Structural basis for the adaptation and function of chlorophyll f in photosystem I (original) (raw)
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Science Advances, 2020
Phototrophic organisms are superbly adapted to different light environments but often must acclimate to challenging competition for visible light wavelengths in their niches. Some cyanobacteria overcome this challenge by expressing paralogous photosynthetic proteins and by synthesizing and incorporating ~8% chlorophyll f into their Photosystem I (PSI) complexes, enabling them to grow under far-red light (FRL). We solved the structure of FRL-acclimated PSI from the cyanobacterium Fischerella thermalis PCC 7521 by single-particle, cryo-electron microscopy to understand its structural and functional differences. Four binding sites occupied by chlorophyll f are proposed. Subtle structural changes enable FRL-adapted PSI to extend light utilization for oxygenic photosynthesis to nearly 800 nm. This structure provides a platform for understanding FRL-driven photosynthesis and illustrates the robustness of adaptive and acclimation mechanisms in nature.
Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium
Proceedings of the National Academy of Sciences, 2007
The composition of photosystem II (PSII) in the chlorophyll (Chl) d -dominated cyanobacterium Acaryochloris marina MBIC 11017 was investigated to enhance the general understanding of the energetics of the PSII reaction center. We first purified photochemically active complexes consisting of a 47-kDa Chl protein (CP47), CP43′ (PcbC), D1, D2, cytochrome b 559 , PsbI, and a small polypeptide. The pigment composition per two pheophytin (Phe) a molecules was 55 ± 7 Chl d , 3.0 ± 0.4 Chl a , 17 ± 3 α-carotene, and 1.4 ± 0.2 plastoquinone-9. The special pair was detected by a reversible absorption change at 713 nm (P713) together with a cation radical band at 842 nm. FTIR difference spectra of the specific bands of a 3-formyl group allowed assignment of the special pair. The combined results indicate that the special pair comprises a Chl d homodimer. The primary electron acceptor was shown by photoaccumulation to be Phe a , and its potential was shifted to a higher value than that in the C...
Structure Determination and Improved Model of Plant Photosystem I * □ S
Photosystem I functions as a sunlight energy converter, cata-lyzing one of the initial steps in driving oxygenic photosynthesis in cyanobacteria, algae, and higher plants. Functionally, Photo-system I captures sunlight and transfers the excitation energy through an intricate and precisely organized antenna system, consisting of a pigment network, to the center of the molecule, where it is used in the transmembrane electron transfer reaction. Our current understanding of the sophisticated mechanisms underlying these processes has profited greatly from elu-cidation of the crystal structures of the Photosystem I complex. In this report, we describe the developments that ultimately led to enhanced structural information of plant Photosystem I. In addition, we report an improved crystallographic model at 3.3-A ˚ resolution, which allows analysis of the structure in more detail. An improved electron density map yielded identification and tracing of subunit PsaK. The location of an additional ten-car-otenes as well as five chlorophylls and several loop regions, which were previously uninterpretable, are now modeled. This represents the most complete plant Photosystem I structure obtained thus far, revealing the locations of and interactions among 17 protein subunits and 193 non-covalently bound pho-tochemical cofactors. Using the new crystal structure, we examine the network of contacts among the protein subunits from the structural perspective, which provide the basis for elucidating the functional organization of the complex. During oxygenic photosynthesis, solar energy is converted into chemical energy for all higher forms of life on Earth. This process is driven by a photosynthetic apparatus within the thy-lakoid membranes of cyanobacteria, algae, and plants. The pho-tochemical functions are performed by two photosystems: Pho-tosystems I (PSI) and II (PSII). 4 These photosystems are multisubunit complexes that consist of protein and non-protein components, and drive light-dependent electron transfer reactions, resulting in the formation of high energy products: ATP and NADPH (1, 2). PSII catalyzes light-driven oxidation of water, providing electrons to PSI via the plastoquinone pool, the cytochrome b 6 f complex, and the water-soluble electron carrier plastocyanin. This electron transfer is coupled to the increase of a transmembrane electrochemical potential gradient (proton motive force), which powers ATP-synthase for phosphorylation of ADP to ATP. PSI catalyzes light-driven electron transport from plastocyanin at the inner face of the membrane (lumen) to ferredoxin on the outside of the membrane (stroma). The reduced ferredoxin is subsequently used for NADPH production, which provides the reducing power for the conversion of carbon dioxide to organic molecules. Although PSII is unique in its ability to extract electrons from water, PSI is arguably the most efficient photoelectric apparatus in nature, exhibiting a quantum efficiency of almost 100% in its utilization of light for electron transport (3). The ability of PS to convert sunlight energy is highly dependent on the precise spatial arrangement of the protein subunits and the relative positions of the cofactors. Therefore, understanding these mechanisms at a molecular level requires detailed knowledge of the three-dimensional arrangement of these complexes. However , PSI and PSII coordinate numerous pigments and comprise at least 19 protein subunits each, most of which transverse the photosynthetic membrane several times, presenting a formidable challenge for structural analysis (4 –9). Our current understanding of the sophisticated mechanism behind PSII sunlight-driven water oxidation and electron transfer is derived mainly from structures determined from cyanobacterial origin (10 –12). In the field of PSI research, the crystal structure of PSI from thermophilic cyanobacterium Thermosynechococcus elongatus provided a breakthrough toward understanding the unprecedented high quantum yield of PSI in light capture and electron transfer (12). The x-ray structure at 2.5-Å resolution revealed a PSI trimer, in which each monomer is composed of 12 protein subunits and 96 chlo-rophylls, and provided detailed insights into the molecular architecture of this complex (14). In PSI from higher plants, our previous crystal structure of the PSI core complex together with its light-harvesting complex (LHCI) at 4.4-Å resolution showed an exquisitely organized monomeric complex of 16 protein subunits and 167 chlorophyll molecules (15), as well as two
Photosynthesis Research, 2019
Certain cyanobacteria can thrive in environments enriched in far-red light (700-800 nm) due to an acclimation process known as far-red light photoacclimation (FaRLiP). During FaRLiP, about 8% of the Chl a molecules in the photosystems are replaced by Chl f and a very small amount of Chl d. We investigated the spectroscopic properties of Photosystem I (PSI) complexes isolated from wild-type (WT) Synechococcus sp. PCC 7335 and a chlF mutant strain (lacking Chl f synthase) grown in white and far-red light (WL-PSI and FRL-PSI, respectively). WT-FRL-PSI complexes contain Chl f and Chl a but not Chl d. The light-minus dark difference spectrum of the trapping center at high spectral resolution indicates that the special pair in WT-FRL-PSI consists of Chl a molecules with maximum bleaching at 703-704 nm. The action spectrum for photobleaching of the special pair showed that Chl f molecules absorbing at wavelengths up to 800 nm efficiently transfer energy to the trapping center in FRL-PSI complexes to produce a charge-separated state. This is ~ 50 nm further into the near IR than WL-PSI; Chl f has a quantum yield equivalent to that of Chl a in the antenna, i.e., ~ 1.0. PSI complexes from Synechococcus 7002 carrying 3.8 Chl f molecules could promote photobleaching of the special pair by energy transfer at wavelengths longer than WT PSI complexes. Results from these latter studies are directly relevant to the issue of whether introduction of Chl f synthase into plants could expand the wavelength range available for oxygenic photosynthesis in crop plants.
Crystal structure of plant photosystem I
Oxygenic photosynthesis is the principal producer of both oxygen and organic matter on Earth. The conversion of sunlight into chemical energy is driven by two multisubunit membrane protein complexes named photosystem I and II. We determined the crystal structure of the complete photosystem I (PSI) from a higher plant (Pisum sativum var. alaska) to 4.4 A ˚ resolution. Its intricate structure shows 12 core subunits, 4 different light-harvesting membrane proteins (LHCI) assembled in a half-moon shape on one side of the core, 45 transmembrane helices, 167 chlorophylls, 3 Fe–S clusters and 2 phylloquinones. About 20 chlorophylls are positioned in strategic locations in the cleft between LHCI and the core. This structure provides a framework for exploration not only of energy and electron transfer but also of the evolutionary forces that shaped the photosynthetic apparatus of terrestrial plants after the divergence of chloroplasts from marine cyanobacteria one billion years ago. Oxygenic photosynthesis, the conversion of sunlight into chemical energy by plants, green algae and cyanobacteria, underpins the survival of virtually all higher life-forms. By producing oxygen and assimilating carbon dioxide into organic matter it determines to a large extent the composition of our atmosphere and provides essential food and fuel. This process is driven by PSI and PSII, two large multisubunit protein complexes that are embedded in the thylakoid membrane and act in series 1,2. Photons absorbed by these complexes induce excitation of a special pair of chlorophylls initiating translocation of an electron across the membrane. This leads to the formation of an electrochemical potential, which powers ATP synthesis 3. Water is the electron donor for this process and is oxidized to O 2 and four H þ ions by PSII. The electrons extracted from water are shuttled through a quinone pool and the b 6 f complex to plastocyanin, a small soluble copper protein 4. Solar energy absorbed by PSI induces translocation of an electron from plastocyanin at the inner face of the membrane (lumen) to ferre-doxin on the opposite side (stroma). The redox potential of ferredoxin is subsequently used in numerous regulatory cycles and reactions, including nitrate assimilation, fatty acid desaturation and NADPH production. In the dark, CO 2 reduction to carbohydrates is fuelled by ATP and NADPH chemical energy 5. Plant PSI is composed of a reaction centre of up to 14 subunits and a membrane-associated antenna complex (LHCI) that captures light and guides its energy to the reaction centre 1. On the whole, plant PSI binds approximately 200 pigments. Despite its complexity , PSI is highly efficient and almost every photon absorbed results in excitation of the special chlorophyll pair P 700 6. LHCI consists of four different membrane proteins (Lhca1–4) with varying stoichio-metry depending on light intensity and other environmental factors 7. As all LHCI proteins share high sequence homology and spectral properties, the need for four different genes is not obvious 8. LHCI proteins are unique among the chlorophyll-a/b binding proteins in their red-shifted absorbance and in the formation of dimers 9. The cyanobacterial PSI is smaller in size compared with plant PSI, having a reaction centre that resembles the one in plants but with no peripheral antenna. Its structure (from Synechococcus elongatus) was recently published, providing detailed insights into the molecular architecture of this complex 10. The model contained 12 protein subunits and 127 cofactors (96 chlorophyll a, 22 carotenoids, 2 phylloquinones, 3 Fe 4 –S 4 clusters and 4 lipids). We sought to understand the interactions within LHCI and between it and the reaction centre, and to reveal how adjustment to a terrestrial habitat shaped the plant complex after divergence from marine cyanobac-teria. To this end, we determined the X-ray crystal structure of PSI from peas and describe here a model at 4.4 A ˚ resolution.
Long-wavelength chlorophylls in photosystem I of cyanobacteria: Origin, localization, and functions
Biochemistry (Moscow), 2014
Photosystem I (PSI) of higher plants, algae, and cyanobacteria is a membrane complex responsible for light energy transformation into chemical energy and for the reduction of ferredoxin on the stromal side and oxidation of plastocyanin (or cytochrome c 6) on the luminal side of thylakoids. The structure of PSI in photosynthesizing organisms is conservative; however, there are differences in subunit composition and spectral characteristics of the antenna [1-3]. The PSI complex in the membrane of cyanobacteria is organized preferentially as a trimer [4-7], whereas the PSI in plants is a monomeric complex encircled by four light-harvesting complexes LHC1 [3, 8, 9]. Due to LHC1, the PSI antenna in plants contains a significantly higher number of chlorophyll molecules per P700 than in PSI in cyanobacteria. As significantly differentiated from higher plants, cyanobacteria do not have light-harvesting complexes LHC1 and LHC2, rather they have chlorophyll localized only in the core-complexes PSI and PSII, as well as a higher content of PSI complexes than PSII in their thylakoids. In higher plants, the PSI/PSII ratio is 1, whereas in the unicellular cyanobacteria it is 3, and in the cyanobacterium Arthrospira (Spirulina) platensis it reaches 5.5 [10]. It is supposed that in cyanobacteria the greater part of P700 is involved in cyclic electron transfer around the PSI.