Molecular Identification of a High-Spin Deprotonated Intermediate during the S₂ to S₃ Transition of Nature’s Water-Oxidizing Complex

Abstract

The identity of a key intermediate in the S2 to S3 transition of nature’s water-oxidizing complex (WOC) in Photosystem 2 is presented. Broken-symmetry density functional theory (BS-DFT) calculations and Heisenberg–Dirac–van Vleck (HDvV) spin ladder calculations show that an S2 state open cubane model of the WOC containing a μ-hydroxo O4 changes from an S = 5/2 form to an S = 7/2, form upon deprotonation of W1. Combined with X-band electron paramagnetic resonance (EPR) spectral analysis, this indicates that the g = 4.1 EPR signal corresponds to an S = 5/2 form of the WOC with W1 present as a water ligand to Mn4, while the g = 4.8/4.9 form observed at high pH values corresponds to an S = 7/2 form, with W1 as a hydroxo ligand. The latter is also likely to represent the form needed to progress to S3 in the functioning enzyme.

CaMn3IVO4 Cubane Models of the Oxygen‐Evolving Complex: Spin Ground States S<9/2 and the Effect of Oxo Protonation

“…[15,39,44] In ar elated computational study,p rotona-tion of the bridging oxo O(4) (Figure 1) in the S 2 state is proposed to lead to ah igh spin state,w hile maintaining the open-cubane structure. [24] XAS studies performed on the high-spin form of the S 2 state indeed show structural differences to the low-spin form, but extracted Mn-Mn distances do not appear consistent with the closed-cubane structure. [18] Such computational and experimental discrepancies highlight the need for data on model compounds in which mechanistic hypotheses can be tested and the effects of structural changes on the electronic structure of the OEC can be evaluated.…”

“…[34] An alternative interpretation for the spin state interconversion in the S 2 state is based on the observation that this process is pH dependent, with a higher pH favoring the highspin ground state. [24,41] Notably, other effects such as low temperature irradiation of the S 1 state and the introduction of F − favor formation of the high-spin state. [42][43] Insofar as the pH effect, the aquo moiety bound to Mn(4) was hypothesized to be the site that is deprotonated following the observation that no pH dependent behavior is observed when NH 3 is bound to this aquo site.…”

“…[42][43] Insofar as the pH effect, the aquo moiety bound to Mn(4) was hypothesized to be the site that is deprotonated following the observation that no pH dependent behavior is observed when NH 3 is bound to this aquo site. [17,24,41] Structural changes to the OEC through either oxo exchange or (de)protonation would be accompanied by concomitant changes in the nature and magnitude of the magnetic exchange coupling J, which in turn affect not only the S G of the cluster but also other spectroscopic properties such as the sign and magnitude of the projected 55 Mn hyperfine coupling constants. [15,39,44] In a related computational study, protonation of the bridging oxo O(4) (Figure 1) in the S 2 state is proposed to lead to a high spin state, while maintaining the open-cubane structure.…”

“…[9][10][11][12][13][14][15][16][17][18][19] In the absence of unambiguous and direct structural data concerning the OÀOb ond forming S 4 intermediate,s tructural and spectroscopic characterization of lower S n state intermediates influence mechanistic proposals for OÀOb ond formation. [20][21][22][23][24] Connected to Mn oxidation state and structural changes, each of the S n state intermediates adopts au nique electronic structure with ac haracteristic spin ground state S G : [25] S G -(S 0 ) = 1/2, [26] S G (S 1 ) = 0 [27] or higher, [28,29] S G (S 2 ) = 1/2 or 5/ 2, [30][31][32] S G (S 3 ) = 3. [15,[33][34][35] Thei nterconversion between the S G = 1/2 and S G = 5/2 forms of the S 2 state is notable.…”

CaMn3IVO4 Cubane Models of the Oxygen‐Evolving Complex: Spin Ground States S<9/2 and the Effect of Oxo Protonation

“…[34] An alternative interpretation for the spin state interconversion in the S 2 state is based on the observation that this process is pHd ependent, with ah igher pHf avoring the high-spin ground state. [24,41] Notably,o ther effects such as low temperature irradiation of the S 1 state and the introduction of F À favor formation of the high-spin state. [42,43] Insofar as the pHeffect, the aquo moiety bound to Mn(4) was hypothesized to be the site that is deprotonated following the observation that no pHd ependent behavior is observed when NH 3 is bound to this aquo site.…”