Natural Photosynthetic Membranes Research Articles

Interfacial organization and phase behavior of mixed galactolipid-DPPC-phytosterol assemblies at the air-water interface and in hydrated mesophases

The structural behavior of model assemblies composed of monogalactosyldiacylglycerol (MGDG) and digalactosyldiacylglycerol (DGDG), the two main galactolipids found in plants, was investigated at the air/water interface and in aqueous dispersion. To approach the composition of the natural photosynthetic membranes, tunable Langmuir model membrane of galactolipids (GL) were used, and were complexified to form either heterogenous binary or ternary assemblies of GL, phospholipids (PL), and phytosterols (pS).The impact of pS, 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) or both on the structural properties of GL membrane was studied. The nature of the interactions between the different molecules was investigated using biophysical characterizations (ellipsometry, tensiometry, atomic force microscopy). In addition, the phase behavior was determined by SAXS analysis on the model assemblies in aqueous dispersions.Results revealed the good interfacial stability of these specific plant membrane lipids. The morphology of the GL film was characteristic of a fluid phase, with an interfacial roughness induced by the intercalation of monogalactosyl and digalactosyl polar heads of MGDG and DGDG, respectively. A phase heterogeneity in the monolayer was induced by the addition of DPPC and/or pS, which resulted in the modification of galactolipid organization and headgroup interactions. These structural changes were confirmed by SAXS analysis, showing more favorable interactions between MGDG and DPPC than between DGDG and DPPC in aqueous dispersion. This phenomenon was exacerbated in the presence of pS.

Photochemically induced dynamic nuclear polarization NMR on photosystem II: donor cofactor observed in entire plant

The solid-state photo-CIDNP (photochemically induced dynamic nuclear polarization) effect allows for increase of signal and sensitivity in magic-angle spinning (MAS) NMR experiments. The effect occurs in photosynthetic reaction centers (RC) proteins upon illumination and induction of cyclic electron transfer. Here we show that the strength of the effect allows for observation of the cofactors forming the spin-correlated radical pair (SCRP) in isolated proteins, in natural photosynthetic membranes as well as in entire plants. To this end, we measured entire selectively 13C isotope enriched duckweed plants (Spirodela oligorrhiza) directly in the MAS rotor. Comparison of 13C photo-CIDNP MAS NMR spectra of photosystem II (PS2) obtained from different levels of RC isolation, from entire plant to isolated RC complex, demonstrates the intactness of the photochemical machinery upon isolation. The SCRP in PS2 is structurally and functionally very similar in duckweed and spinach (Spinacia oleracea). The analysis of the photo-CIDNP MAS NMR spectra reveals a monomeric Chl a donor. There is an experimental evidence for matrix involvement, most likely due to the axial donor histidine, in the formation of the SCRP. Data do not suggest a chemical modification of C-131 carbonyl position of the donor cofactor.

Selective immobilization of bacterial light-harvesting proteins and their photoelectric responses

Abstract

(Invited) Nanophotonic Structures for Solar Light Harvesting and the Generation of Hot Plasmonic Electrons

Future nanophotonic architectures for optical energy conversion and photocatalysis will require nanostructures with roles that work together cooperatively, such as structures with a large absorption cross section combined with features that enable guiding, propagating, and converting energy. Ultrafast optical responses in nanostructures are potentially important for modulating energy flow and also for characterizing and minimizing energy dissipation pathways in nanophotonic structures. Also, ultrafast extraction of hot plasmonic electrons from metal nanostructures is an important opportunity for increasing efficiency of solar energy conversion and photocatalysis. Efforts to greatly improve the efficiency of hot electron generation through plasmonic metamaterials, and characterization of hot electron dissipation pathways are described. I further describe efforts to induced long-range energy propagation in nanostructures. Nanostructured materials inspired by natural photosynthetic membranes represent an opportunity for efficient and directional energy transport. In natural photosystems, light harvesting complexes can transport excitons to the reaction center core with near unity conversion of absorbed photons to separated charge. A key to this process is the high rate of exciton hopping and the directionality of exciton flow due to an energy level waterfall effect of excitons in complexes as the reaction center core is approached. Efforts to induce similar behavior in biomimetically inspired nanostructures are described. Finally efforts to image exciton flow in light harvesting nanoscale materials are introduced. Use of the Center for Nanoscale Materials was supported by the U. S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. DE-AC02-06CH11357.

Hybrid bio-photo-electro-chemical cells for solar water splitting

Photoelectrochemical water splitting uses solar power to decompose water to hydrogen and oxygen. Here we show how the photocatalytic activity of thylakoid membranes leads to overall water splitting in a bio-photo-electro-chemical (BPEC) cell via a simple process. Thylakoids extracted from spinach are introduced into a BPEC cell containing buffer solution with ferricyanide. Upon solar-simulated illumination, water oxidation takes place and electrons are shuttled by the ferri/ferrocyanide redox couple from the thylakoids to a transparent electrode serving as the anode, yielding a photocurrent density of 0.5 mA cm−2. Hydrogen evolution occurs at the cathode at a bias as low as 0.8 V. A tandem cell comprising the BPEC cell and a Si photovoltaic module achieves overall water splitting with solar to hydrogen efficiency of 0.3%. These results demonstrate the promise of combining natural photosynthetic membranes and man-made photovoltaic cells in order to convert solar power into hydrogen fuel.

Alternating current output from a photosynthesis-inspired photoelectrochemical cell

Photosynthesis involves two opposite directions of proton flux across the photosynthetic membrane through embedded proton pumps and proton channels, which provides a biological prototype for designing new photovoltaic systems with alternating current (AC) generation. Here, Pt nanoparticles (Pt NPs) unilaterally covered TiO2 nanoporous membrane, owing to similar characteristics with natural photosynthetic membrane, is employed to construct a photoelectrochemical cell with AC output through the combination with electron donor and acceptor. Ultraviolet light (UV) irradiation induces protons consumption and generation respectively in the two parts of solution across the membrane via asymmetric photochemical reactions. The resulting concentration gradient of HCl powers the generation of a forward photocurrent. Turning UV illumination off causes a reversed transmembrane HCl concentration gradient mainly because hydrogen atoms adsorbed on Pt NPs are oxidized to be protons, which leads to a reversal in the direction of the current. Upon illumination periodically switching on and off, a continuous and steady AC is generated from the photoelectrochemical cell. Moreover, the waveform of AC is adjustable, and a stable square-wave signal can be obtained by optimizing light on/off frequency and proton source concentration in this system.

Redesigning Photosynthetic Membranes: Development of Bio-Inspired Photonic Nanomaterials

Biological cell membranes rely upon hierarchical organization to elicit functional responses. In natural photosynthetic membranes, light harvesting (LH) membrane protein complexes act as a framework for coordination of chromophores which absorb solar energy and channel it to downstream bioenergetic processes. Supported lipid bilayers (SLBs) are established as simple model membranes, into which membrane proteins can be incorporated. As an alternative to lipids, certain diblock copolymers can from membrane-mimetic systems with potential advantages (increased robustness, functionality, responsivity). Here, we present research into two different bio-inspired LH systems.Firstly, a modular, artificial LH system is described, where amphiphilic diblock polymers, poly(ethylene oxide)-block-poly(butadiene), act a matrix for noncovalent arrangement of BODIPY energy donor and bacteriochlorin energy acceptor chromophores. The polymer/ chromophore composites form nanoscale micelles in aqueous solution and defect-free monolayer and bilayer films on solid substrates. Donor-acceptor Forster resonance energy transfer is shown by steady state and time-resolved fluorescence spectroscopy and the system is modelled by theoretical calculations. Supported polymer bilayers demonstrated energy transfer efficiency up to 90%. Secondly, we present ongoing research into the redesign of protein/ lipid LH systems. Purified plant proteins and lipids are used as building blocks to form novel reconstructed protein/SLBs with defined compositions and 3-D organization using a combination of surface patterning and photolithography techniques. Atomic force and fluorescence microscopy and spectroscopy show protein arrangement and light harvesting functionality can be controlled. These new protein/chromophore and polymer/chromophore bio-inspired systems could act as a platforms to investigate membrane self-assembly and organization and could lead to applications in chip-based nanodevices.

Biomimetic Monolayer Films of Monogalactosyldiacylglycerol Incorporating Plastoquinone

Photosynthetic organisms use light to convert the inorganic matter in organic one. Photosynthetic process consists on several steps, and one of them involves plastoquinone (PQ) that acts as electron and proton shuttle between photosystem II and cytochrome. We prepared membranes that mimic the characteristics and composition of natural photosynthetic membranes and we characterized them using several techniques in order to obtain both the PQ molecules disposition in the membrane and their electrochemical behavior. The selected lipid was monogalactosyldiacylglycerol (MGDG) that represents the 50% of the lipid content of the thylakoid membrane. Both MGDG and PQ, and the MGDG:PQ mixtures have been studied using surface pressure-area isotherms and the presence of PQ alters the physical state and compactness of the MGDG matrix. Langmuir-Blodgett (LB) films have been obtained by transferring a monolayer that mimics half of the bilayer of a biological membrane. The AFM topographical characterization of the monolayers on mica indicates the presence of differentiated domains, corresponding to different physical states linked to the influence of the PQ content. Moreover, the electrochemical behavior of the monolayers has been studied when transferred on ITO, observing one main electrochemical process that is due to the diving position of PQ molecules in the lipid matrix.

Correlated AFM-Spectroscopy Imaging of Linear Light Harvesting Protein Aggregates in Bacterial Native Photosynthetic Membrane

How light energy is harvested in a natural photosynthetic membrane through energy transfer is closely related to the stoichiometry and arrangement of light harvesting antenna proteins in the membrane. The specific photosynthetic architecture facilitates a rapid and efficient energy transfer among the light harvesting proteins (LH2 and LH1) and to the reaction center. Here we report the identification of linear aggregates of light harvesting proteins, LH2, in the photosynthetic membranes under ambient conditions by using atomic force microscopy (AFM) imaging and spectroscopic analysis. Our results suggest that the light harvesting proteins, LH2, can exist as linear aggregates of 2 to 8 proteins in the photosynthetic membranes, and the protein distributions are highly heterogeneous. LH2 antenna proteins are responsible for absorbing most of the light energy for photosynthesis, and efficient intra- and inter-molecular energy transfers of LH2 complexes are important for the overall efficiency of the light harvesting mechanism. We combined AFM imaging and spectroscopic analysis with J aggregate theoretical calculations to characterize the linear aggregation of LH2. AFM images reveal the linear aggregation of LH2, where the LH2 complexes are tilted to the plane of the photosynthetic membrane. The spectroscopic results support the attribution of LH2 complexes in the membrane to linear aggregates. The calculated values for the absorption, emission and lifetime using a model developed from J aggregate theory are consistent with the experimentally determined spectroscopic values, further proving a J type aggregation of the LH2 complexes in the photosynthetic membrane.

Revealing Linear Aggregates of Light Harvesting Antenna Proteins in Photosynthetic Membranes

How light energy is harvested in a natural photosynthetic membrane through energy transfer is closely related to the stoichiometry and arrangement of light harvesting antenna proteins in the membrane. The specific photosynthetic architecture facilitates a rapid and efficient energy transfer among the light harvesting proteins (LH2 and LH1) and to the reaction center. Here we report the identification of linear aggregates of light harvesting proteins, LH2, in the photosynthetic membranes under ambient conditions by using atomic force microscopy (AFM) imaging and spectroscopic analysis. Our results suggest that the light harvesting protein, LH2, can exist as linear aggregates of 4 +/- 2 proteins in the photosynthetic membranes and that the protein distributions are highly heterogeneous. In the photosynthetic membranes examined in our measurements, the ratio of the aggregated to the nonaggregated LH2 proteins is about 3:1 to 5:1 depending on the intensity of the illumination used during sample incubation and on the bacterial species. AFM images further identify that the LH2 proteins in the linear aggregates are monotonically tilted at an angle 4 +/- 2 degrees from the plane of the photosynthetic membranes. The aggregates result in red-shifted absorption and emission spectra that are measured using various mutant membranes, including an LH2 knockout, LH1 knockout, and LH2 at different population densities. Measuring the fluorescence lifetimes of purified LH2 and LH2 in membranes, we have observed that the LH2 proteins in membranes exhibit biexponential lifetime decays whereas the purified LH2 proteins gave single exponential lifetime decays. We attribute that the two lifetime components originate from the existence of both aggregated and nonaggregated LH2 proteins in the photosynthetic membranes.

Revealing The Linear Aggregates Of Light Harvesting Antenna Proteins In Photosynthetic Membranes

How light energy is harvested in a natural photosynthetic membrane through energy transfer is closely related to the stoichiometry and arrangement of light harvesting antenna proteins in the membrane. Their specific architecture helps them to absorb photons in the primary process of photosynthesis that is subsequently followed by a rapid and efficient energy transfer among the light harvesting proteins (LH2 and LH1) and to the reaction center. In this work, using atomic force microscopy (AFM) imaging, single membrane fragment FRET spectroscopy, spectral fluctuation analysis, and time-resolved spectroscopic analysis, we show the identification of linear aggregates of light harvesting proteins, LH2, in the photosynthetic membranes under ambient conditions. Our results suggest that the light harvesting proteins, LH2, mostly exist in two states, the aggregated and non-aggregated states in the photosynthetic membranes. Our results shed a light on understanding the complex intramolecular energy transfer dynamics and mechanism of the light harvesting in the photosynthetic membranes.

Simulating photosynthetic quantum conversion

Report reviews attempts to duplicate the process of photosynthesis using a physical system wherein the two quantum acts are separated in space. Included is a brief description of the natural photosynthetic systems with special emphasis on the lamellar or membrane system. The chemistry of artificial photosynthesis is discussed in terms of a photosynthetic electron-transfer system involving a phase boundary, a sensitizer, a sink, another phase boundary, sensitizer, and a source. Criteria for the choice of a sensitizer (dyestuff) and the method of construction of a semiconductor with the appropriate band gap are outlined. The author concludes with a discussion of photoelectron transfer across a phase boundary, and states that this essential feature of the natural photosynthetic membrane must be duplicated in any artificial system. 43 references, 8 figures.