An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser

Abstract

Photosynthetic water oxidation is catalyzed by the Mn4CaO5 cluster of photosystem II (PSII) with linear progression through five S-state intermediates (S0 to S4). To reveal the mechanism of water oxidation, we analyzed structures of PSII in the S1, S2, and S3 states by x-ray free-electron laser serial crystallography. No insertion of water was found in S2, but flipping of D1 Glu189 upon transition to S3 leads to the opening of a water channel and provides a space for incorporation of an additional oxygen ligand, resulting in an open cubane Mn4CaO6 cluster with an oxyl/oxo bridge. Structural changes of PSII between the different S states reveal cooperative action of substrate water access, proton release, and dioxygen formation in photosynthetic water oxidation.

Capturing structural changes of photosystem II using time-resolved serial femtosecond crystallography with proper flash excitations

“…This gives rise to equivalent values of the temperature factors between the two equivalent atoms in the multiple model, and this population of S 2 and S 1 -states after one-ash illumination is similar to the e ciencies of the S i -state transition estimated by the Fourier transform infrared spectroscophy 7,20 . The OEC structures in the S 1 and S 2 states determined in the present study are similar to those reported in the previous studies 8,9 . The OEC structure in the S 2 state was in the open-cubane form, in which the right side of the O5 is open, giving rise to the ve-coordinate trigonal bipyramidal coordination of Mn1.…”

“…4). However, the changes found in the isomorphous difference Fourier map, such as the shorting of Mn3-Mn4 and elongations of Mn1-Mn3, Mn3-Ca, and Mn4-Ca, were consistent with the previous study with the diffraction data collected at 100 K for the room temperature-trapped S 2 -state 8 (Fig. 4 and Table 2).…”

“…The OEC in the S 1 state is dark-stable, and its structure has been determined to have a chemical composition of Mn 4 CaO 5 5,6 . This structure changes to a Mn 4 CaO 6 -cluster in the highest metastable S 3 state by incorporation of a new oxygen atom (O6 7,8 or Ox 9 ) near the unique µ-oxo bridge O5. The interatomic distance between O6 and O5 is 1.9-2.0 Å in the S 3 state 8,9 , which is suitable for an oxyl/oxo type coupling to form dioxygen between them.…”

“…This structure changes to a Mn 4 CaO 6 -cluster in the highest metastable S 3 state by incorporation of a new oxygen atom (O6 7,8 or Ox 9 ) near the unique µ-oxo bridge O5. The interatomic distance between O6 and O5 is 1.9-2.0 Å in the S 3 state 8,9 , which is suitable for an oxyl/oxo type coupling to form dioxygen between them. The detailed mechanism of the water oxidation, however, has not been well understood, in particular with respect to the origin of O6 and the proton exit pathways.…”

Amphiphilic Oxo-Bridged Ruthenium “Green Dimer” for Water Oxidation

“…In natural photosystem II (PSII), a tetra-manganese-calcium molecular cluster (Mn 4 CaO 5 ) serves as the active center to split water for oxygen evolution with generation of four protons and electrons (2H 2 O / O 2 + 4H + + 4e À ) (Ferreira et al, 2004;Umena et al, 2011;Yano and Yachandra, 2014;Suga et al, 2019). The astonishing activity and stability of the oxygen evolution complex (OEC-PSII) stimulate the scientific community to develop artificial molecular catalysts that are sufficiently rugged and efficient to remove four electrons and four protons for water oxidation (Concepcion et al, 2009;Inoue et al, 2011;Garrido-Barros et al, 2017).…”