5.B.4 The Plant Photosystem I Supercomplex (PSI) Family
Oxygenic photosynthesis is the principal producer of both oxygen and organic matter on Earth. Water, the electron donor for this process, is oxidized to O2 and four protons by PSII. The electrons that have been extracted from water are shuttled through a quinone pool and the cytochrome b6f complex to plastocyanin, a small, soluble, copper-containing protein. There are 12 core subunits and 4 different LHCIs (Ben-Shem et al. 2003).Solar energy that has been absorbed by PSI induces the translocation of an electron from plastocyanin at the inner face of the membrane (thylakoid lumen) to ferredoxin on the opposite side (stroma). PSI generates the most negative redox potential in nature (-1 V), and thus largely determines the global amount of enthalpy in living systems (Amunts et al. 2007). The structures of three of the four complexes that catalyse oxygenic photosynthesis in cyanobacteria have been solved at relatively high resolution, and the position of most of their amino acids and prosthetic groups has been defined. Thus, the architecture of oxygenic photosynthesis in cyanobacteria has largely been determined. The structure of the cytochrome b6f complex from chloroplasts of the algae Chlamydomonas reinhardtii has also been solved at high resolution, and has remarkable similarity to the cyanobacterial complex. Two high-resolution structures of light-harvesting complexes of PSII from higher plants have also been published (Cao et al. 2020).
All higher organisms on Earth receive energy directly or indirectly from oxygenic photosynthesis performed by plants, green algae and cyanobacteria. Photosystem I (PSI) is a supercomplex of reaction centre and light-harvesting complexes. It generates the most negative redox potential in nature. The structure of plant PSI has been solved at 3.4 Å resolution, revealing 17 protein subunits. The crystal structure of PSI provides a picture at near atomic detail of 11 out of 12 protein subunits of the reaction centre. At this level, 168 chlorophylls (65 assigned with orientations for Qx and Qy transition dipole moments), 2 phylloquinones, 3 Fe4S4 clusters and 5 carotenoids are described. This structural information extends the understanding of the most efficient nano-photochemical machine in nature. (Amunts et al., 2007).
PSI) is a light-energy converter with diverse light-harvesting antennas associated with its core. In green algae, an extremely large light-harvesting complex I (LHCI) captures and transfers energy to the PSI core. Qin et al. 2019 reported the structure of PSI-LHCI from a green alga Bryopsis corticulans at 3.49 Å resolution, obtained by single-particle cryo-electron microscopy, which revealed 13 core subunits including subunits characteristic of both prokaryotes and eukaryotes, and 10 light-harvesting complex a (Lhca) antennas that form a double semi-ring and an additional Lhca dimer, including a novel 4 TMS Lhca. In total, 244 chlorophylls were identified, some of which were located at key positions for the fast energy transfer.
In vascular plants, bryophytes and algae, the photosynthetic light reaction takes place in the thylakoid membrane where two transmembrane supercomplexes PSII and PSI work together with cytochrome b6f and ATP synthase to harvest the light energy and produce ATP and NADPH (Li et al. 2022). Vascular plant PSI is a 600-kDa protein-pigment supercomplex, the core complex of which is partly surrounded by peripheral light-harvesting complex I (LHCI) that captures sunlight and transfers the excitation energy to the core to be used for charge separation. PSI is unique mainly in the absorption of longer-wavelengths than PSII, fast excitation energy transfer including uphill energy transfer, and an extremely high quantum efficiency. Much effort has been dedicated to structural and functional studies of PSI-LHCI, leading to an understanding of how more than 200 cofactors are kept at the correct distance and geometry to facilitate fast energy transfer (Li et al. 2022).
PSI enables photo-electron transfer and regulates photosynthesis in the bioenergetic membranes of cyanobacteria and chloroplasts. A chloroplast PSI from the green alga Chlamydomonas reinhardtii is organized as a homodimer, comprising 40 protein subunits with 118 transmembrane helices that provide a scaffold for 568 pigments (Naschberger et al. 2022). CryoEM revealed that the absence of PsaH and Lhca2 gives rise to a head-to-head relative orientation of the PSI-light-harvesting complex I monomers, different from the oligomer in cyanobacteria. The light-harvesting protein Lhca9 is the key element for mediating this dimerization. The interface between the monomers is lacking PsaH and thus partially overlaps with the surface area that would bind one of the LHC II complexes in state transitions. A PSI-light-harvesting complex I model at 2.3 Å resolution, including a flexibly bound electron donor plastocyanin with orientations to all the pigments, as well as 621 water molecules that affect energy transfer pathways (Naschberger et al. 2022).