Pathway for Mn-cluster oxidation by tyrosine-Z in the S2 state of photosystem II

Abstract

Water oxidation in photosynthetic organisms occurs through the five intermediate steps S0-S4 of the Kok cycle in the oxygen evolving complex of photosystem II (PSII). Along the catalytic cycle, four electrons are subsequently removed from the Mn4CaO5 core by the nearby tyrosine Tyr-Z, which is in turn oxidized by the chlorophyll special pair P680, the photo-induced primary donor in PSII. Recently, two Mn4CaO5 conformations, consistent with the S2 state (namely, S2(A) and S2(B) models) were suggested to exist, perhaps playing a different role within the S2-to-S3 transition. Here we report multiscale ab initio density functional theory plus U simulations revealing that upon such oxidation the relative thermodynamic stability of the two previously proposed geometries is reversed, the S2(B) state becoming the leading conformation. In this latter state a proton coupled electron transfer is spontaneously observed at ∼100 fs at room temperature dynamics. Upon oxidation, the Mn cluster, which is tightly electronically coupled along dynamics to the Tyr-Z tyrosyl group, releases a proton from the nearby W1 water molecule to the close Asp-61 on the femtosecond timescale, thus undergoing a conformational transition increasing the available space for the subsequent coordination of an additional water molecule. The results can help to rationalize previous spectroscopic experiments and confirm, for the first time to our knowledge, that the water-splitting reaction has to proceed through the S2(B) conformation, providing the basis for a structural model of the S3 state.

Keywords: QM/MM; molecular dynamics; photosynthesis; reaction mechanisms.

Fig. 1.

Ab initio QM/MM model of photosystem II. (Right) The QM region, consisting of 224 atoms, is shown in balls and sticks representation. (Upper Left) A selection of the the most important residues and distances involved in the oxidation of the Mn₄CaO₅ cluster by the radical Tyr-Z are sketched. (Lower Left) Representation of the two investigated conformations $S_2^A$ and $S_2^B$.

Fig. 2.

Electronic structure and energetics along the interconversion between the two $S_2$ structural models upon removal of one electron from the system (${\left[S_2\right]}^{+}$ oxidized state). The two upper panels follow changes in the spin population (absolute value) of the Mn ions (left scale) and of the Tyr-Z (right scale) as a function of the reaction coordinate ξ for the two models. In the bottom panel, the calculated free energy profiles (solid lines) show that the HS ground state in ${\left[S_2^B\right]}^{+}$ is thermodynamically favored by 2.6 kcal/mol with respect to the LS ${\left[S_2^A\right]}^{+}$ state. The relative stability in the oxidized system is therefore inverted compared with the reduced ${\left[S_2\right]}^0$ state (dashed lines; data from ref. 37).

Fig. 3.

QM/MM molecular dynamics in the LS ${\left[S_2^A\right]}^{+}$ (Left) and HS ${\left[S_2^B\right]}^{+}$ (Right) state. ${\left[S_2^A\right]}^{+}$ state: In the top panel the spin populations of the four Mn ions (left scale) and the Tyr-Z (violet line, right scale) show that in the simulated time the removed electron remains localized on the Tyr-Z radical. Selected distances (as sketched in Fig. 1) are reported in the middle and bottom panel showing that along dynamics His190 remains protonated, whereas Asp61 is negatively charged. ${\left[S_2^B\right]}^{+}$ state: In the top panel the changes in spin population of the four Mn ions (right scale) and the Tyr-Z (violet line, left scale) are reported as a function of the simulated time. A spontaneous Mn cluster oxidation by the radical Tyr-Z in the ${\left[S_2^B\right]}^{+}$ state occurs through a proton coupled electron transfer mechanism on sub-picosecond timescale (the electron has been transferred from Mn4 to Tyr-Z). Middle and bottom panels report the analysis of selected distances showing the occurrence of a proton transfer from the water molecule W1 to Asp61 and the prevalent neutrality of His190 after the Tyr-Z electron transfer.

Fig. 4.

Spin densities of selected snapshots along the ${\left[S_2^B\right]}^{+}$ dynamics. Representative snapshots were chosen to describe the PCET steps. Blue and red isosurfaces refer to the down and up spin densities, respectively. To improve the visual representation of the spin densities a different density cutoff has been used for the Tyr-Z and the Mn cluster.

Fig. 5.

Sketch of the proposed intermediates in the transition between $S_2$ to $S_3$ states of the Kok cycle.