Dimeric and high-resolution structures of Chlamydomonas Photosystem I from a temperature-sensitive Photosystem II mutant

Abstract

Water molecules play a pivotal functional role in photosynthesis, primarily as the substrate for Photosystem II (PSII). However, their importance and contribution to Photosystem I (PSI) activity remains obscure. Using a high-resolution cryogenic electron microscopy (cryo-EM) PSI structure from a Chlamydomonas reinhardtii temperature-sensitive photoautotrophic PSII mutant (TSP4), a conserved network of water molecules - dating back to cyanobacteria - was uncovered, mainly in the vicinity of the electron transport chain (ETC). The high-resolution structure illustrated that the water molecules served as a ligand in every chlorophyll that was missing a fifth magnesium coordination in the PSI core and in the light-harvesting complexes (LHC). The asymmetric distribution of the water molecules near the ETC branches modulated their electrostatic landscape, distinctly in the space between the quinones and FX. The data also disclosed the first observation of eukaryotic PSI oligomerisation through a low-resolution PSI dimer that was comprised of PSI-10LHC and PSI-8LHC.

Algal photosystem I dimer and high resolution model of PSI:plastocyanin complex

“…The membrane architecture in dark- and light-adapted membranes contains ordered rows of closely packed PSI dimers, which are more abundant in the dark state 15 . Similarly, closely associated PSI-LHCI complexes were detected in plants by negative stain electron microscopy 16 , and dimers were found in a subpopulation of PSI from a temperature-sensitive PSII mutant alga 17 . This suggests that reversible PSI dimer formation may have a physiological role in thylakoid membrane structure maintenance in chloroplasts.…”

“…4, Supplementary Table 2). The map can improve the level of detail not only when compared to the previous cryo-EM studies of algal PSI [1][2][3]17 , but also the plant PSI maps obtained by X-ray crystallography 19,20 (Extended Data Fig. 10).…”

“…No density for the His-tag on PsaB could be detected. Overall, taking into account the challenges of modelling photosynthetic complexes 18 , we were able to further improve the quality of the structure, resulting in the significantly better validation statistics, compared to the most recent cryo-EM 17 and X-ray crystallography studies 19, 20 (Supplementary Table 1). Thus, the current study represents the most complete reference model of PSI.…”

“…Updated libraries are used for correct chlorophyll modeling. b , The same region from X-ray study at 2.4 Å resolution 17 lacks the density for waters, whereas the modeled water molecule has no density, and Mg atoms are not in the correct plane.…”

Algal photosystem I dimer and high-resolution model of PSI-plastocyanin complex

“…No density for the His-tag on PsaB could be detected. Overall, taking into account the challenges of modelling photosynthetic complexes 18 , we were able to further improve the quality of the structure, resulting in better validation statistics, compared with the most recent cryo-EM 17 and X-ray crystallography studies 19 , 20 (Extended Data Table 1 ). Thus, the current study represents the most complete reference model of PSI.…”