ray scattering. The transition occurs via a metastable perforated lamellar structure. The perforations initially have liquidlike ordering before developing hexagonal packing. The transient phase of irregularly perforated layers is revealed by the development of diffuse scattering peaks, just below the Bragg peaks of the lamellar structure. The diffuse scattering is modeled by Monte Carlo simulations of perforated layers. Following the formation of perforations, Bragg peaks characteristic of a hexagonal structure signal an ordering into a hexagonal lattice (with the concomitant loss of diffuse scattering). Computer simulations based on a dynamic density functional model reproduce these features. The hexagonal perforated lamellar phase is rapidly replaced by the gyroid phase. The domain spacing of the gyroid phase is larger than that of the perforated lamellar structure. The perforated lamellar and gyroid phases coexist for a defined period. The reverse transition from gyroid to lamellae occurs directly, with no transient or metastable intermediates.