Bicarbonate-induced redox tuning in Photosystem II for regulation and protection

Abstract

The midpoint potential (E m ) of Q A =Q −• A , the one-electron acceptor quinone of Photosystem II (PSII), provides the thermodynamic reference for calibrating PSII bioenergetics. Uncertainty exists in the literature, with two values differing by ∼80 mV. Here, we have resolved this discrepancy by using spectroelectrochemistry on plant PSII-enriched membranes. Removal of bicarbonate (HCO 3 − ) shifts the E m from ∼−145 mV to −70 mV. The higher values reported earlier are attributed to the loss of HCO 3 − during the titrations (pH 6.5, stirred under argon gassing). P hotosystem II (PSII), the water/plastoquinone photooxidoreductase, is at the heart of the major energy cycle that powers the biosphere. Chlorophyll-based photochemistry drives charge separation followed by electron transfer reactions that result in the reduction of quinone on one side of the thylakoid membrane ( Fig. 1) and the oxidation of water on the other. The photochemistry is intrinsically a one-photon/one-electron process, but the quinone reduction and water oxidation are two-and fourelectron processes, respectively. As a result, both processes involve the accumulation of intermediates that are stabilized by the protein and by coupling to protonation reactions (1-3).The electron acceptor side of PSII contains a nonheme ferrous iron (Fe 2+ ) that is flanked by the two quinones, Q A and Q B (Fig. 1) (reviewed in refs. 3 and 4). The Fe 2+ is coordinated by four histidine residues, two from D1 and two from D2, and a bicarbonate ion (HCO 3 − ) that provides a bidentate ligand (3-5). The HCO 3 − is thought to play a role in the Q B protonation pathway (reviewed in refs. 3-5). Recent EPR (6) and computation chemistry studies (7) based on the highest-resolution X-ray crystallographic model (8) implicated HCO 3 − in the second of two protonation steps that are associated with Q B reduction. Measurements of the dissociation constant of HCO 3 − (K d = 40-80 μM), compared with estimates of the HCO 3 − concentration in the stroma (reviewed in ref. 9), led to the assumption that HCO 3 − remains bound under physiological conditions (10). Recently, however, it was reported that the HCO 3 − bound to PSII in Chlamydomonas can be displaced by acetate when present in the culture medium (11).The redox potential of Q A has been the subject of research for decades (12). The current detailed thermodynamic picture of PSII redox chemistry is based on estimates of energy differences between the electron transfer components, but these estimates A , differing by ∼150 mV, depending on the nature of the PSII (12-14). The fully active enzyme showed an E m value that was ∼150 mV lower than that in PSII lacking the Mn 4 CaO 5 cluster. This shift was, in fact, due to the binding (or absence thereof) of the Ca 2+ ion involved in water splitting, but because the Mn cluster provides the Ca binding site, the potential is indirectly determined by the presence of Mn cluster (12)(13)(14). Given the high valence state on the Mn cluster even in the lowest redox state of the water splitti...

Mass spectrometry-based cross-linking study shows that the Psb28 protein binds to cytochrome b 559 in Photosystem II

“…A definitive recent study confirmed the importance of the protective Q A redox switch under conditions when a functional Mn cluster is absent (47), such as occurs in the RC47 complex and other subcomplexes during PSII assembly. Because absence of PsbO destabilizes the Mn cluster, it seems reasonable that a greater proportion of PSII centers would require the protective effect of Psb28, explaining the increased levels of Psb28 in ΔpsbO PSII.…”

Hacking the thylakoid proton motive force for improved photosynthesis: modulating ion flux rates that control proton motive force partitioning into Δ ψ and ΔpH

“…Towards that end, it is hoped that future work (by us and others) will expand the model presented here to test the effects of important processes, including newly discovered ion transport systems and their regulation (69,70), effects on thylakoid osmotic balance (71), the PSII damage/repair cycle (72,73), the accumulation of electrons on the acceptor side of PSI, which can lead to irreversible PSI photodamage (74), alternative modes of PSII regulation including the recent report of bicarbonate mediated protective redox tuning (17), regulation of the ATP synthase, and the need for alternative electron transfer pathways.…”

A Proposal for Formation of Archaean Stromatolites before the Advent of Oxygenic Photosynthesis

“…Photosystem I uses light energy at its primary photochemical reaction center to oxidize a chlorophyll molecule that donates its electron to a series of iron–sulfur proteins (Fromme et al, 2001; Amunts et al, 2007), and then on to coupled assimilatory metabolism such as the Benson-Calvin cycle of CO 2 fixation. In contrast, the oxidized chlorophyll of the photosystem II reaction center passes its electron to a pair of quinone molecules (Nitschke and Rutherford, 1991; Brinkert et al, 2016). The photooxidised chlorophyll of photosystem II is reduced by electrons from water (Umena et al, 2011; Shen, 2015; Ho et al, 2016).…”