Thermodynamic Limitations of Photosynthetic Water Oxidation at High Proton Concentrations

Abstract

In oxygenic photosynthesis, solar energy drives the oxidation of water catalyzed by a Mn 4 Ca complex bound to the proteins of Photosystem II. Four protons are released during one turnover of the water oxidation cycle (S-state cycle), implying thermodynamic limitations at low pH. For proton concentrations ranging from 1 nM (pH 9) to 1 mM (pH 3), we have characterized the low-pH limitations using a new experimental approach: a specific pH-jump protocol combined with time-resolved measurement of the delayed chlorophyll fluorescence after nanosecond flash excitation. Effective pK values were determined for low-pH inhibition of the light-induced S-state transitions: pK 1 ‫؍‬ 3.3 ؎ 0.3, pK 2 ‫؍‬ 3.5 ؎ 0.2, and pK 3 ≈ pK 4 ‫؍‬ 4.6 ؎ 0.2. Alkaline inhibition was not observed. An extension of the classical Kok model facilitated assignment of these four pK values to specific deprotonation steps in the reaction cycle. Our results provide important support to the extended S-state cycle model and criteria needed for assessment of quantum chemical calculations of the mechanism of water oxidation. They also imply that, in intact organisms, the pH in the lumen compartment can hardly drop below 5, thereby limiting the ⌬pH contribution to the driving force of ATP synthesis.Light-driven water oxidation by plants, algae, and cyanobacteria is a pivotal process in biological solar energy conversion (1). Its evolutionary development, ϳ3.5 billion years ago, has boosted life on Earth by facilitating the efficient use of water as a source of electrons and protons for the synthesis of energystoring carbohydrates and biomass in general. The long-standing scientific interest in photosynthetic water oxidation has recently been invigorated by the vision of future technological systems that, akin to plants and cyanobacteria, use water as a substrate for light-driven formation of energy-rich and storable compounds (H 2 or other fuel materials) (2-5). We believe that insights into energetics and reaction mechanisms of the natural paragon could provide inspiration and guidelines for the development of new technologies (6 -8). However, the biological process is understood only insufficiently (9).In oxygenic photosynthesis, solar energy drives the oxidation of water and the accumulation of "energized" electrons by reduction of quinones (Fig.

Crystal Structure and Functional Characterization of Photosystem II-Associated Carbonic Anhydrase CAH3 in Chlamydomonas reinhardtii

“…Using isolated PSII membranes from C. reinhardtii, Shutova et al (2008) presented data suggesting that CrCAH3 is important for efficient water oxidation by facilitating the removal of protons that are produced when water is oxidized by PSII. This is in line with recent studies (Zaharieva et al, 2011;Klauss et al, 2012) showing that it is crucial to have alternating electron and proton removals from the oxygen-evolving complex (OEC) during the five-state catalytic cycle, i.e. the Kok cycle (Kok et al, 1970), of photosynthetic water oxidation.…”

Alternating electron and proton transfer steps in photosynthetic water oxidation

“…1B), resulting in S 1 þ formation. Mn oxidation in the S 0 n → S 1 þ transition lowers the pK of a Mn ligand, possibly a bridging hydroxide (44,55,56), to a value around 3.3 (57). The proton is removed from the Mn complex and relocated toward the lumen only after S 1 þ formation in the S 1 þ → S 1 n transition.…”

Electron transfer from Cyt b 559 and tyrosine-D to the S2 and S3 states of the water oxidizing complex in photosystem II at cryogenic temperatures

“…The S 1  S 2 transition involves only a one step oxidation of Mn in the WOC while no proton movement occurs (see e.g. [7,10,11,13]). Therefore the S 1 transition occurs smoothly at cryogenic temperatures [40], e.g.…”

“…While the S 0 and S 1 states are quasi-stable and stable, respectively, the S 2 and S 3 states are energetically unstable and decay to S 1 state in the dark. The accumulation of oxidizing equivalents on the WOC is accompanied by proton release/relocation [5,[8][9][10][11][12][13], and references therein] in which process apparently the Y Z  D1-H190 interaction plays a key role. The spatial arrangement of the Mn 4 CaO 5 cluster suggests that Mn4, the manganese located outside the cubane in connection with Y Z via a hydrogen-bond network [2], may provide the catalytic site for water oxidation.…”