Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy

doi:10.1126/science.aay2058

GSTDTAP > 气候变化

DOI	10.1126/science.aay2058
	Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy
	Roberta Croce; Herbert van Amerongen
	2020-08-21
发表期刊	Science
出版年	2020
英文摘要	Conversion of light energy into chemical energy ultimately drives most biochemistry on earth. Photosynthetic organisms use diverse chemical and biological structures to harvest light in different environmental contexts. Croce and van Amerongen synthesized recent structural and spectroscopic work on photosystem complexes from oxygenic photosynthetic organisms. To best capture light, photosystems contain accessory light-harvesting complexes harboring complex networks of pigments that shuttle electronic excitations toward the core complex, which contains the reaction center. The arrangement of pigments and their connectivity, as seen in high-resolution x-ray and cryo–electron microscopy structures, inform our understanding of energy transfer rates derived from spectroscopic measurements and vice versa. The model that emerges is one of many parallel and unconnected pathways for energy transfer into the reaction center from the exterior light-harvesting complexes. Science , this issue p. [eaay2058][1] ### BACKGROUND The harvesting of photons is the first step in photosynthesis, the biological process that transforms solar energy into chemical energy. The photosynthetic membranes of algae and plants are packed with protein complexes binding many chlorophyll and carotenoid pigments, which are combined to form functional units. These units, called the photosystem I and II (PSI and PSII) supercomplexes, are composed of a reaction center (RC) where photochemistry occurs and an antenna comprising hundreds of pigments. Because even direct sunlight is a dilute form of energy, the antenna is crucial to increasing the light-harvesting capacity of the RC. After light is absorbed by a pigment in one of these complexes, excitation energy transfer (EET) to a nearby pigment occurs. EET proceeds until the excitation reaches the RC, where charge separation (CS) takes place. The faster the energy reaches the RC, the higher the photon-to-electron conversion efficiency is because this process needs to beat the natural excited-state decay of the pigments. The trapping in the RCs of PSI and PSII in vivo occurs within 20 to 300 ps, and the maximal quantum efficiency is close to 1.0 for PSI and 0.9 for PSII. How is this high efficiency achieved? ### ADVANCES In recent years, structures of supercomplexes from various algae and plants have been determined at near-atomic resolution using cryo–electron microscopy. These structures revealed the pigment-binding architecture of many subunits and showed the static interactions between subunits in detail for the first time. The biggest surprise was probably the large variability between organisms in the design of the organization of the antenna around a highly conserved core. This is particularly striking for PSI, which can accommodate many antenna subunits associated to the core at positions that can change between organisms. These differences mainly reflect adaptation to specific light conditions. For example, whereas organisms living in water or in a low-light environment have developed a large antenna, plants seem to have a smaller but more modular antenna system to quickly respond to the typical changes in light intensity experienced on land. The processes of EET and CS in some of these supercomplexes and their subcomplexes have been studied with a variety of time-resolved spectroscopic techniques. The excited-state kinetics of these complexes can now be related to the structures to reveal the preferred EET pathways and possible bottlenecks of the process. This leads to, for example, the surprising conclusion that excitations created in the major light-harvesting complex of plants and green algae are not always transferred to the RCs through the minor antenna complexes, but rather, several parallel transfer pathways exist that may facilitate regulatory processes. It is also becoming clear that the antenna of PSI can become substantially larger than that of PSII while maintaining a high quantum efficiency. ### OUTLOOK The high-resolution structures of the supercomplexes of plants and algae represent an excellent starting point for studying energy flow in detail using advanced modeling. Complexes such as plant PSI have been studied in detail by spectroscopy, but little is known about the functional behavior of most of the algal supercomplexes. Spectroscopic measurements on these complexes are now required to relate structure to functionality. All supercomplexes in vivo are embedded in the very crowded environment of the thylakoid membrane, where they can interact with each other, so the next step is to study the complexes in their natural environment. The combination of structural biology, advanced spectroscopy, and modeling will provide a molecular understanding of light harvesting and its regulation in physiologically relevant conditions. These insights will also provide a basis for rational redesign of the photosynthetic apparatus, which could yield increases in crop productivity. ![Figure][2] Timeline of light-harvesting processes. (Top) Many transfer steps between carotenoid and chlorophyll (Chl) a and b molecules occurring on different time scales eventually lead to CS and trapping in the RCs. Transfer between complexes occurs mainly through Chl a and not Chl b . (Bottom) Together, these individual steps determine the average trapping times in the PSI and PSII supercomplexes. Oxygenic photosynthesis is the main process that drives life on earth. It starts with the harvesting of solar photons that, after transformation into electronic excitations, lead to charge separation in the reaction centers of photosystems I and II (PSI and PSII). These photosystems are large, modular pigment-protein complexes that work in series to fuel the formation of carbohydrates, concomitantly producing molecular oxygen. Recent advances in cryo–electron microscopy have enabled the determination of PSI and PSII structures in complex with light-harvesting components called “supercomplexes” from different organisms at near-atomic resolution. Here, we review the structural and spectroscopic aspects of PSI and PSII from plants and algae that directly relate to their light-harvesting properties, with special attention paid to the pathways and efficiency of excitation energy transfer and the regulatory aspects. [1]: /lookup/doi/10.1126/science.aay2058 [2]: pending:yes
领域	气候变化 ; 资源环境
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文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/291209
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Roberta Croce,Herbert van Amerongen. Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy[J]. Science,2020.
APA	Roberta Croce,&Herbert van Amerongen.(2020).Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy.Science.
MLA	Roberta Croce,et al."Light harvesting in oxygenic photosynthesis: Structural biology meets spectroscopy".Science (2020).