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&151;a small, soluble, copper-containing protein. 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. 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.

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). 

Photosystem I (PSI) is a highly efficient natural light-energy converter, and has 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).



This family belongs to the Iron-Sulfur Protein (ISP) Superfamily.

 

References:

Amunts A., O. Drory, N. Nelson. (2007). The structure of a plant photosystem I supercomplex at 3.4 Å resolution. Nature. 447: 58-63

Beck, J., J.N. Lohscheider, S. Albert, U. Andersson, K.W. Mendgen, M.C. Rojas-Stütz, I. Adamska, and D. Funck. (2017). Small One-Helix Proteins Are Essential for Photosynthesis in Arabidopsis. Front Plant Sci 8: 7.

Caspy, I. and N. Nelson. (2018). Structure of the plant photosystem I. Biochem Soc Trans 46: 285-294.

Li, X., G. Yang, X. Yuan, F. Wu, W. Wang, J.R. Shen, T. Kuang, and X. Qin. (2022). Structural elucidation of vascular plant photosystem I and its functional implications. Funct Plant Biol 49: 432-443.

Niroomand, H., D. Mukherjee, and B. Khomami. (2017). Tuning the photoexcitation response of cyanobacterial Photosystem I via reconstitution into Proteoliposomes. Sci Rep 7: 2492.

Qin, X., X. Pi, W. Wang, G. Han, L. Zhu, M. Liu, L. Cheng, J.R. Shen, T. Kuang, and S.F. Sui. (2019). Structure of a green algal photosystem I in complex with a large number of light-harvesting complex I subunits. Nat Plants 5: 263-272.

Xu, C., Q. Zhu, J.H. Chen, L. Shen, X. Yi, Z. Huang, W. Wang, M. Chen, T. Kuang, J.R. Shen, X. Zhang, and G. Han. (2021). A unique photosystem I reaction center from a chlorophyll d-containing cyanobacterium Acaryochloris marina. J Integr Plant Biol 63: 1740-1752.

Examples:

TC#NameOrganismal TypeExample
5.B.4.1.1

The plant photosystem I (PSI) supercomplex at 3.4 Å resolution (Amunts et al., 2007). It contains 4 light harvesting chlorophyll a/b binding proteins as well as 13 additional constituents. One helix (TMS) proteins, OHP1 (O81208) amd OHP2 (Q9FEC1) play an essential role in the assembly or stabilization of photosynthetic pigment-protein complexes, especially photosystem reaction centers, in the thylakoid membrane (Beck et al. 2017). PSI consists of two complexes, a reaction center and light-harvesting complex (LHC), which together form the PSI-LHC supercomplex. The crystal structure of plant PSI has been solved with two distinct crystal forms. The first, crystallized at pH 6.5, exhibited P21 symmetry; the second, crystallized at pH 8.5, exhibited P212121 symmetry. The surfaces involved in binding plastocyanin and ferredoxin were identical in both forms. The crystal structure at 2.6 Å resolution revealed 16 subunits, 45 transmembrane helices, and 232 prosthetic groups, including 143 chlorophyll a, 13 chlorophyll b, 27 beta-carotene, 7 lutein, 2 xanthophyll, 1 zeaxanthin, 20 monogalactosyl diglyceride, 7 phosphatidyl diglyceride, 5 digalactosyl diglyceride, 2 calcium ions, 2 phylloquinone, and 3 iron sulfur clusters (Caspy and Nelson 2018). The model revealed detailed interactions, providing mechanisms for excitation energy transfer and its modulation in one of nature's most efficient photochemical machine. The photoexcitation response of cyanobacterial Photosystem I has been studied following reconstitution in proteoliposomes (Niroomand et al. 2017).

Plants

Photosystem I of Arabidopsis thaliana
(PsaA-L; Lhca 1-4)
PsaA (chlorophyll a apoprotein; 750 aas; 7 TMSs) (P56766)
PsaB (chlorophyll a apoprotein; 734 aas; 11-12 TMSs) (P56767)
PsaC (iron sulfur center protein) (P62090)
PsaD (Reaction Center Subunit II) (Q9SA56)
PsaE (Reaction Center Subunit IV) (Q9S714)
PsaF (Reaction Center Subunit III) (Q9SUI8)
PsaG (Reaction Center Subunit V) (Q9S7N7)
PsaH (Reaction Center Subunit VI) (Q9SUI6)
PsaI (Reaction Center Subunit VIII) (P56768)
PsaJ (Reaction Center Subunit IX) (P56769)
PsaK (Reaction Center Subunit X) (Q9SUI5)
PsaL (Reaction Center Subunit XI) (Q9SUI4)
Lhca1 (225 aas; 1-2 TMSs) (ABD37878)
Lhca2 (257 aas; 1-2 TMSs) (Q9SYW8)
Lhca3 (273 aas; 1-2 TMSs) (Q43381)
Lhca4 (244 aas; 2-4 TMSs) (Q6YWJ7)

 
5.B.4.1.2

Photosystem I reaction center from a chlorophyll d-containing cyanobacterium, Acaryochloris marina (Xu et al. 2021). Photosystem I (PSI) is a large protein supercomplex that catalyzes the light-dependent oxidation of plastocyanin (or cytochrome c6 ) and the reduction of ferredoxin. This catalytic reaction is realized by a transmembrane electron transfer chain consisting of a primary electron donor (a special chlorophyll (Chl) pair) and electron acceptors A0 , A1 , and three Fe4 S4 clusters, FX , FA , and FB. Xu et al. 2021 reported the PSI structure from a Chl d-dominated cyanobacterium Acaryochloris marina at 3.3 Å resolution obtained by single-particle cryo-electron microscopy. The A. marina PSI exists as a trimer with three identical monomers. The structure reveals a unique composition of electron transfer chain proteins in which the primary electron acceptor, A0, is composed of two pheophytins a rather than Chl a found in other well-known PSI structures. A novel subunit Psa27 is observed in the A. marina PSI structure. In addition, 77 Chls, 13 alpha-carotenes, two phylloquinones, three Fe-S clusters, two phosphatidyl glycerols, and one monogalactosyl-diglyceride were identified in each PSI monomer. This provides a structural basis for deciphering the mechanism of photosynthesis in a PSI complex with Chl d as the dominating pigment, absorbing far-red light (Xu et al. 2021).

PSI of Acaryochloris marina

PsaA, 753 aas and 11 TMSs, B0C474
PsaB, 736 aas and 11 TMSs, B0C475
PsaC, 81 aas and probably 0 TMSs, B0CB42
PsaD, 139 aas and 0 TMSs, B0C8F1
PsaE, 89 aas and 0 TMSs, B0C5D5
PsaF, 167 aas and 3 TMSs in a 1 + 2 TMS arrangement, B0C7S7
PsaJ, 51 aas and 1 TMS, B0C7S6
PsaK, 86 aas and 1 TMS, B0CA71
PsaL, 153 aas and 2 C-terminal TMSs
PsaM, 31 aas and 1 TMS