Structural basis for an early stage of the photosystem II repair cycle in Chlamydomonas reinhardtii.

Photosystem II (PSII) catalyzes water oxidation and plastoquinone reduction by utilizing light energy. It is highly susceptible to photodamage under high-light conditions and the damaged PSII needs to be restored through a process known as the PSII repair cycle. The detailed molecular mechanism underlying the PSII repair process remains mostly elusive. Here, we report biochemical and structural features of a PSII-repair intermediate complex, likely arrested at an early stage of the PSII repair process in the green alga Chlamydomonas reinhardtii. The complex contains three protein factors associated with a damaged PSII core, namely Thylakoid Enriched Factor 14 (TEF14), Photosystem II Repair Factor 1 (PRF1), and Photosystem II Repair Factor 2 (PRF2). TEF14, PRF1 and PRF2 may facilitate the release of the manganese-stabilizing protein PsbO, disassembly of peripheral light-harvesting complexes from PSII and blockage of the QB site, respectively. Moreover, an α-tocopherol quinone molecule is located adjacent to the heme group of cytochrome b559, potentially fulfilling a photoprotective role by preventing the generation of reactive oxygen species.

Ultrafast energy quenching mechanism of LHCSR3-dependent photoprotection in Chlamydomonas.

Photosynthetic organisms have evolved an essential energy-dependent quenching (qE) mechanism to avoid any lethal damages caused by high light. While the triggering mechanism of qE has been well addressed, candidates for quenchers are often debated. This lack of understanding is because of the tremendous difficulty in measuring intact cells using transient absorption techniques. Here, we have conducted femtosecond pump-probe measurements to characterize this photophysical reaction using micro-sized cell fractions of the green alga Chlamydomonas reinhardtii that retain physiological qE function. Combined with kinetic modeling, we have demonstrated the presence of an ultrafast excitation energy transfer (EET) pathway from Chlorophyll a (Chl a) Qy to a carotenoid (car) S1 state, therefore proposing that this carotenoid, likely lutein1, is the quencher. This work has provided an easy-to-prepare qE active thylakoid membrane system for advanced spectroscopic studies and demonstrated that the energy dissipation pathway of qE is evolutionarily conserved from green algae to land plants.

Weak acids produced during anaerobic respiration suppress both photosynthesis and aerobic respiration.

While photosynthesis transforms sunlight energy into sugar, aerobic and anaerobic respiration (fermentation) catabolizes sugars to fuel cellular activities. These processes take place within one cell across several compartments, however it remains largely unexplored how they interact with one another. Here we report that the weak acids produced during fermentation down-regulate both photosynthesis and aerobic respiration. This effect is mechanistically explained with an "ion trapping" model, in which the lipid bilayer selectively traps protons that effectively acidify subcellular compartments with smaller buffer capacities - such as the thylakoid lumen. Physiologically, we propose that under certain conditions, e.g., dim light at dawn, tuning down the photosynthetic light reaction could mitigate the pressure on its electron transport chains, while suppression of respiration could accelerate the net oxygen evolution, thus speeding up the recovery from hypoxia. Since we show that this effect is conserved across photosynthetic phyla, these results indicate that fermentation metabolites exert widespread feedback control over photosynthesis and aerobic respiration. This likely allows algae to better cope with changing environmental conditions.