A kaleidoscope of photosynthetic antenna proteins and their emerging roles

Photosynthetic light-harvesting antennae are pigment-binding proteins that perform one of the most fundamental tasks on Earth, capturing light and transferring energy that enables life in our biosphere. Adaptation to different light environments led to the evolution of an astonishing diversity of light-harvesting systems. At the same time, several strategies have been developed to optimize the light energy input into photosynthetic membranes in response to fluctuating conditions. The basic feature of these prompt responses is the dynamic nature of antenna complexes, whose function readily adapts to the light available. High-resolution microscopy and spectroscopic studies on membrane dynamics demonstrate the crosstalk between antennae and other thylakoid membrane components. With the increased understanding of light-harvesting mechanisms and their regulation, efforts are focusing on the development of sustainable processes for effective conversion of sunlight into functional bio-products. The major challenge in this approach lies in the application of fundamental discoveries in light-harvesting systems for the improvement of plant or algal photosynthesis. Here, we underline some of the latest fundamental discoveries on the molecular mechanisms and regulation of light harvesting that can potentially be exploited for the optimization of photosynthesis.

The latest fundamental knowledge obtained on the light-harvesting mechanisms of the antenna proteins can be bridged to biotechnical optimization of photosynthesis.     

Structural and functional diversification of the light-harvesting complexes in photosynthetic eukaryotes

Eukaryotes acquired photosynthetic metabolism over a billion years ago, and during that time the light-harvesting antennae have undergone significant structural and functional divergence. The antenna systems are generally used to harvest and transfer excitation energy into the reaction centers to drive photosynthesis, but also have the dual role of energy dissipation. Phycobilisomes formed the first antenna system in oxygenic photoautotrophs, and this soluble protein complex continues to be the dominant antenna in extant cyanobacteria, glaucophytes, and red algae. However, phycobilisomes were lost multiple times during eukaryotic evolution in favor of a thylakoid membrane-integral light-harvesting complex (LHC) antenna system found in the majority of eukaryotic taxa. While photosynthesis spread across different eukaryotic kingdoms via endosymbiosis, the antenna systems underwent extensive modification as photosynthetic groups optimized their light-harvesting capacity and ability to acclimate to changing environmental conditions. This review discusses the different classes of LHCs within photosynthetic eukaryotes and examines LHC diversification in different groups in a structural and functional context.     

Effect of disorder and polarization sequences on two-dimensional spectra of light-harvesting complexes

Photosynthesis Research - Two-dimensional electronic spectra (2DES) provide unique ways to track the energy transfer dynamics in light-harvesting complexes. The interpretation of the peaks and...     

紫细菌光合机构及光合作用基因的表达调控

紫细菌是研究细菌光合作用的重要生物。介绍了紫细菌光合机构捕光色素蛋白复合体Ⅰ(light-harvesting I)、捕光色素蛋白复合体Ⅱ(light-harvesting II)和光化学反应中心(reaction center)的结构, 并探讨了其光合作用基因的转录调控机制, 重点阐述了PpsR/AppA系统对紫细菌光合作用基因的转录调控。     

紫细菌光合机构及光合作用基因的表达调控

紫细菌是研究细菌光合作用的重要生物.介绍了紫细菌光合机构捕光色素蛋白复合体Ⅰ(light-harvestingⅠ)、捕光色素蛋白复合体Ⅱ(1ight-harvesting Ⅱ)和光化学反应中心(reaction center)的结构,并探讨了其光合作用基因的转录调控机制,重点阐述了PpsR/AppA系统对紫细菌光合作用基因的转录调控.     

FRAP analysis of photosynthetic membranes

Fluorescence Recovery after Photobleaching (FRAP) is a technique widely used in cell biology to observe the dynamics of biological systems, including the diffusion of membrane components. More information is needed on the dynamics of photosynthetic membranes in order to help to understand processes such as photosynthetic electron transport, regulation of light-harvesting, and biogenesis and turnover of the photosynthetic apparatus. FRAP has the potential to provide this information, although applying the technique to photosynthetic membranes is not always straightforward. This review explains the potential and the problems, and gives a brief guide to performing FRAP measurements and analysing the data.     

Fluorescence spectroscopy of single photosynthetic light-harvesting supramolecular systems

Recent spectroscopic studies of photosynthetic light-harvesting supramolecular complexes at the single supramolecule level are reviewed. This report describes the “single-molecule” investigation on light-harvesting complex 2 (LH2) of purple photosynthetic bacteria, phycobiliproteins of cyanobacteria and red algae, light-harvesting complex 2 (LHC2) of higher plants, and chlorosomes of green photosynthetic bacteria. Unique behaviors and spectral features of single light-harvesting apparatus have been unraveled that were hidden by the ensemble averaging of many of the complexes. The information obtained with be useful for understanding the electronic structures and energy-transfer mechanism of photosynthetic light-harvesting supramolecular systems.     

Protein dynamics and lipid affinity of monomeric,zeaxanthin-binding LHCII in thylakoid membranes

The xanthophyll cycle in the antenna of photosynthetic organisms under light stress is one of the most well-known processes in photosynthesis, but its role is not well understood. In the xanthophyll cycle, violaxanthin (Vio) is reversibly transformed to zeaxanthin (Zea) that occupies Vio binding sites of light-harvesting antenna proteins. Higher monomer/trimer ratios of the most abundant light-harvesting protein, the light-harvesting complex II (LHCII), usually occur in Zea accumulating membranes and have been observed in plants after prolonged illumination and during high-light acclimation. We present a combined NMR and coarse-grained simulation study on monomeric LHCII from the npq2 mutant that constitutively binds Zea in the Vio binding pocket. LHCII was isolated from ¹³C-enriched npq2 Chlamydomonas reinhardtii (Cr) cells and reconstituted in thylakoid lipid membranes. NMR results reveal selective changes in the fold and dynamics of npq2 LHCII compared with the trimeric, wild-type and show that npq2 LHCII contains multiple mono- or digalactosyl diacylglycerol lipids (MGDG and DGDG) that are strongly protein bound. Coarse-grained simulations on npq2 LHCII embedded in a thylakoid lipid membrane agree with these observations. The simulations show that LHCII monomers have more extensive lipid contacts than LHCII trimers and that protein-lipid contacts are influenced by Zea. We propose that both monomerization and Zea binding could have a functional role in modulating membrane fluidity and influence the aggregation and conformational dynamics of LHCII with a likely impact on photoprotection ability.     

Time-resolved infrared spectroscopy in the study of photosynthetic systems

Time-resolved (TR) infrared (IR) spectroscopy in the nanosecond to second timescale has been extensively used, in the last 30 years, in the study of photosynthetic systems. Interesting results have also been obtained at lower time resolution (minutes or even hours). In this review, we first describe the used techniques—dispersive IR, laser diode IR, rapid-scan Fourier transform (FT)IR, step-scan FTIR—underlying the advantages and disadvantages of each of them. Then, the main TR-IR results obtained so far in the investigation of photosynthetic reactions (in reaction centers, in light-harvesting systems, but also in entire membranes or even in living organisms) are presented. Finally, after the general conclusions, the perspectives in the field of TR-IR applied to photosynthesis are described.     

First solid-state NMR analysis of uniformly ¹³C-enriched major light-harvesting complexes from Chlamydomonas reinhardtii and identification of protein and cofactor spin clusters

The light-harvesting complex II (LHCII) is the main component of the antenna system of plants and green algae and plays a major role in the capture of sun light for photosynthesis. The LHCII complexes have also been proposed to play a key role in the optimization of photosynthetic efficiency through the process of state 1-state 2 transitions and are involved in down-regulation of photosynthesis under excess light by energy dissipation through non-photochemical quenching (NPQ). We present here the first solid-state magic-angle spinning (MAS) NMR data of the major light-harvesting complex (LHCII) of Chlamydomonas reinhardtii, a eukaryotic green alga. We are able to identify nuclear spin clusters of the protein and of its associated chlorophyll pigments in 13C-13C dipolar homonuclear correlation spectra on a uniformly 13C-labeled sample. In particular, we were able to resolve several chlorophyll 131 carbon resonances that are sensitive to hydrogen bonding to the 131-keto carbonyl group. The data show that 13C NMR signals of the pigments and protein sites are well resolved, thus paving the way to study possible structural reorganization processes involved in light-harvesting regulation through MAS solid-state NMR.     

Molecular design of the photosystem II light-harvesting antenna: photosynthesis and photoprotection

The photosystem II (PSII) light-harvesting system carries out two essential functions, the efficient collection of light energy for photosynthesis, and the regulated dissipation of excitation energy in excess of that which can be used. This dual function requires structural and functional flexibility, in which light-harvesting proteins respond to an external signal, the thylakoid DeltapH, to induce feedback control. This process, referred to as non-photochemical quenching (NPQ) depends upon the xanthophyll cycle and the PsbS protein. In nature, NPQ is heterogeneous in terms of kinetics and capacity, and this adapts photosynthetic systems to the specific dynamic features of the light environment. The molecular features of the thylakoid membrane which may enable this flexibility and plasticity are discussed.     

Molecular adaptation of photoprotection: triplet states in light-harvesting proteins

The photosynthetic light-harvesting systems of purple bacteria and plants both utilize specific carotenoids as quenchers of the harmful (bacterio)chlorophyll triplet states via triplet-triplet energy transfer. Here, we explore how the binding of carotenoids to the different types of light-harvesting proteins found in plants and purple bacteria provides adaptation in this vital photoprotective function. We show that the creation of the carotenoid triplet states in the light-harvesting complexes may occur without detectable conformational changes, in contrast to that found for carotenoids in solution. However, in plant light-harvesting complexes, the triplet wavefunction is shared between the carotenoids and their adjacent chlorophylls. This is not observed for the antenna proteins of purple bacteria, where the triplet is virtually fully located on the carotenoid molecule. These results explain the faster triplet-triplet transfer times in plant light-harvesting complexes. We show that this molecular mechanism, which spreads the location of the triplet wavefunction through the pigments of plant light-harvesting complexes, results in the absence of any detectable chlorophyll triplet in these complexes upon excitation, and we propose that it emerged as a photoprotective adaptation during the evolution of oxygenic photosynthesis.     

Spectroscopy of the peridinin-chlorophyll-a protein: insight into light-harvesting strategy of marine algae

An important component of the photosynthetic apparatus is a light-harvesting system that captures light energy and transfers it efficiently to the reaction center. Depending on environmental conditions, photosynthetic antennae have adopted various strategies for this function. Peridinin-chlorophyll-a protein (PCP) represents a unique situation because, unlike other antenna systems which have a preponderance of chlorophyll, it has the carotenoid, peridinin, as its major pigment. The key structural feature of peridinin is a conjugated carbonyl group. Owing to the presence of this group, an intramolecular charge-transfer excited state is formed in peridinin which exhibits different excited state spectra and dynamics depending on the polarity of the environment. The charge-transfer state also facilitates energy transfer between peridinin and chlorophyll-a in PCP. This review summarizes results of spectroscopic investigations of PCP in the past few years, emphasizing the specific light-harvesting strategy developed by marine photosynthetic organisms utilizing carbonyl-containing carotenoids in their antenna complexes.     

Quantum transport in the FMO photosynthetic light-harvesting complex

The very high light-harvesting efficiency of natural photosynthetic systems in conjunction with recent experiments, which showed quantum-coherent energy transfer in photosynthetic complexes, raised questions regarding the presence of non-trivial quantum effects in photosynthesis. Grover quantum search, quantum walks, and entanglement have been investigated as possible effects that lead to this efficiency. Here we explain the near-unit photosynthetic efficiency without invoking non-trivial quantum effects. Instead, we use non-equilibrium Green’s functions, a mesoscopic method used to study transport in nano-conductors to compute the transmission function of the Fenna–Matthews–Olson (FMO) complex using an experimentally derived exciton Hamiltonian. The chlorosome antenna and the reaction center play the role of input and output contacts, connected to the FMO complex. We show that there are two channels for which the transmission is almost unity. Our analysis also revealed a dephasing-driven regulation mechanism that maintains the efficiency in the presence of varying dephasing potentials.     

光合作用对光和CO2响应模型的研究进展

光合作用对光和CO₂响应模型是研究植物生理和植物生态学的重要工具, 可为植物光合特性对主要环境因子的响应提供科学依据。该文综述了当前光合作用对光和CO₂响应模型的研究进展和存在的问题, 并在此基础上探讨了这些模型的可能发展趋势。光合作用涉及光能的吸收、能量转换、电子传递、ATP合成、CO₂固定等一系列复杂的物理和化学反应过程。光合作用由原初反应、同化力形成和碳同化3个基本过程构成, 任一个过程均可对光合作用速率产生直接的影响。光合作用对光响应模型只涉及光能的转换, 而光合作用的生化模型包含了同化力形成和碳同化这两个基本过程。把光合作用的原初反应, 即把参与光能吸收、传递和转换的捕光色素分子的物理参数(如捕光色素分子数、捕光色素分子光能吸收截面、捕光色素分子处于激发态的平均寿命等)结合到生化模型中, 可能是今后光合作用对光响应机理模型的发展方向。     

Elements of a dynamic systems model of canopy photosynthesis

Improving photosynthesis throughout the full canopy rather than photosynthesis of only the top leaves of the canopy is central to improving crop yields. Many canopy photosynthesis models have been developed from physiological and ecological perspectives, however most do not consider heterogeneities of microclimatic factors inside a canopy, canopy dynamics and associated energetics, or competition among different plants, and most models lack a direct linkage to molecular processes. Here we described the rationale, elements, and approaches necessary to build a dynamic systems model of canopy photosynthesis. A systems model should integrate metabolic processes including photosynthesis, respiration, nitrogen metabolism, resource re-mobilization and photosynthate partitioning with canopy level light, CO(2), water vapor distributions and heat exchange processes. In so doing a systems-based canopy photosynthesis model will enable studies of molecular ecology and dramatically improve our insight into engineering crops for improved canopy photosynthetic CO(2) uptake, resource use efficiencies and yields.     

Spectroscopy of individual light-harvesting 2 complexes of Rhodopseudomonas acidophila: diagonal disorder, intercomplex heterogeneity, spectral diffusion, and energy transfer in the B800 band

This paper reports a detailed spectroscopic study of the B800 absorption band of individual light-harvesting 2 (LH2) complexes of the photosynthetic purple bacterium Rhodopseudomonas acidophila at 1. 2 K. By applying single-molecule detection techniques to this system, details and properties can be revealed that remain obscured in conventional ensemble experiments. For instance, from fluorescence-excitation spectra of the individual complexes a more direct measure of the diagonal disorder could be obtained. Further spectral diffusion phenomena and homogeneous linewidths of individual bacteriochlorophyll a (BChl a) molecules are observed, revealing valuable information on excited-state dynamics. This work demonstrates that it is possible to obtain detailed spectral information on individual pigment-protein complexes, providing direct insight into their electronic structure and into the mechanisms underlying the highly efficient energy transfer processes in these systems.     

Means of optimizing conversion of light energy in the primary stages of photosynthesis. I. The need for optimizing the structure of a photosynthetic unit and calculation of its efficiency

It is shown, that the photosynthetic unit structure is to be strongly optimized in vivo to operate with a 90% quantum yield of primary charge separation in reaction centers, which means that a macroscopic photosynthetic unit is neither uniform nor isotropic. Some requirements for optimization of photosynthetic unit structure are determined. The modified probability matrix method to simulate the excitation energy transfer in photosynthesis is proposed. The method is adapted to excitation trapping time (but not to excitation jumps number) calculation. The calculations assume a F?rster inductive resonance mechanism for energy transfer within light-harvesting antenna and pairwise dipolar interactions.     

UNIQUE LOCATION OF THE PHYCOBILIPROTEIN LIGHT-HARVESTING PIGMENT IN THE CRYPTOPHYCEAE1

The cryptophyte algae, or cryptomonads, comprise a small algal group with a unique photosynthetic apparatus. Both a chlorophyll a/c₂ light-harvesting complex and a phycobiliprotein antenna (which can be either phycoerythrin or phycocyanin) are present, with the phycobiliprotein playing the major role in harvesting light for photosynthesis. Longstanding circumstantial evidence suggested that, in cryptophytes, the phycobiliprotein is located in the intrathylakoid space (thylakoid lumen) rather than on the outer surface of the thylakoid as part of a phycobilisome as in other algae. We used immunogold labeling to show conclusively that 1) the phycoerythrin (PE) of the cryptophyte Rhodomonas lens Pascher and Ruttner is located within the intrathylakoid space, 2) the PE is not exclusively bound to the thylakoid membrane but instead is distributed across the thylakoid lumen and 3) a fraction of this PE is tightly associated with the thylakoid membrane. The thylakoids are not everted to compensate for this unusual arrangement. The location of the major light-harvesting pigment on the “wrong” side of the otherwise very normal photo-synthetic membrane is unexpected, unique to the cryptophytes, and, remarkably, does not impair the photosynthetic abilities of this organism. A model is presented which incorporates these results -with previous information to give a complete structural picture of the cryptophyte light-harvesting apparatus.