Substrate–water exchange in photosystem II is arrested before dioxygen formation

Abstract

Light-driven oxidation of water into dioxygen, catalysed by the oxygen-evolving complex (OEC) in photosystem II, is essential for life on Earth and provides the blueprint for devices for producing fuel from sunlight. Although the structure of the OEC is known at atomic level for its dark-stable state, the mechanism by which water is oxidized remains unsettled. Important mechanistic information was gained in the past two decades by mass spectrometric studies of the H218O/H216O substrate–water exchange in the four (semi) stable redox states of the OEC. However, until now such data were not attainable in the transient states formed immediately before the O–O bond formation. Using modified photosystem II complexes displaying up to 40-fold slower O2 production rates, we show here that in the transient state the substrate–water exchange is dramatically slowed as compared with the earlier S states. This further constrains the possible sites for substrate–water binding in photosystem II.

Structural rearrangements preceding dioxygen formation by the water oxidation complex of photosystem II

“…Recent analysis indicates that both fast and slowly exchangeable substrate waters (W f and W s , respectively) are bound to Mn and that W s is either O5 or possibly, W2 (28,35,36,45,51,54). These results have been interpreted to favor a direct radical coupling mechanism.…”

“…Among these, mutations at the hydrophobic D1-V185 located in the proximity of O5, a strong candidate for the slowly exchanging substrate water (W s ) (35,36), proved to have the most dramatic effects on the catalytic properties of the Mn 4 CaO 5 . The bulky phenyalanine substitution (D1-V185F) permitted assembly of Mn clusters that could advance at least to the S + 2 state but were otherwise inactive with respect to O 2 evolution.…”

“…In the case of the D1-V185N mutation, an alteration in the structure of the water cluster is a distinct possibility, because the mutation introduces a strong H-bonding moiety in a place where 36), despite longer lag and slower release phases measured polarographically (24). By analogy, we might expect proton release to be rapid on Y…”

Oxygen-evolving complex of Photosystem II: an analysis of second-shell residues and hydrogen-bonding networks

“…18 O water exchange kinetics in PSII substituted with Sr 2+ / Br À and Sr 2+ /I À in place of Ca 2+ /Cl À have shown that exchange of W f is 1.5 times slower and W s is 9.5 times faster in the S 3 state of PSII [21]. In contrast, in PSII substituted with only Sr 2+ , W f is unaffected while the W s exchange rate increased by a factor of 3-4 [22].…”

The biological water-oxidizing complex at the nano–bio interface

“…The characteristics and position of each metal ion in the Mn 4 CaO 5 cluster have been studied compared with artificial models [16][17][18][19][20][21][22][23][24][25][26][27][28][29][30][31][32] and using various methods [5][6][7][8][9][10][11][33][34][35]. However, the positions of the metal ions, together with the five oxygen atoms bridging the five metal ions, were clearly resolved by the high-resolution crystal structure analysis [10].…”