Towards artificial photosynthesis: ruthenium-manganese chemistry mimicking photosystem II reactions

The reaction center Photosystem II is a key component of the most successful solar energy converting machinery on earth: the oxygenic photosynthesis. Photosystem II uses light to drive the reduction of plastoquinone and the oxidation of water. Water-oxidation is catalyzed by a manganese cluster and gives the organism an abundant source of electrons. The principles of photosynthesis have inspired chemists to mimic these reactions in artificial molecular assemblies. Synthetic light-harvesting antennae and light-induced charge separation systems have been demonstrated by several groups. More recently, there has been an increasing effort to mimic Photosystem II by coupling light-driven charge separation to water oxidation, catalyzed by synthetic manganese complexes.     

Structural and mechanistic investigations of photosystem II through computational methods

The advent of oxygenic photosynthesis through water oxidation by photosystem II (PSII) transformed the planet, ultimately allowing the evolution of aerobic respiration and an explosion of ecological diversity. The importance of this enzyme to life on Earth has ironically been paralleled by the elusiveness of a detailed understanding of its precise catalytic mechanism. Computational investigations have in recent years provided more and more insights into the structural and mechanistic details that underlie the workings of PSII. This review will present an overview of some of these studies, focusing on those that have aimed at elucidating the mechanism of water oxidation at the CaMn? cluster in PSII, and those exploring the features of the structure and dynamics of this enzyme that enable it to catalyse this energetically demanding reaction. This article is part of a Special Issue entitled: Photosystem II.     

Light-induced quinone reduction in photosystem II

The photosystem II core complex is the water:plastoquinone oxidoreductase of oxygenic photosynthesis situated in the thylakoid membrane of cyanobacteria, algae and plants. It catalyzes the light-induced transfer of electrons from water to plastoquinone accompanied by the net transport of protons from the cytoplasm (stroma) to the lumen, the production of molecular oxygen and the release of plastoquinol into the membrane phase. In this review, we outline our present knowledge about the "acceptor side" of the photosystem II core complex covering the reaction center with focus on the primary (Q(A)) and secondary (Q(B)) quinones situated around the non-heme iron with bound (bi)carbonate and a comparison with the reaction center of purple bacteria. Related topics addressed are quinone diffusion channels for plastoquinone/plastoquinol exchange, the newly discovered third quinone Q(C), the relevance of lipids, the interactions of quinones with the still enigmatic cytochrome b559 and the role of Q(A) in photoinhibition and photoprotection mechanisms. This article is part of a Special Issue entitled: Photosystem II.     

Molecular organization of oxygen-evolution system in chloroplast

The main function of Photosystem II in chloroplast is to oxidize water molecules to produce oxygen. Strong oxidant produced by photoreaction at Photosystem II reaction center derives electrons from water and the electrons are transferred via Photosystem I to NADP⁺. The components required for water oxidation in Photosystem II were identified and their molecular properties as well as their roles in the oxygen evolution process were elucidated. The entity of the oxygen evolution system is a supramolecular complex of Photosystem II in the thylakoid membrane where reaction center binding polypeptides, three extrinsic polypeptides, managenese atoms, Ca²⁺ and Cl⁻ ions are the essential components, and they constitute a specific catalytic domain for water oxidation. Recipient of the Botanical Society Award for Young Scientists, 1988.     

The structure of photosystem I and evolution of photosynthesis

Oxygenic photosynthesis is the principal producer of both oxygen and organic matter on earth. The primary step in this process--the conversion of sunlight into chemical energy--is driven by four multi-subunit membrane protein complexes named photosystem I, photosystem II, cytochrome b(6)f complex and F-ATPase. Photosystem I generates the most negative redox potential in nature and thus largely determines the global amount of enthalpy in living systems. The recent structural determination of PSI complexes from cyanobacteria and plants sheds light on the evolutionary forces that shaped oxygenic photosynthesis. The fortuitous formation of our solar system in a space plentiful of elements, our distance from the sun and the long time of uninterrupted evolution enabled the perfection of photosynthesis and the evolution of advanced organisms. The available structural information complements the knowledge gained from genomic and proteomic data to illustrate a more precise scenario for the evolution of life systems on earth.     

The evolution of Photosystem II: insights into the past and future

This article attempts to address the molecular origin of Photosystem II (PSII), the central component in oxygenic photosynthesis. It discusses the possible evolution of the relevant cofactors needed for splitting water into molecular O₂ with respect to the following functional domains in PSII: the reaction center (RC), the oxygen evolving complex (OEC), and the manganese stabilizing protein (MSP). Possible ancestral sources of the relevant cofactors are considered, as are scenarios of how these components may have been brought together to produce the intermediate steps in the evolution of PSII. Most importantly, the driving forces that maintained these intermediates for continued adaptation are considered. We then apply our understanding of the evolution of PSII to the bioengineering of a water oxidizing catalyst for utilization of solar energy.     

The evolutionary pathway from anoxygenic to oxygenic photosynthesis examined by comparison of the properties of photosystem II and bacterial reaction centers

In photosynthetic organisms, such as purple bacteria, cyanobacteria, and plants, light is captured and converted into energy to create energy-rich compounds. The primary process of energy conversion involves the transfer of electrons from an excited donor molecule to a series of electron acceptors in pigment–protein complexes. Two of these complexes, the bacterial reaction center and photosystem II, are evolutionarily related and structurally similar. However, only photosystem II is capable of performing the unique reaction of water oxidation. An understanding of the evolutionary process that lead to the development of oxygenic photosynthesis can be found by comparison of these two complexes. In this review, we summarize how insight is being gained by examination of the differences in critical functional properties of these complexes and by experimental efforts to alter pigment–protein interactions of the bacterial reaction center in order to enable it to perform reactions, such as amino acid and metal oxidation, observable in photosystem II.     

The structure and function of CP47 and CP43 in Photosystem II

This Minireview presents a summary of recent investigations examining the structure and functions of the Photosystem II chlorophyll-proteins CP47 and CP43, updating our previous review which appeared in 1990 (TM Bricker, Photosynth Res 24: 1–13). Since this time, numerous studies have clarified the roles of these chlorophyll-proteins within the photosystem. Biochemical, molecular and structural studies (electron and X-ray diffraction) have demonstrated the close association of these components with the photochemical reaction center of the photosystem and with the extrinsic oxygen evolution enhancer proteins. This revised version was published online in June 2006 with corrections to the Cover Date.     

Nano-sized manganese-calcium cluster in photosystem II

Cyanobacteria, algae, and plants are the manufacturers that release O₂ via water oxidation during photosynthesis. Since fossil resources are running out, researchers are now actively trying to use the natural catalytic center of water oxidation found in the photosystem II (PS II) reaction center of oxygenic photosynthetic organisms to synthesize a biomimetic supercatalyst for water oxidation. Success in this area of research will transcend the current bottleneck for the development of energy-conversion schemes based on sunlight. In this review, we go over the structure and function of the water-oxidizing complex (WOC) found in Nature by focusing on the recent advances made by the international research community dedicated to achieve the goal of artificial water splitting based on the WOC of PS II.     

Imidazolium or guanidinium/layered manganese (III, IV) oxide hybrid as a promising structural model for the water-oxidizing complex of Photosystem II for artificial photosynthetic systems

Photosystem II is responsible for the light-driven biological water-splitting system in oxygenic photosynthesis and contains a cluster of one calcium and four manganese ions at its water-oxidizing complex. This cluster may serve as a model for the design of artificial or biomimetic systems capable of splitting water into oxygen and hydrogen. In this study, we consider the ability of manganese oxide monosheets to self-assemble with organic compounds. Layered structures of manganese oxide, including guanidinium and imidazolium groups, were synthesized and characterized by scanning electron microscopy, transmission electron microscopy, X-ray diffraction spectrometry, and atomic absorption spectroscopy. The compounds can be considered as new structural models for the water-oxidizing complex of Photosystem II. The overvoltage of water oxidation for the compounds in these conditions at pH = 6.3 is ~0.6 V. These compounds may represent the first step to synthesize a hybrid of guanidinium or imidazole together with manganese as a biomimetic system for the water-oxidizing complex of Photosystem II.     

Hydrogen peroxide and the evolution of oxygenic photosynthesis

The early atmosphere of the Earth is considered to have been reducing (H₂ rich) or neutral (CO₂-N₂). The present atmosphere by contrast is highly oxidizing (20% O₂). The source of this oxygen is generally agreed to have been oxygenic photosynthesis, whereby organisms use water as the electron donor in the production of organic matter, liberating oxygen into the atmosphere. A major question in the evolution of life is how oxygenic photosynthesis could have evolved under anoxic conditions — and also when this capability evolved. It seems unlikely that water would be employed as the electron donor in anoxic environments that were rich in reducing agents such as ferrous or sulfide ions which could play that role. The abiotic production of atmospheric oxidants could have provided a mechanism by which locally oxidizing conditions were sustained within spatially confined habitats thus removing the available reductants and forcing photosynthetic organisms to utilize water as the electron donor. We suggest that atmospheric H₂O₂ played the key role in inducing oxygenic photosynthesis because as peroxide increased in a local environment, organisms would not only be faced with a loss of reductant, but they would also be pressed to develop the biochemical apparatus (e.g., catalase) that would ultimately be needed to protect against the products of oxygenic photosynthesis. This scenario allows for the early evolution of oxygenic photosynthesis while global conditions were still anaerobic.     

The carboxyl-terminal processing of precursor D1 protein of the photosystem II reaction center

The D1 protein, a key subunit of photosystem II reaction center, is synthesized as a precursor form with a carboxyl-terminal extension, in oxygenic photosynthetic organisms with some exceptions. This part of the protein is removed by the action of an endopeptidase, and the proteolytic processing is indispensable for the manifestation of oxygen-evolving activity in photosynthesis. The carboxyl-terminus of mature D1 protein, which appears upon the cleavage, has recently been demonstrated to be a ligand for a manganese atom in the Mn₄Ca-cluster, which is responsible for the water oxidation chemistry in photosystem II, based on the isotope-edited Fourier transform infrared spectroscopy and the X-ray crystallography. On the other hand, the structure of a peptidase involved in the cleavage of precursor D1 protein has been resolved at a higher resolution, and the enzyme–substrate interactions have extensively been analyzed both in vivo and in vitro. The present article briefly summarizes the history of research and the present state of our knowledge on the carboxyl-terminal processing of precursor D1 protein in the photosystem II reaction center.     

Protein-pigments and the photosystem II reaction center: a glimpse into the history of research and reminiscences

This article provides a glimpse into the dawning of research on chlorophyll-protein complexes and a brief recollection of the path that led us to the identification of the photosystem II reaction center, i.e., the polypeptides that carry the site of primary charge separation in oxygenic photosynthesis. A preliminary version of the personal review on the latter topic has already appeared in this journal (Satoh Photosynth Res 76:233-240, 2003).     

Functional and structural organization of chlorophyll in the developing photosynthetic membranes of Euglena gracilis Z. II. Formation of system II photosynthetic units during greening under optimal light intensity.

The relationships between light-harvesting chlorophyll and reaction centers in Photosystem II were analyzed during the chloroplast development of dark-grown, non-dividing Euglena gracilis Z. Comparative measurements included light saturation of photosynthesis, oxygen evolution under flashing-light and fluorescence induction. The results obtained can be summarized as follows: (1) Photosystem II photocenters are formed in parallel with chlorophyll synthesis, but after a long lag phase. (2) As a consequence, the chlorophyll reaction center ratio (Emerson's type photosynthetic unit) decreases during greening. (3) This decrease is accompanied by considerable changes in the energy transfer and trapping properties of Photosystem II. Most of the initially synthesized chlorophylls are inactive in the transfer of excitations to active photochemical centers and are shared among newly formed Photosystem II photocenters; as a consequence, the number of chlorophylls functionally connected to each Photosystem II photocenter decreases and cooperatively between these centers appears. Results are discussed in terms of chlorophyll organization in developing photosynthetic membranes with reference to the lake or puddle models of photosynthetic unit organization.     

The identification of the Photosystem II reaction center: a personal story

This minireview is about the path that led me to the identification of the Photosystem II reaction center in oxygenic photosynthesis. It is based mostly on my own experiences and viewpoints. Thus, the article is essentially a personal account, and does not include all contributions that led to the identification of this functional unit of Photosystem II. This revised version was published online in August 2006 with corrections to the Cover Date.     

The enigmatic cytochrome b-559 of oxygenic photosynthesis

The ubiquitous and obligatory association of cytochrome b -559 with the photosystem II reaction center of oxygenic photosynthesis is a conundrum since it seems not to have a function in the primary electron transport pathway of oxygen evolution. A model for the cytochrome structure that satisfies the cis -positive rule for membrane protein assembly consists of two short, non-identical hydrophobic membrane-spanning polypeptides (α and β), each containing a single histidine residue, as ligands for the bridging heme prosthetic group that is on the side of the membrane opposite to the water splitting apparatus. The ability of the heterodimer, but not the single α-subunit, to satisfy the cis -positive rule implies that the cytochrome inserts into the membrane as a heterodimer, with some evidence implicating it as the first membrane inserted unit of the assembling reaction center. The very positive redox potential of the cytochrome can be explained by a position for the heme in a hydrophobic niche near the stromal aqueous interface where it is also influenced by the large positive dipole potential of the parallel α-helices of the cytochrome. The requirement for the cytochrome in oxygenic photosynthesis may be a consequence of the presence of the strongly oxidizing reaction center needed for H₂O-splitting. This may lead to the need, under conditions of stress or plastid development, for an alternate source of electrons when the H₂O-splitting system is not operative as a source of reductant for the reaction center.     

Crown group Oxyphotobacteria postdate the rise of oxygen

The rise of oxygen ca. 2.3 billion years ago (Ga) is the most distinct environmental transition in Earth history. This event was enabled by the evolution of oxygenic photosynthesis in the ancestors of Cyanobacteria. However, long‐standing questions concern the evolutionary timing of this metabolism, with conflicting answers spanning more than one billion years. Recently, knowledge of the Cyanobacteria phylum has expanded with the discovery of non‐photosynthetic members, including a closely related sister group termed Melainabacteria, with the known oxygenic phototrophs restricted to a clade recently designated Oxyphotobacteria. By integrating genomic data from the Melainabacteria, cross‐calibrated Bayesian relaxed molecular clock analyses show that crown group Oxyphotobacteria evolved ca. 2.0 billion years ago (Ga), well after the rise of atmospheric dioxygen. We further estimate the divergence between Oxyphotobacteria and Melainabacteria ca. 2.5–2.6 Ga, which—if oxygenic photosynthesis is an evolutionary synapomorphy of the Oxyphotobacteria—marks an upper limit for the origin of oxygenic photosynthesis. Together, these results are consistent with the hypothesis that oxygenic photosynthesis evolved relatively close in time to the rise of oxygen.     

Functional and structural organization of chlorophyll in the developing photosynthetic membranes of Euglena gracilis Z. I. Formation of System II photosynthetic units during greening under optimal light intensity

The relationships between light-harvesting chlorophyll and reaction centers in Photosystem II were analyzed during the chloroplast development of dark-grown, non-dividing Euglena gracilis Z. Comparative measurements included light saturation of photosynthesis, oxygen evolution under flashing-light and fluorescence induction. The results obtained can be summarized as follows: (1) Photosystem II photocenters are formed in parallel with chlorophyll synthesis, but after a longer lag phase. (2) As a consequence, the chlorophyll: reaction center ratio (Emerson's type photosynthetic unit) decreases during greening. (3) This decrease is accompanied by considerable changes in the energy transfer and trapping properties of Photosystem II. Most of the initially synthesized chlorophylls are inactive in the transfer of excitations to active photochemical centers and are shared among newly formed Photosystem II photocenters; as a consequence, the number of chlorophylls functionally connected to each Photosystem II photocenter decreases and cooperativity between these centers appears. Results are discussed in terms of chlorophyll organization in developing photosynthetic membranes with reference to the lake or puddle models of photosynthetic unit organization.