Probing the design principles of photosynthetic systems through fluorescence noise measurement.

Elucidating the energetic processes which govern photosynthesis, the engine of life on earth, are an essential goal both for fundamental research and for cutting-edge biotechnological applications. Fluorescent signal of photosynthetic markers has long been utilised in this endeavour. In this research we demonstrate the use of fluorescent noise analysis to reveal further layers of intricacy in photosynthetic energy transfer. While noise is a common tool analysing dynamics in physics and engineering, its application in biology has thus far been limited. Here, a distinct behaviour in photosynthetic pigments across various chemical and biological environments is measured. These changes seem to elucidate quantum effects governing the generation of oxidative radicals. Although our method offers insights, it is important to note that the interpretation should be further validated expertly to support as conclusive theory. This innovative method is simple, non-invasive, and immediate, making it a promising tool to uncover further, more complex energetic events in photosynthesis, with potential uses in environmental monitoring, agriculture, and food-tech.

Chiral Molecular Coating of a LiNiCoMnO2 Cathode for High-Rate Capability Lithium-Ion Batteries.

The growing demand for energy has increased the need for battery storage, with lithium-ion batteries being widely used. Among those, nickel-rich layered lithium transition metal oxides [LiNi1-x-yCoxMnyO2 NCM (1 - x - y > 0.5)] are some of the promising cathode materials due to their high specific capacities and working voltages. In this study, we demonstrate that a thin, simple coating of polyalanine chiral molecules improves the performance of Ni-rich cathodes. The chiral organic coating of the active material enhances the discharge capacity and rate capability. Specifically, NCM811 and NCM622 electrodes coated with chiral molecules exhibit lower voltage hysteresis and better rate performance, with a capacity improvement of >10% at a 4 C discharge rate and an average improvement of 6%. We relate these results to the chirally induced spin selectivity effect that enables us to reduce the resistance of the electrode interface and to reduce dramatically the overpotential needed for the chemical process by aligning the electron spins.

Chiral Induced Spin Selectivity.

Since the initial landmark study on the chiral induced spin selectivity (CISS) effect in 1999, considerable experimental and theoretical efforts have been made to understand the physical underpinnings and mechanistic features of this interesting phenomenon. As first formulated, the CISS effect refers to the innate ability of chiral materials to act as spin filters for electron transport; however, more recent experiments demonstrate that displacement currents arising from charge polarization of chiral molecules lead to spin polarization without the need for net charge flow. With its identification of a fundamental connection between chiral symmetry and electron spin in molecules and materials, CISS promises profound and ubiquitous implications for existing technologies and new approaches to answering age old questions, such as the homochiral nature of life. This review begins with a discussion of the different methods for measuring CISS and then provides a comprehensive overview of molecules and materials known to exhibit CISS-based phenomena before proceeding to identify structure-property relations and to delineate the leading theoretical models for the CISS effect. Next, it identifies some implications of CISS in physics, chemistry, and biology. The discussion ends with a critical assessment of the CISS field and some comments on its future outlook.

Probing chiral discrimination in biological systems using atomic force microscopy: The role of van der Waals and exchange interactions.

We analyze from a theoretical perspective recent experiments where chiral discrimination in biological systems was established using Atomic Force Microscopy (AFM). Even though intermolecular forces involved in AFM measurements have different origins, i.e., electrostatic, bonding, exchange, and multipole interactions, the key molecular forces involved in enantiospecific biorecognition are electronic spin exchange and van der Waals (vdW) dispersion forces, which are sensitive to spin-orbit interaction (SOI) and space-inversion symmetry breaking in chiral molecules. The vdW contribution to chiral discrimination emerges from the inclusion of SOI and spin fluctuations due to the chiral-induced selectivity effect, a result we have recently demonstrated theoretically. Considering these two enantiospecific contributions, we show that the AFM results regarding chiral recognition can be understood in terms of a simple physical model that describes the different adhesion forces associated with different electron spin polarization generated in the (DD), (LL), and (DL) enantiomeric pairs, as arising from the spin part of the exchange and vdW contributions. The model can successfully produce physically reasonable parameters accounting for the vdW and exchange interaction strength, accounting for the chiral discrimination effect. This fact has profound implications in biorecognition where the relevant intermolecular interactions in the intermediate-distance regime are clearly connected to vdW forces.

The structural basis for light acclimation in phycobilisome light harvesting systems systems in Porphyridium purpureum.

Photosynthetic organisms adapt to changing light conditions by manipulating their light harvesting complexes. Biophysical, biochemical, physiological and genetic aspects of these processes are studied extensively. The structural basis for these studies is lacking. In this study we address this gap in knowledge by focusing on phycobilisomes (PBS), which are large structures found in cyanobacteria and red algae. In this study we focus on the phycobilisomes (PBS), which are large structures found in cyanobacteria and red algae. Specifically, we examine red algae (Porphyridium purpureum) grown under a low light intensity (LL) and a medium light intensity (ML). Using cryo-electron microscopy, we resolve the structure of ML-PBS and compare it to the LL-PBS structure. The ML-PBS is 13.6 MDa, while the LL-PBS is larger (14.7 MDa). The LL-PBS structure have a higher number of closely coupled chromophore pairs, potentially the source of the red shifted fluorescence emission from LL-PBS. Interestingly, these differences do not significantly affect fluorescence kinetics parameters. This indicates that PBS systems can maintain similar fluorescence quantum yields despite an increase in LL-PBS chromophore numbers. These findings provide a structural basis to the processes by which photosynthetic organisms adapt to changing light conditions.

Does Coherence Affect the Multielectron Oxygen Reduction Reaction?

The oxygen reduction reaction (ORR) is the key for oxygen-based respiration and the operation of fuel cells. It involves the transmission of two pairs of electrons. We probed what type of interaction between the electrons is required to enable their efficient transfer into the oxygen. We show experimentally that the transfer of the electrons is controlled by the "hidden property" and present a theoretical model suggesting that it is related to coherent phase relations between the two electrons. Using spin polarization electrochemical measurements, with electrodes coated with different thicknesses of chiral coating, we confirm the special relation between the electrons. This relation is destroyed by multiple scattering events that result in the formation of hydrogen peroxide, which indicates a reduction in the ORR efficiency. Another indication for the possible role of coherence is the fluctuations in the reaction efficiency as a function of thickness of the chiral coated electrode.

Chirality-induced avalanche magnetization of magnetite by an RNA precursor.

Homochirality is a hallmark of life on Earth. To achieve and maintain homochirality within a prebiotic network, the presence of an environmental factor acting as a chiral agent and providing a persistent chiral bias to prebiotic chemistry is highly advantageous. Magnetized surfaces are prebiotically plausible chiral agents due to the chiral-induced spin selectivity (CISS) effect, and they were utilized to attain homochiral ribose-aminooxazoline (RAO), an RNA precursor. However, natural magnetic minerals are typically weakly magnetized, necessitating mechanisms to enhance their magnetization for their use as effective chiral agents. Here, we report the magnetization of magnetic surfaces by crystallizing enantiopure RAO, whereby chiral molecules induce a uniform surface magnetization due to the CISS effect, which spreads across the magnetic surface akin to an avalanche. Chirality-induced avalanche magnetization enables a feedback between chiral molecules and magnetic surfaces, which can amplify a weak magnetization and allow for highly efficient spin-selective processes on magnetic minerals.

Bacterial extracellular electron transfer components are spin selective.

Metal-reducing bacteria have adapted the ability to respire extracellular solid surfaces instead of soluble oxidants. This process requires an electron transport pathway that spans from the inner membrane, across the periplasm, through the outer membrane, and to an external surface. Multiheme cytochromes are the primary machinery for moving electrons through this pathway. Recent studies show that the chiral-induced spin selectivity (CISS) effect is observable in some of these proteins extracted from the model metal-reducing bacteria, Shewanella oneidensis MR-1. It was hypothesized that the CISS effect facilitates efficient electron transport in these proteins by coupling electron velocity to spin, thus reducing the probability of backscattering. However, these studies focused exclusively on the cell surface electron conduits, and thus, CISS has not been investigated in upstream electron transfer components such as the membrane-associated MtrA, or periplasmic proteins such as small tetraheme cytochrome (STC). By using conductive probe atomic force microscopy measurements of protein monolayers adsorbed onto ferromagnetic substrates, we show that electron transport is spin selective in both MtrA and STC. Moreover, we have determined the spin polarization of MtrA to be ∼77% and STC to be ∼35%. This disparity in spin polarizations could indicate that spin selectivity is length dependent in heme proteins, given that MtrA is approximately two times longer than STC. Most significantly, our study indicates that spin-dependent interactions affect the entire extracellular electron transport pathway.

Biobased Electronics: Tunable Dielectric and Piezoelectric Cellulose Nanocrystal-Protein Films.

Cellulose has been a go-to material for its dielectric properties from the onset of capacitor development. The demand for an energy storage solution continues to grow, but the supply remains limited and relies too often on fossil and mined materials. This work proposes a fully sustainable and green method with which to produce dielectric thin films made of renewable and degradable materials. Cellulose nanocrystals (CNC) made an excellent matrix for the dispersion of proteins and the fabrication of robust transparent thin films with enhanced dielectric permittivity. A range of proteins sources, additives and concentrations allowed for us to control the dielectric permittivity from εr = 4 to 50. The proteins screened came from animal and plant sources. The films were formed from drying a water suspension of the CNC and proteins through evaporation-induced self-assembly. This yielded nano-layered structures with very high specific surface areas, ideal for energy storage devices. The resulting films were characterized with respect to the electrical, mechanical, piezoelectric, and optical properties to be compared. Electrically conductive (σ = 1.53 × 103 S/m) CNC films were prepared with carbon nanotubes (CNT). The fabricated films were used to make flexible, sustainable, and degradable capacitors by layering protein-based films between CNC-CNT composite films.

Magneto-optical imaging of magnetic-domain pinning induced by chiral molecules.

Chiral molecules have the potential for creating new magnetic devices by locally manipulating the magnetic properties of metallic surfaces. When chiral polypeptides chemisorb onto ferromagnets, they can induce magnetization locally by spin exchange interactions. However, direct imaging of surface magnetization changes induced by chiral molecules was not previously realized. Here, we use magneto-optical Kerr microscopy to image domains in thin films and show that chiral polypeptides strongly pin domains, increasing the coercive field locally. In our study, we also observe a rotation of the easy magnetic axis toward the out-of-plane, depending on the sample's domain size and the adsorption area. These findings show the potential of chiral molecules to control and manipulate magnetization and open new avenues for future research on the relationship between chirality and magnetization.

Nuclear spin effects in biological processes.

Traditionally, nuclear spin is not considered to affect biological processes. Recently, this has changed as isotopic fractionation that deviates from classical mass dependence was reported both in vitro and in vivo. In these cases, the isotopic effect correlates with the nuclear magnetic spin. Here, we show nuclear spin effects using stable oxygen isotopes (16O, 17O, and 18O) in two separate setups: an artificial dioxygen production system and biological aquaporin channels in cells. We observe that oxygen dynamics in chiral environments (in particular its transport) depend on nuclear spin, suggesting future applications for controlled isotope separation to be used, for instance, in NMR. To demonstrate the mechanism behind our findings, we formulate theoretical models based on a nuclear-spin-enhanced switch between electronic spin states. Accounting for the role of nuclear spin in biology can provide insights into the role of quantum effects in living systems and help inspire the development of future biotechnology solutions.

Modification of Weak Localization in Metallic Thin Films Due to the Adsorption of Chiral Molecules.

We perform low-temperature magneto-conductance measurements on Cu and Au thin films with adsorbed chiral molecules and investigate their phase-coherent transport properties. Upon adsorption of chiral molecules, the spin-orbit coupling strength in Cu decreases and the Au films become ferromagnetic as evident from weak localization and antilocalization data. A theoretical model indicates that anisotropy in the molecular tilt angles, provided that the chiral molecules act as magnetic moments, induces a nonvanishing magnetic exchange interaction, causing changes in the spin-orbit coupling strength in Cu and Au. Our work adds a new viewpoint to the plethora of unique phenomena emerging from chiral molecule adsorption on materials.

Mosquito bite prevention through self-assembled cellulose nanocrystals.

Mosquitoes are the deadliest of all combined insects and animals affecting millions and killing hundreds or thousands of people each year. Existing protection methods however are limited and include volatile compounds that actively repel mosquitoes such as N,N-Diethyl-meta-toluamide (DEET) or different essential oils such as geraniol and citronella. Most are odorous compounds and require organic solvents for dispersion. This work investigates the barrier properties of cellulose nanocrystals (CNCs). CNCs are known to self-assemble in strong, transparent, chemical barrier films. They are fully bio-based, and their surface chemistry is ideal for aqueous dispersion of many compounds. This work saw a significant 80% decrease in feeding on human skin when a thin CNC coat was applied. The effect was further confirmed by artificial feeding on Aedes aegypti wherein CNC appears to act as a chemical camouflage to the many cues sought by the insects. The combined effect of CNC with indole reduced egg laying post exposure to mammalian blood close to null with 99.4% less eggs as compared to control. The chemical barrier effect was assessed through a simple headspace experiment showing that the same CNC coat blocked the passage of ammonium hydroxide vapor, a commonly used mosquito attractant, when applied on a filter paper membrane.

Spin Polarization of Polyalanine Molecules in 2D and Dimer-Row Assemblies Adsorbed on Magnetic Substrates: The Role of Coupling, Chirality, and Coordination.

Propagation of electrons along helical molecules adsorbed on surfaces comes along with a robust spin polarization effect called chirality induced spin selectivity CISS. However, experiments on the molecular scale that allow a true correlation of spin effects with the molecular structure are quite rare. Here we have studied the structure of self-assembled chiral molecules and the electronic transmission and spin polarization of the current through the system by means of ambient scanning tunneling microscopy and spectroscopy in heterostructures of various α-helix polyalanine-based molecules (PA) adsorbed on Al2O3/Pt/Au/Co/Au substrates with perpendicular magnetic anisotropy. We have found a phase separation of the molecules into well-ordered enantiopure 2D hexagonal phases and quasi-1D heterochiral-dimer structures, which allows for the analysis of the spin polarization with almost atomic precision of PA in different phases. The spin polarization reaches up to 75% for chemisorbed molecules arranged in a hexagonal phase. On the contrary, for weakly coupled PA molecules without cysteine anchoring groups in a quasi-1D phase, a spin polarization of around 50% was found. Our results show that both the intermolecular interaction as well as the coupling to the substrate are important and point out that collective effects within the molecules and at the interfaces are required to achieve a high chiral induced spin selectivity.

Optical Activity and Spin Polarization: The Surface Effect.

Chirality ('handedness') is a property that underlies a broad variety of phenomena in nature. Chiral molecules appear in two forms, and each is a mirror image of the other, the two enantiomers. The chirality of molecules is associated with their optical activity, and circular dichroism is commonly applied to identify the handedness of chiral molecules. Recently, the chiral induced spin selectivity (CISS) effect was established, according to which transfer of electrons within chiral molecules depends on the electron's spin. Which spin is preferred depends on the handedness of the chiral molecule and the direction of motion of the electron. Several experiments in the past indicated that there may be a relation between the optical activity of the molecules and their spin selectivity. Here, we show that for a molecule containing several stereogenic axes, when adsorbed on a metal substrate, the peaks in the CD spectra have the same signs for the two enantiomers. This is not the case when the molecules are adsorbed on a nonmetallic substrate or dissolved in solution. Quantum chemical simulations are able to explain the change in the CD spectra upon adsorption of the molecules on conductive and nonconductive surfaces. Surprisingly, the CISS properties are similar for the two enantiomers when adsorbed on the metal substrate, while when the molecules are adsorbed on nonmetallic surface, the preferred spin depends on the molecule handedness. This correlation between the optical activity and the CISS effect indicates that the CISS effect relates to the global polarizability of the molecule.

Ultrafast Coherent Delocalization Revealed in Multilayer QDs under a Chiral Potential.

In recent years, it was found that current passing through chiral molecules exhibits spin preference, an effect known as Chiral Induced Spin Selectivity (CISS). The effect also enables the reduction of scattering and therefore enhances delocalization. As a result, the delocalization of an exciton generated in the dots is not symmetric and relates to the electronic and hole excited spins. In this work utilizing fast spectroscopy on hybrid multilayered QDs with a chiral polypeptide linker system, we probed the interdot chiral coupling on a short time scale. Surprisingly, we found strong coherent coupling and delocalization despite having long 4-nm chiral linkers. We ascribe the results to asymmetric delocalization that is controlled by the electron spin. The effect is not measured when using shorter nonchiral linkers. As the system mimics light-harvesting antennas, the results may shed light on a mechanism of fast and efficient energy transfer in these systems.

The effect of spin exchange interaction on protein structural stability.

Partially charged chiral molecules act as spin filters, with preference for electron transport toward one type of spin ("up" or "down"), depending on their handedness. This effect is named the chiral induced spin selectivity (CISS) effect. A consequence of this phenomenon is spin polarization concomitant with electric polarization in chiral molecules. These findings were shown by adsorbing chiral molecules on magnetic surfaces and investigating the spin-exchange interaction between the surface and the chiral molecule. This field of study was developed using artificial chiral molecules. Here we used such magnetic surfaces to explore the importance of the intrinsic chiral properties of proteins in determining their stability. First, proteins were adsorbed on paramagnetic and ferromagnetic nanoparticles in a solution, and subsequently urea was gradually added to induce unfolding. The structural stability of proteins was assessed using two methods: bioluminescence measurements used to monitor the activity of the Luciferase enzyme, and fast spectroscopy detecting the distance between two chromophores implanted at the termini of a Barnase core. We found that interactions with magnetic materials altered the structural and functional resilience of the natively folded proteins, affecting their behavior under varying mild denaturing conditions. Minor structural disturbances at low urea concentrations were impeded in association with paramagnetic nanoparticles, whereas at higher urea concentrations, major structural deformation was hindered in association with ferromagnetic nanoparticles. These effects were attributed to spin exchange interactions due to differences in the magnetic imprinting properties of each type of nanoparticle. Additional measurements of proteins on macroscopic magnetic surfaces support this conclusion. The results imply a link between internal spin exchange interactions in a folded protein and its structural and functional integrity on magnetic surfaces. Together with the accumulating knowledge on CISS, our findings suggest that chirality and spin exchange interactions should be considered as additional factors governing protein structures.

Large-scale FRET simulations reveal the control parameters of phycobilisome light-harvesting complexes.

Phycobilisomes (PBS) are massive structures that absorb and transfer light energy to photochemical reaction centres. Among the range of light harvesting systems, PBS are considered to be excellent solutions for absorption cross-sections but relatively inefficient energy transferring systems. This is due to the combination of a large number of chromophores with intermediate coupling distances. Nevertheless, PBS systems persisted from the origin of oxygenic photosynthesis to present-day cyanobacteria and red algae, organisms that account for approximately half of the primary productivity in the ocean. In this study, we modelled energy transfer through subsets of PBS structures, using a comprehensive dynamic Hamiltonian model. Our approach was applied, initially, to pairs of phycobilin hexamers and then extended to short rods. By manipulating the distances and angles between the structures, we could probe the dynamics of exciton transfer. These simulations suggest that the PBS chromophore network enhances energy distribution over the entire PBS structure-both horizontally and vertically to the rod axis. Furthermore, energy transfer was found to be relatively immune to the effects of distances or rotations, within the range of intermediate coupling distances. Therefore, we suggest that the PBS provides unique advantages and flexibility to aquatic photosynthesis.

Controlling photosynthetic energy conversion by small conformational changes.

Control phenomena in biology usually refer to changes in gene expression and protein translation and modification. In this paper, another mode of regulation is highlighted; we propose that photosynthetic organisms can harness the interplay between localization and delocalization of energy transfer by utilizing small conformational changes in the structure of light-harvesting complexes. We examine the mechanism of energy transfer in photosynthetic pigment-protein complexes, first through the scope of theoretical work and then by in vitro studies of these complexes. Next, the biological relevance to evolutionary fitness of this localization-delocalization switch is explored by in vivo experiments on desert crust and marine cyanobacteria, which are both exposed to rapidly changing environmental conditions. These examples demonstrate the flexibility and low energy cost of this mechanism, making it a competitive survival strategy.

Enhanced Chiral Sensing at the Few-Molecule Level Using Negative Index Metamaterial Plasmonic Nanocuvettes.

Chirality is a fundamental property of biological molecules and some pharmaceutical molecules. Chiral molecules have a pair of chiral isomers (enantiomers) with opposite handedness. Although both enantiomers of the same molecule have identical chemical and physical properties, one enantiomer may be toxic to living organisms while the other one is harmless. The detection of these enantiomers is done using their small differential absorption between right and left circularly polarized light, known as circular dichroism (CD). Considering the macroscopic size of these molecules, combined with their small differential absorption, the obtained CD signal is very small, imposing a severe limitation on the minimal concentration that can be detected. Chiral plasmonic and metamaterial structures have been used to enhance the sensitivity of CD measurements by orders of magnitude through chiral density hot spots (super chiral fields). However, the large background signal due to these structures' intrinsic chirality limits the effectiveness of these methods. Contrary to absorption-based chiral sensing measurements (CD), fluorescence detection circular dichroism (FDCD) sensing can greatly improve chiral measurement sensitivity, down to the ultimate limit of a few and even a single chiral molecule. Like differential absorption, differential fluorescence also produces a weak signal at the few-chiral-molecule limit. However, here we demonstrate a negative-index metamaterial (NIM) cavity that acts as a "plasmonic nanocuvette" with globally enhanced volume super chiral fields. Moreover, the achiral structure of the plasmonic nanocuvette allows for completely background-free chiral sensing. We show that with NIM-cavity-enhanced FDCD, we can detect as low as a few tens of chiral molecules, well within the zeptomole range.