The exchange of the fast substrate water in the S2 state of photosystem II is limited by diffusion of bulk water through channels – implications for the water oxidation mechanism. Issue 38 (6th September 2021)

• Record Type: Journal Article
• Authors: de Lichtenberg, Casper; Kim, Christopher J.; Chernev, Petko; Debus, Richard J.; Messinger, Johannes
• Is Part Of: Chemical science. Volume 12:Issue 38(2021)
• Page Start: 12763
• Page End: 12775
• Publication Date: 2021-09-06
• Subjects: Chemistry -- Periodicals; 540.5
• DOI: 10.1039/d1sc02265b
• Languages: English
• ISSNs: 2041-6520

Abstract

Abstract : Access to the oxygen-evolving complex in photosynthesis is restricted by specific barriers in the channels connecting the Mn4 CaO5 catalyst with bulk water. Together with other recent data, this finding allows assigning the two substrate waters. Abstract : The molecular oxygen we breathe is produced from water-derived oxygen species bound to the Mn4 CaO5 cluster in photosystem II (PSII). Present research points to the central oxo-bridge O5 as the 'slow exchanging substrate water (Ws )', while, in the S2 state, the terminal water ligands W2 and W3 are both discussed as the 'fast exchanging substrate water (Wf )'. A critical point for the assignment of Wf is whether or not its exchange with bulk water is limited by barriers in the channels leading to the Mn4 CaO5 cluster. In this study, we measured the rates of H2 16 O/H2 18 O substrate water exchange in the S2 and S3 states of PSII core complexes from wild-type (WT) Synechocystis sp. PCC 6803, and from two mutants, D1-D61A and D1-E189Q, that are expected to alter water access via the Cl1/O4 channels and the O1 channel, respectively. We found that the exchange rates of Wf and Ws were unaffected by the E189Q mutation (O1 channel), but strongly perturbed by the D61A mutation (Cl1/O4 channel). It is concluded that all channels have restrictions limiting the isotopic equilibration of the inner water pool near the Mn4 CaO5 cluster, and that D61 participates in one such barrier. In the D61A mutant this barrier is lowered so that Wf exchange occurs more rapidly. This finding removes the main argument against Ca-bound W3 as fast substrate water in the S2 state, namely the indifference of the rate of Wf exchange towards Ca/Sr substitution.