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

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. Caspy et al. report the structure of PSI from a temperature-sensitive photoautotrophic PSII mutant of Chlamydomonas reinhardtii (TSP4), and report the distribution of conserved water molecules in the structure from cyanobacterial to higher plant PSI. They suggest that the asymmetric distribution of water molecules near the electron transfer chain modulates the electron transfer from quinones to FX.