Structure and energy transfer in photosystems of oxygenic photosynthesis.

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Review in Advance first posted online on March 5, 2015. (Changes may still occur before final publication online and in print.)

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Annu. Rev. Biochem. 2015.84. Downloaded from www.annualreviews.org Access provided by Ecole Polytechnique Federal Lausanne on 03/21/15. For personal use only.

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Structure and Energy Transfer in Photosystems of Oxygenic Photosynthesis Nathan Nelson1 and Wolfgang Junge2 1

Department of Biochemistry, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 69978, Israel; email: [email protected]

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Department of Biophysics, Universität Osnabruck, DE-49069 Osnabruck, Germany ¨ ¨

Annu. Rev. Biochem. 2015. 84:26.1–26.25

Keywords

The Annual Review of Biochemistry is online at biochem.annualreviews.org

photosynthesis, light harvesting, electron transfer, membrane complexes, structure, chloroplasts, cyanobacteria

This article’s doi: 10.1146/annurev-biochem-092914-041942 c 2015 by Annual Reviews. Copyright All rights reserved

Abstract Oxygenic photosynthesis is the principal converter of sunlight into chemical energy on Earth. Cyanobacteria and plants provide the oxygen, food, fuel, fibers, and platform chemicals for life on Earth. The conversion of solar energy into chemical energy is catalyzed by two multisubunit membrane protein complexes, photosystem I (PSI) and photosystem II (PSII). Light is absorbed by the pigment cofactors, and excitation energy is transferred among the antennae pigments and converted into chemical energy at very high efficiency. Oxygenic photosynthesis has existed for more than three billion years, during which its molecular machinery was perfected to minimize wasteful reactions. Light excitation transfer and singlet trapping won over fluorescence, radiation-less decay, and triplet formation. Photosynthetic reaction centers operate in organisms ranging from bacteria to higher plants. They are all evolutionarily linked. The crystal structure determination of photosynthetic protein complexes sheds light on the various partial reactions and explains how they are protected against wasteful pathways and why their function is robust. This review discusses the efficiency of photosynthetic solar energy conversion.

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Contents


INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26.2 ADVANCES IN STRUCTURAL BIOLOGY . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26.3 PHOTOSYSTEMS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26.4 A Scenario for the Evolution of Photosynthetic Reaction Centers . . . . . . . . . . . . . . . . . 26.4 Structure and Function of Photosystem I . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26.8 Functional Organization of Light-Harvesting Complex I . . . . . . . . . . . . . . . . . . . . . . . . . 26.9 Light Absorption and Excitation Transfer. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .26.11 Excitation Transfer Among the Light-Harvesting Proteins of Purple Bacteria . . . . .26.11 Excitation Transfer in Light-Harvesting Complex II . . . . . . . . . . . . . . . . . . . . . . . . . . . . .26.12 Excitation Transfer in Reaction Centers of Oxygenic Photosynthesis . . . . . . . . . . . . . .26.13 Excitation Transfer in Photosystem II Complexes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .26.14 Excitation Transfer in Cyanobacterial Photosystem I Complexes . . . . . . . . . . . . . . . . . .26.15 Excitation Transfer in Eukaryotic Photosystem I . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .26.16

INTRODUCTION Oxygenic photosynthesis in cyanobacteria, algae, and plants is accomplished by a series of reactions catalyzed by large membrane protein complexes, soluble factors, and electron donors and acceptors. The reaction velocities of the primary processes span a wide time range. The whole reaction cascade—which covers light absorption by pigment cofactors, excitation energy transfer among antennae, electron transfer (ET) within and between photosystems, proton transfer, ATP synthesis, carbon fixation, and the export of stable products—ranges from femtoseconds (10−15 ) to picoseconds (10−12 ), nanoseconds (10−9 ), microseconds (10−6 ), milliseconds (10−3 ), and seconds. The photochemical reactions operate in the range of femto- to nanoseconds, and the biochemical reactions operate on the microsecond-to-second scale. One of the most important properties of oxygenic photosynthesis is its ability to orchestrate all of those processes while minimizing loss and damage. Photosynthesis spans the widest range of redox potential in the biochemistry of life, as it can produce the most oxidative reaction [water oxidation by photosystem II (PSII); ε0 = +0.8, where ε 0 is the standard redox potential at 25◦ C] and the most powerful reducing compound [ferredox ins by photosystem I (PSI); ε0 = −0.4]. Operation under extreme redox potential presents an enormous challenge, mainly for protection against damage by highly reactive components such as singlet oxygen, which is a by-product of the photochemical activity, as well as loss of high-energy electrons to nonproductive components in the environment. All of these challenges have been addressed in various ways by the long evolution of oxygenic photosynthesis, which is reflected in the fine structure of its components. Determination of the atomic structure of the photosynthetic complexes in several organisms that thrive in different environments shows how each component copes with the specific challenges it faces. The mechanism of each reaction depends on its specific respective time domain. The photophysical and photochemical reactions that occur between femtoseconds and nanoseconds are governed by quantum mechanics. Those that occur between microseconds and seconds are governed by electrostatics and statistical mechanics. Despite nature’s general tendency to avoid wasteful reactions, some leaks and slips are used to control the production rates; quite often they become a necessity and a vehicle for advancing the evolution of elaborate systems (1). 26.2

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This review attempts to capture the excitement generated by the determination of the threedimensional structures of the photosystems that catalyze oxygenic photosynthesis. Several recent reviews contain detailed discussions and list original references to earlier research (2–12). We focus on the photosystems of higher plants, but we also refer to the wealth of structural information that is available on the photosystems of thermophilic cyanobacteria, especially in the case of PSII, for which a plant crystal structure has not yet been obtained. Regarding the function of the photosystems, we focus on excitation energy transfer and trapping; the mechanisms of ET have been described elsewhere. Briefly, ET between fixed cofactors within the photosystems occurs by a nuclear electron tunneling mechanism, as described by Marcus (13) and Marcus & Sutin (14). Over more than 12 orders of magnitude, the rate is exponentially related to the edge-to-edge distance between the cofactors in the respective proteins (15, 16). Detailed structural information is necessary to understand the mechanism of action of photosynthetic systems.

ADVANCES IN STRUCTURAL BIOLOGY Before discussing the photosystems of plants, we begin with a short survey of recent advances of structural biology. Recent developments in electron tomography and single-particle analysis enabled advances in this important research direction. Electron tomography is an extension of transmission electron microscopy, in which a beam of electrons is passed through a sample at incremental degrees of rotation; the information is collected and used to assemble a three-dimensional image of the target. This technique has been successfully adapted to biological materials, but its resolution initially ranged between 50 and 200 A˚ (17). Improvements in electron microscopy (EM) and especially in the detection system advanced the method up to atomic resolution in solid material and close to atomic resolution in biological DNA and protein complexes (18, 19). In these studies, three-dimensional particles identified in biological organelles were fitted with known three-dimensional structures, usually obtained by X-ray crystallography; this process revealed the distribution and organization of the protein complexes. The approach revolutionized our perspective of several aspects of membrane architecture and provided previously unobtainable information. A prime example is the organization of ATP synthase in chloroplast and mitochondrial membrane and its influence on the structure of thylakoids and cristae in their respective organelles (20). Structure determination by electron diffraction of membrane proteins using two-dimensional crystals is a highly promising technique (21, 22). Whereas X-rays travel through a thin twodimensional crystal without diffracting significantly, electrons can be used to form an image (23). Conversely, the strong interaction between electrons and proteins renders this technique useless for thick (1-μm) crystals. Therefore, proteins such as bacteriorhodopsin, which forms ordered two-dimensional arrays in vivo, became the first subjects of high-resolution EM structures. This technique was used to determine the structure of light-harvesting complex II (LHCII) (24). The eventual crystal structures of LHCII and its homolog CP29 by X-ray crystallography yielded superior structural information (25–27). Not only did the resolution increase from 3.4 to 2.5 A˚, but also the quality of the model significantly improved. Recent advances in single-particle cryo-EM and electron tomography promise to provide unprecedented structural information about intact membrane complexes (28–30). Electron tomography studies have revealed the rowlike organization of ATP synthase in mitochondrial membranes (31, 32), supporting the idea (33) that the interaction between these complexes determines the curvature of the membranes (19, 34, 35). Future electron tomography studies are likely to yield valuable information about the fine structure and dynamic of photosynthetic membranes. www.annualreviews.org • Structure and Energy Transfer in Photosystems


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Improvements in cryo-EM and data processing will revolutionize structural biology. Cryo-EM was used to determine the structure of the large subunit of mitochondrial ribosome at near-atomic resolution, demonstrating that this technique can provide information of comparable quality to X-ray crystallography but requires much smaller amounts of more heterogeneous material (36, 37). Cryo-EM is likely to dominate structure determination of large (∼1-MDa) complexes and to gradually replace X-ray crystallography in such studies. However, we must be cautious not to overinterpret these results. The main advantage of X-ray crystallography is that, quite often, all the purified protein in the well ends up in the crystal (38). Consequently, one can solubilize the crystals and verify that the structural information was obtained from an active protein. Moreover, photochemical activity can be analyzed in the crystals of photosynthetic complexes (39). This activity-verification approach is not possible with cryo-EM. The small proportion of the single particles selected for improved resolution poses a greater challenge. In this case, one could solve the structure of a conformation or substate that is irrelevant to the in vivo active complex. This drawback also applies to electron tomography. Improved detection and analysis of electron diffraction may become an important tool for future structure determination at atomic resolution. In a study that subjected small lysozyme crystals to cryo-EM electron diffraction, electron diffraction data were collected at 1.7-A˚ resolution, and the structure was refined to 2.9-A˚ resolution (40). During crystallization of membrane proteins, one often obtains relatively large but thin (∼1-μm) crystals that are useless for X-ray crystallography but potentially amenable to electron diffraction and cryo-EM structure determination. Thus, combinations of all these techniques, including X-ray and electron diffraction, cryo-EM, and electron tomography, are necessary for a deep understanding of structural biology.



PHOTOSYSTEMS A Scenario for the Evolution of Photosynthetic Reaction Centers Biological systems involved in electron transport operate in redox potential boundaries. Oxygenic photosynthesis operates at the most extreme redox potentials of +1.0 to −1.0 V, but the reactions in these extremes last for 1-ps timescale, and the trapping time within the cores of both PSI and PSII is very short (∼3 ps) (136). The respective trapping times with attached antennae, however, are much longer: 60–90 ps in PSI (137) and 300–500 ps in PSII. The longer trapping time in the complete photosystem, compared with that in the core, is due to a small extent to interprotein hopping and to a large extent to dilution of the exciton density in the core by the many pigments surrounding the trap. It is an entropic effect. The dilution is more pronounced in PSII, which is a shallow trap, than in PSI, which is a deep trap. Some authors have argued that trapping in PSII, which is approximately one-fourth as fast as that in PSI, requires that PSII and PSI be separated in grana and stroma lamellae in order for their turnover rates to be balanced under weak illumination (136). Experiments using the anisotropic pump-probe method and other ultrafast kinetic techniques with cyanobacterial PSI revealed excitation transfer as fast as 100 fs, which represents the fastest process of a single energy transfer step between two chlorophylls (see References 7 and 64 and www.annualreviews.org • Structure and Energy Transfer in Photosystems


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references therein). Experiments performed at 77 K, where the absorbance spectrum and fluorescence emission are sharper, revealed a few states of excitation transfer, equilibration, and trapping within the PSI complex. Excitation of the bulk antenna at 670 and 680 nm induced an energy transfer process that populates the chlorophyll a spectral form at 685 to 687 nm within a few transfer steps of 300 to 400 fs. Equilibration with the longest-wavelength-absorbing pigments occurs within 4 to 6 ps, and energy equilibration processes involving low-energy chlorophylls participate in a 30–50-ps process of photochemical trapping for excitation by P700 (86). Time-resolved fluorescence emission measurements, performed at room temperature, revealed differences between the equilibration components of 3.4 to 15 ps and differences between the trapping components of 23 to 50 ps (138, 139). It has been suggested that excitation energy is equilibrated with a lifetime of 0.6 ps among the bulk chlorophylls, is distributed in 3 to 4 ps between the bulk and red chlorophylls, and is trapped in the RC within 19 ps (140). The presence of an additional LHC in eukaryotic PSI, operating without loss in quantum efficiency, demands even more sophisticated studies.



Excitation Transfer in Eukaryotic Photosystem I The eukaryotic PSI complex is much larger and more complicated than its cyanobacterial counterpart. Algae and higher plants contain additional LHCs that increase the absorption cross section of PSI. In higher plants, these LHCs are composed of two heterodimers: Lhca1–Lhca4 and Lhca2– Lhca3, which are organized as a crescent shape around the core (7, 64, 82, 141). Several specific properties distinguish PSI from other photosynthetic complexes: (a) Its high chlorophyll density renders specific time-resolved studies of the ET processes in the RC more difficult, and (b) it has chlorophyll forms with lower energy than the RC chlorophylls, known as red chlorophylls. Despite their low energy, red chlorophylls are supposed to be very important for the overall function of PSI (7, 64). Time-resolved fluorescence measurements have been performed on isolated core and intact PSI particles and stroma membranes from Arabidopsis thaliana to characterize the type of energy-trapping kinetics in higher-plant PSI (142). No bottleneck in the energy flow from the bulk antenna compartments to the RC has been found. Both the core PSI and the full PSI were trap limited. The apparent charge-separation lifetime was ∼6 ps, which is faster than the trap limitation of 50 ps. No red chlorophylls were found in the PSI core complex. Two red chlorophyll compounds located in the peripheral LHCs, with decay lifetimes of 33 and 95 ps, were observed in the intact PSI particles. The two red states have been tentatively attributed to the two light-harvesting complexes Lhca3 and Lhca4. The influence of the red chlorophylls on the slowing of the overall trapping kinetics in the intact PSI complex was estimated to be approximately four times larger than the effect of the bulk antenna enlargement. The fact that those experiments were carried out at ambient temperature reinforces these conclusions. More recent research has investigated the role of the individual antenna complexes in excitation energy transfer and trapping in PSI of higher plants (143, 144). Native PSI and subcomplexes with different antenna composition have been studied by picosecond fluorescence spectroscopy. These studies showed that Lhca3 and Lhca4, which harbor the red chlorophyll forms, have similar emission spectra and that they transfer excitation energy to the core at a rate of ∼25 ns. In contrast, the energy transfer from Lhca1 and Lhca2, the blue antenna complexes, occurs about four times faster. Thus, the energy transfer from the Lhca1– Lhca4 and Lhca2–Lhca3 dimers to the core is faster than energy equilibration within these dimers. Moreover, all four monomers contribute almost equally to the transfer to the core, and the red forms decrease the overall trapping rate by approximately one-half. The excitation energy transfer 26.16

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PsaA


PsaB

Lhca1 Lhca3

Lhca4

Lhca2

Figure 8 Pathways for excitation transfer in plant photosystem I. Coordinates are from Protein Data Bank entry 3LW5. The protein chains and peripheral chlorophylls have been removed; only the porphyrin rings are shown. Core chlorophylls are in magenta, light-harvesting complex I (LHCI) in green, and quinones in blue. The Fx cluster is represented as orange and yellow spheres. The two circled groups of chlorophylls are symmetrically organized in PsaA and PsaB, but their contribution to excitation transfer from LHCI is vastly different. The arrows indicate the two main pathways for excitation transfer; the Lhca1 pathway is likely to be dominant.

routes in PSI have been presented in detail (143, 144). Figure 8 depicts energy transfer and trapping in plant PSI as presented in these studies, superimposed on a model highlighting the chlorophyll positions in the complex. The crystal structure of plant PSI identified three plausible routes for excitation transfer from the LHCI complex to the core complex (52, 79, 82). The most prominent one connects Lhca1 chlorophylls and chlorophylls coordinated by the core PsaB (Figure 8). The second route is between Lhca2 and PsaA, and the third, most elusive one is between Lhca3 and PsaA. Similarly, light-harvesting measurements performed with the PSI–LHCI supercomplex indicated the presence of two or three decay components. The fast one was ∼10 ps, which represented excitation equilibration between the bulk pigments and the redmost forms in the core complex (7, 64). Two slower decay components of 18 to 24 ps and 60 to 100 ps were attributed to direct trapping in the core and trapping following excitation in LHCI, respectively. The average lifetimes are similar to those obtained by modeling of excitation transfer in plant PSI (117). A recent detailed study showed that transfer from the blue Lhcas (Lhca1 and Lhca2) to the core is very fast and occurs in ∼10 ps (144). These two complexes also transfer excitation to the red Lhcas (Lhca3 and Lhca4) at a similar transfer rate. Lhca3 and Lhca4 can also transfer excitation directly to the core, but at a slower rate of ∼40 ps. This study concluded that in PSI the trapping time is ∼50 ps and that most red forms are associated with LHCI. All Lhca chlorophylls transfer www.annualreviews.org • Structure and Energy Transfer in Photosystems


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excitation energy to the core—Lhca1 and Lhca2 very rapidly and Lhca3 and Lhca4 somewhat more slowly (64). Clearly, excitation transfer between the two Lhca dimers is very poor, and most of the excitation transfer from the LHCI proceeds through Lhca1 and Lhca2, which are bluer and have higher energy levels. Apparently, excitation transfer from chlorophylls in the periphery of PSI is occurs via the paradoxical route of blue to red to blue in LHCI, then red to blue to P700 in the core. Red chlorophylls are present in the PSI of cyanobacteria and in the light-harvesting belt of plant PSI. In cyanobacteria, red chlorophylls can affect the trapping kinetics of excitation energy, as shown by measurements performed in PSI from various species (139). All calculations of individual pigment energies are based on the high-resolution PSI structure from Thermosynechococcus elongatus, which contains a relatively large number of red pigments (53). The strength of the red absorption varies significantly between various cyanobacterial species; in particular, Synechocystis has very low levels of red chlorophylls in comparison to Thermosynechococcus (139). On the basis of ring-toring distances and dipole orientation, Jordan et al. (53) identified one chlorophyll trimer (B31– B32–B33) and three dimers (A32–B7, A38–A37, and B37–B38) as candidates for strongly coupled pigments in the RC. We crystallized and solved the structure of Synechocystis PSI and found that the ring location and the local environment of dimer A38–A39 remained virtually unchanged between Synechocystis and Thermosynechococcus (58). The ring positions of the A32–B7 dimer shifted slightly from Thermosynechococcus to Synechocystis, and the side chain coordinating the magnesium of B7 changed from glutamine to histidine. These changes can contribute greatly to the Qy position of the pigment (126). The A32–B7 dimer may be sensitive to the oligomerization state of the complex, given that some red absorption is lost upon monomerization (139). In contrast, it is very clear that chlorophyll b33 is completely missing from the stacked trimer observed in Thermosynechococcus. In plant PSI, the corresponding chlorophyll has shifted substantially, which may cause the loss of red forms in the core complex (79, 82). One of the remaining dimers, either B37–B38 or B31–B32, may be responsible for the residual red absorbance observed in Synechocystis (58). Due to the pseudosymmetry of PsaA and PsaB, cyanobacterial PSI and the core of plant PSI contain another chlorophyll trimer (A20–A21–PL1) that is coordinated by PsaA. These sections of PSI contain high chlorophyll concentrations, and they may represent the so-called red sections of the core complex. The excitation transfer from Lhca1 to P700 must go through the corresponding red section of PsaB (Figure 8). For symmetry reasons, it is likely that the corresponding section in PsaA has a similar role in excitation transfer. However, its position, in proximity to Lhca2 and Lhca3, precludes direct excitation transfer between them. It is highly likely that the PsaA symmetrical bundle of chlorophylls depicted in Figure 8 is functional in state transition and binds LHCII in an almost identical fashion to the binding of Lhca1 by PsaB (58). This scenario suggests that LHCII monomers play an important role in state transition. Symmetrical sections of the PSI core may be directly involved in the final stage of excitation transfer from the antenna of the core to P700. Two critical chlorophyll molecules (X1140 and X1239) that are supposed to transfer the excitation energy directly to the ETC are symmetrically present in these sections. The chlorophyll distribution in this area suggests that it is “blue.” If so, excitation transfer from Lhca4 (red) goes through Lhca1 (blue), through the contact in PsaB (red) to P700, and finally through the connecting chlorophyll assembly (blue) to P700. Such a route is difficult to explain without assuming coherent excitation transfer among adjacent chlorophyll assemblies, regardless of the presence of the red inclination in some of them. The most intriguing properties of plant PSI are that its chlorophyll concentration is ∼0.5 M, its carotenoid concentration is ∼0.15 M, and it is able to avoid concentration quenching to keep the quantum efficiency close to one (52, 64, 68). The explanation for this may be hidden in the protein structure that, at least in the core, was highly conserved over more than 3.5 billion years of evolution



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(42, 47). Apparently, the proteins serve as a scaffold that keeps the pigments in the correct geometry to facilitate fast energy transfer and to prevent excited-state quenching. In addition, the protein must play a role in controlling the energy levels of the pigments. The tight structure of the protein and the fine-tuning of the position of the amino acids and their side chains provide vibrational energy (phonons) for fine-tuning the energy levels of both individual pigments and a group of pigments that form the excitation transfer moiety. Such quantum-mechanical consideration may provide a better explanation for the mechanism of excitation transfer than spectral deconvolution attributed to individual pigments (125, 145). This arrangement allows energy transfer uphill and downhill through the excited-state energy landscape and may allow a fresh look at the phenomenon of red chlorophylls. Three chlorophylls (B31, B32, and B33), identified in the crystal structure of PSI from Thermosynechococcus elongatus, may form the long-wavelength red spectrum (53). This idea gained strong support with the observations that plant PSI B33 has moved significantly (38, 79, 82) and that B33 is lacking in Synechocystis PSI, as is the long “red” pigment (58). Thus, the red form was attributed to B33. The lack of quantum losses at the physiological temperatures was explained by thermal energy that fills the energetic gap between the red donor and the blue acceptor (146). At 77 K, fluorescence loses energy when B33 creates an energy trap. However, B33 is in the periphery of PSI, which limits its function in dissipating excess energy. In contrast, several theoretical and experimental results suggest that the red form plays a major role in excitation transfer to P700 (64). If we assume room-temperature conditions, coherent excitation transfer may provide an alternative and more general explanation for the presence of the red form. According to this view, the red form may arise from an ambient-temperature quantum effect in a group of pigments. The red form arose from the interaction between the pigments and the phonon, which has positive effects on excitation transfer. At low temperatures, the positive thermal energy dissipates, causing increased fluorescence and energy loss. Investigating quantum-mechanical effects on the red forms at various temperatures may provide a wealth of information about excitation transfer in PSI. Experiments on 2DES and transient absorption with PSI crystals may play a key role in the unraveling the mechanism of excitation transfer in large pigment–protein complexes.

DISCLOSURE STATEMENT The authors are not aware of any affiliations, memberships, funding, or financial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS We apologize to all the investigators whose work could not be cited in this review. N.N. thanks the ESRF, SLS, and BESSY II synchrotrons for beam time and the staff scientists for excellent guidance and assistance. The writing of this review was supported by the European Research Council through grant 293579-HOPSEP, the Israel Science Foundation through grant 71/14, and the I-CORE Program of the Planning and Budgeting Committee and the Israel Science Foundation through grant 1775/12.

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www.annualreviews.org • Structure and Energy Transfer in Photosystems


26.25

Energy transfer in photosynthesis.

Divergent pathways of photosynthetic electron transfer: The autonomous oxygenic and anoxygenic photosystems.

Oxygenic photosynthesis without galactolipids.

Vibronic coherence in oxygenic photosynthesis.

Carbon dioxide assimilation in oxygenic and anoxygenic photosynthesis.

Energy transfer in photosynthesis: pigment concentration effects and fluorescent lifetimes.

NDH-1 and NDH-2 Plastoquinone Reductases in Oxygenic Photosynthesis.

Chlorophyll modifications and their spectral extension in oxygenic photosynthesis.

Energy transfer and dynamical structure.

Mechanism of enhanced superoxide production in the cytochrome b(6)f complex of oxygenic photosynthesis.

Photosynthesis. Structural basis for energy transfer pathways in the plant PSI-LHCI supercomplex.

Multi-Omic Dynamics Associate Oxygenic Photosynthesis with Nitrogenase-Mediated H2 Production in Cyanothece sp. ATCC 51142.

Decoding Redox Evolution Before Oxygenic Photosynthesis Based on the Sulfur-Mass Independent Fractionation (S-MIF) Record.

Photosynthesis: Dissipating energy by carotenoids.

Editorial: Assembly of the Photosystem II Membrane-Protein Complex of Oxygenic Photosynthesis.

Reversible effects of moderately elevated temperature on the distribution of excitation energy between the two photosystems of photosynthesis in intact avocado leaves.

Ultrafine Cobalt Catalysts on Covalent Carbon Nitride Frameworks for Oxygenic Photosynthesis.

thioredoxin system. Perspective on its discovery, present status, and future development.

Myosin structure. Proximity measurements by fluorescence energy transfer.

Photo-induced oxidation of the uniquely liganded heme f in the cytochrome b6f complex of oxygenic photosynthesis.

Photoinhibition of photosynthesis: effect of O2 and selective excitation of the photosystems in intact Lemna gibba plants.

Geological evidence of oxygenic photosynthesis and the biotic response to the 2400-2200 ma "great oxidation event".

Energy migration and exciton trapping in green plant photosynthesis.

Oxygenic photosynthesis as a protection mechanism for cyanobacteria against iron-encrustation in environments with high Fe(2+) concentrations.