Mechanism of Water Delivery to the Active Site of Photosystem II along the S₂ to S₃ Transition

Abstract

The two water molecules serving as substrate for the oxygen evolution in Photosystem II are already bound in the S2 state of the Kok-Joliot's cycle. Nevertheless, an additional water molecule is supposed to bind the cluster during the transition between the S2 and S3 states, which has been recently revealed to have the Mn4CaO5 catalytic cluster arranged in an open cubane fashion. In this Letter, by means of ab initio calculations, we investigated the possible pathways for the binding of the upcoming water molecule. Upon the four different possibilities checked in our calculations, the binding of the crystallographic water molecule, originally located nearby the Cl(-) binding site, showed the lowest activation energy barrier. Our findings therefore support the view in which the W2 hydroxyl group and the O5 oxygen act as substrates for the oxygen evolution. Within this framework the role of the open and closed Mn4CaO5 conformers is clarified as well as the exact mechanistic events occurring along the S2 to S3 transition.

Interaction of methanol with the oxygen-evolving complex: atomistic models, channel identification, species dependence, and mechanistic implications

“…Substrate analogues are instead found either on Mn4 or at the endpoint of the O4 channel, implying that this channel may be the only one involved in substrate delivery and that Mn4 may be the only site involved in substrate binding. This is consistent with recent studies of the S 2 –S 3 progression, 73,134,142,148 which showed that the first component of the S 3 state is a “closed-cubane” structure with a five-coordinate Mn4( iv ) center. 73 The approximately trigonal bipyramidal geometry of the Mn4( iv ) site of this species results in properties such as absorption in the near-IR and high zero-field splitting, 73 similarly to analogous synthetic Mn( iv ) complexes.…”

“…73 The approximately trigonal bipyramidal geometry of the Mn4( iv ) site of this species results in properties such as absorption in the near-IR and high zero-field splitting, 73 similarly to analogous synthetic Mn( iv ) complexes. 149–151 These studies established that water binding can only occur at this S 3 -state species: water is delivered via the O4 channel to the Mn4 center and binds via a low-barrier transition state, 73,148 allowing access to the other components of the S 3 state. 71 Based on the above, we propose that occupation of the W6 site by methanol may enhance the S 3 population with the five-coordinate Mn( iv ) ion by inhibiting water delivery to the Mn4 site.…”

“…71 Based on the above, we propose that occupation of the W6 site by methanol may enhance the S 3 population with the five-coordinate Mn( iv ) ion by inhibiting water delivery to the Mn4 site. 73,148 …”

“…Water binding to the Mn4 ion 73,148 and internal structural rearrangement 134,152 would be necessary to reach the structural form of the S 3 state attributed to an all-octahedral Mn( iv ) species 71 that has been proposed by Siegbahn to be the active form of the OEC in O–O bond formation, 15,143,153 in an oxo–oxyl coupling scenario. 14,104,154,155 Given that neither methanol nor ammonia are inhibitors and that the kinetics of substrate exchange show both substrates to be already bound in the S 2 state, 156–159 we believe that further evidence is required to conclusively establish whether water binding in the S 3 state 71,160,161 is catalytically required for progression to the S 3 Y Z ˙ state and its subsequent deprotonation and transition to S 4 .…”

Gernot Renger (1937–2013): his life, Max-Volmer Laboratory, and photosynthesis research

“…This was supported further by the very slow reaction of S 3 with reductants like hydrazine or hydroxylamine as compared to that with S 2 state (Messinger et al 1991;Messinger and Renger 1990). At present, it appears that this structural change is relatively minor with regard to Mn-Mn and Mn-Ca distances, but may involve the binding of one water molecule to the Mn 4 CaO 5 cluster (Noguchi 2008;Suzuki et al 2008;Siegbahn 2009)-possibly in a complex sequence of events (Cox and Messinger 2013;Siegbahn 2013;Retegan et al 2016;Capone et al 2016;Ugur et al 2016). We note though that substrate water exchange experiments exclude the water molecule binding to the Mn 4 CaO 5 cluster, during this transition, to act as a Fig.…”