Structure and function of wild-type and subunit-depleted photosystem I in Synechocystis

Abstract

The ability of photosynthetic organisms to use the sun's light as a sole source of energy sustains life on our planet. Photosystems I (PSI) and II (PSII) are large, multi-subunit, pigment-protein complexes that enable photosynthesis, but this intriguing process remains to be explained fully. Currently, crystal structures of these complexes are available for thermophilic prokaryotic cyanobacteria. The mega-Dalton trimeric PSI complex from thermophilic cyanobacterium, Thermosynechococcus elongatus, was solved at 2.5 Å resolution with X-ray crystallography. That structure revealed the positions of 12 protein subunits (PsaA-F, PsaI-M, and PsaX) and 127 cofactors. Although mesophilic organisms perform most of the world's photosynthesis, no well-resolved trimeric structure of a mesophilic organism exists. Our research model for a mesophilic cyanobacterium was Synechocystis sp. PCC6803. This study aimed to obtain well-resolved crystal structures of [1] a monomeric PSI with all subunits, [2] a trimeric PSI with a reduced number of subunits, and [3] the full, trimeric wild-type PSI complex. We only partially succeeded with the first two structures, but we successfully produced the trimeric PSI structure at 2.5 Å resolution. This structure was comparable to that of the thermophilic species, but we provided more detail. The PSI trimeric supercomplex consisted of 33 protein subunits, 72 carotenoids, 285 chlorophyll a molecules, 51 lipids, 9 iron-sulfur clusters, 6 plastoquinones, 6 putative calcium ions, and over 870 water molecules. This study showed that the structure of the PSI in Synechocystis sp. PCC6803 differed from previously described PSI structures. These findings have broadened our understanding of PSI structure.

Structural basis for the adaptation and function of chlorophyll f in photosystem I

“…35 Supplementary Fig. 4a, b), and the overall structures are similar to that of the cyanobacterial PSI trimer (containing only Chl a) reported previously 6,11 , except for PsaF, PsaJ, and PsaX (and PsaK in the case of white PSI). Although the gene for PsaX was not found in the genome of H. hongdechloris, the genes for PsaF, PsaJ, and PsaK are present 29 .…”

“…These results indicate that the far-red light-induced expression of different copies of the PSI genes psaA, psaB, psaI, and psaL, and differences in the sequences of these genes, especially the psaA gene, caused the structural changes of the PSI complex, especially with respect The cofactors of the white PSI monomer contained 90 Chl a, 16 β-carotene (BCR), 3 [4Fe-4S] cluster, 2 phylloquinones, and three lipid molecules (Supplementary Table 5). The locations of the cofactors are similar to those of the Chl a-containing cyanobacterial PSI 6,11 . However, we identified seven molecules of Chl f (f826A, f827A, f830A, f832A, f844A, f810B, and f825B) in the monomer of the far-red PSI based on the difference density maps calculated between the cryo-EM experimental maps of the white PSI and that of the far-red PSI, as well as between the cryo-EM experimental map of the far-red PSI and the calculated density map derived from the atomic models of the far-red PSI with all Chls assigned as Chl a (see Methods for details) ( Fig.…”

“…In addition to these Chls, a largely red-shifted Chl, Chl f, was first found in a filamentous cyanobacterium Halomicronema hongdechloris 2 , and subsequently in several other species [3][4][5] . The Chl species in the reaction center (RC) of photosystem I (PSI) whose structure has been reported from cyanobacteria to higher plants are all Chl a [6][7][8][9][10][11][12][13][14][15] . However, the location and exact function of Chl f in the photosystems are not clear, although some reports have suggested that one or multiple Chl f molecules may function in the electron transfer chain (ETC) of PSI [16][17][18][19] .…”

Physiological and Evolutionary Implications of Tetrameric Photosystem I in Cyanobacteria

“…1d). Amongst this group 106 of PSI trimer-containing cyanobacteria, T. elongatus and Synechocystis PCC 6803 were 107 included, within which the existence of trimeric PSI has been confirmed via crystallography 108 (Jordan et al, 2001;Malavath et al, 2018). Many of the other cyanobacteria studied were also 109 observed to contain trimeric PSI (Figs 1c, S2, S3; Dataset S1).…”

A novel Ca2+-binding protein influences photosynthetic electron transport inAnabaenasp. PCC 7120

“…Six Ca 2+ ions were detected in the crystal structure of trimeric PSI in the Synechocystis sp. PCC 6803 PSI complex, two of which were localised to PsaL and PsaB subunits, suggesting a role in the oligomerisation of PSI or in providing a binding site for an unidentified regulatory protein [19].…”