Structure of Chlorella ohadii Photosystem II Reveals Protective Mechanisms against Environmental Stress

Abstract

Green alga Chlorella ohadii is known for its ability to carry out photosynthesis under harsh conditions. Using cryogenic electron microscopy (cryoEM), we obtained a high-resolution structure of PSII at 2.72 Å. This structure revealed 64 subunits, which encompassed 386 chlorophylls, 86 carotenoids, four plastoquinones, and several structural lipids. At the luminal side of PSII, a unique subunit arrangement was observed to protect the oxygen-evolving complex. This arrangement involved PsbO (OEE1), PsbP (OEE2), PsbB, and PsbU (a homolog of plant OEE3). PsbU interacted with PsbO, PsbC, and PsbP, thereby stabilizing the shield of the oxygen-evolving complex. Significant changes were also observed at the stromal electron acceptor side. PsbY, identified as a transmembrane helix, was situated alongside PsbF and PsbE, which enclosed cytochrome b559. Supported by the adjacent C-terminal helix of Psb10, these four transmembrane helices formed a bundle that shielded cytochrome b559 from the surrounding solvent. Moreover, the bulk of Psb10 formed a protective cap, which safeguarded the quinone site and likely contributed to the stacking of PSII complexes. Based on our findings, we propose a protective mechanism that prevents QB (plastoquinone B) from becoming fully reduced. This mechanism offers insights into the regulation of electron transfer within PSII.

Structure of native photosystem II assembly intermediate from Chlamydomonas reinhardtii

“…It’s essential to note that a structurally similar component, the four-helix bundle PsbQ, is present in mature PSII, despite lacking sequence homology and exhibiting an opposite orientation ( Figure 8 , Burton-Smith et al., 2019 ; Fadeeva et al., 2023 ). During maturation, it is plausible that PsbQ substitutes Psb2 and acts as a template for the assembly of the extrinsic proteins PsbO and PsbP, thereby rendering its presence unnecessary in the mature PSII.…”

“…Upon the dimerization of PSII monomers and subsequent attachment of LHCII trimers, the assembly process is finalized (Tokutsu et al, 2012). The ultimate Chlamydomonas PSII structure comprises up to 46 subunits (Sheng et al, 2021), which closely resembles the more comprehensive supercomplex identified in Chlorella ohadii (Fadeeva et al, 2023).…”

Coupling and Slips in Photosynthetic Reactions—From Femtoseconds to Eons

“…Two distinct excitation pathways are operating: the productive pathway (A), which goes from P680 to QA, and the nonproductive pathway (B), which goes from P680 to pheophytin A409 (Figure 2). Remarkably, the two pheophytin molecules are placed at a similar distance to QA (9.7 Å), as is pheophytin A408 to QB (9.3 Å), yet the latter is not active in productive photoreduction [34]. This phenomenon could be attributed to the persistence of coherence in Branch A, while decoherence predominates in Branch B. QB-related slips have been recognized for some time [36].…”

“…On the other hand, PSII must cope with potentially damaging events on the micro-to-millisecond timescale. In this case, extensive mechanistic slips, including internal cyclic electron transport, have evolved, some of which are species-specific [34]. The mechanistic couplings and interactions within PSII are exceptionally intricate, leading to a quantum efficiency of approximately 85% in While PSI operates via single electron events, PSII operates via two-electron reduction and four-electron oxidation steps.…”

Independent Mutation of Two Bridging Carboxylate Ligands Stabilizes Alternate Conformers of the Photosynthetic O2-Evolving Mn4CaO5 Cluster in Photosystem II

“…Each monomer of PSII contains approximately 20 subunits and over 60 cofactors and has a molecular weight of approximately 350 kDa. Structures of cyanobacterial PSII have been determined to resolutions of 1.85–1.95 Å with X-ray crystallography − and cryo-EM. , Structures of eukaryotic PSII from plants, algae, and diatoms have been determined to resolutions of 2.5–5.3 Å with X-ray crystallography and cryo-EM. − Our understanding of photosynthetic water oxidation has increased dramatically in the past decade because of advances in structural, computational, and biophysical methods (for recent reviews, see refs – ).…”