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.

Highlights

  • Water molecules play a pivotal functional role in photosynthesis, primarily as the substrate for Photosystem II (PSII)

  • The high resolution of TSP4 PSI revealed over 330 water molecules within the complex, many of them conserved across cyanobacteria and eukaryotes

  • linear electron transfer (LEF) and cyclic electron transfer (CEF) occur simultaneously in the thylakoid membrane and are used to regulate the ATP:NAPDH ratio generated during photosynthesis[16]

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Summary

Introduction

Water molecules play a pivotal functional role in photosynthesis, primarily as the substrate for Photosystem II (PSII). The high resolution of TSP4 PSI revealed over 330 water molecules within the complex, many of them conserved across cyanobacteria and eukaryotes. The observed differences in P700 oxidation when DBMIB was added to TSP4 cells adapted to 37 °C compared to 25 °C suggested a change, either in the composition of PSI or its interaction with other proteins, since electrons were still delivered to PSI even though PSII had degraded and plastocyanin was unable to receive electrons from cytochrome b6f.

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