Supporting Information

Redox-coupled substrate water reorganization in the

active site of Photosystem II - the role of calcium in

substrate water delivery

Ilke Ugura, A. William Rutherfordb, Ville R. I. Kailaa,*

aDepartment Chemie, Technische Universität München, Lichtenbergstraße 4, D-85748 Garching, Germany.bDepartment of Life Sciences, Imperial College, London SW7 2AZ, UK.

S2+

Yz Mn1-Mn2 Mn2-Mn3 Mn3-Mn4 Mn1-Mn3Avg. diff.

EXAFS [1] 2.82 2.73 2.73 3.30 0.000EXAFS [2] 2.69 2.74 >3.0 >3.0 0.178EXAFS [3] 2.70 2.70 2.70 3.20 0.070DFT [4] 2.83 2.80 2.74 3.46 0.063open-LS 2.76 2.80 2.77 3.43 0.075closed-HS 2.73 2.77 3.26 2.91 0.263

S3+

Yz Mn1-Mn2 Mn2-Mn3 Mn3-Mn4 Mn1-Mn3 Avg.

EXAFS[1] 2.73 2.80 3.00 3.30 0.000EXAFS[2] 2.73 2.73 2.77 >3.0 0.150EXAFS[3] 2.70 2.70 3.20/2.8 2.80 0.208DFT [4] 2.84 2.81 2.76 3.55 0.153open-LS 2.80 2.82 2.81 3.60 0.145closed-HS 2.73 2.77 3.26 2.92 0.168

Table S1: Mn-Mn and Mn-Ca distances of two isomers (open and closed) of the S2+

Yz

and S3+ Yz states, in comparison with EXAFS data from refs [1-3]. Avg. diff refers to the

average absolute difference between the central distances in comparison to those reported in Ref. [1]. DFT refers to a B3LYP model of the open high-spin state optimized in Ref. [4].

Figure S1. Optimized molecular structures and B3LYP*-D3 energetics relative to the S3 +Yz

W3:OH- state, as given in Table 2, main text. Only the central catalytic core of the 220 atom models are shown with Ca (in yellow), O (in red), H (in white), N (in blue), C (in gray), Mn(III) (in blue) and Mn(IV) (in green). All the distances are given in Å.

Figure 2. A) Hydrogen-bonded network connecting W3 with Asp-61 in the S2+Yz

• state, and B) optimized molecular structure and B3LYP*-D3 energetics of the state after proton transfer to Asp-61 relative to the S2

+Yz• state. Color scheme as reported in Figure S1.

Figure S3. The changes in hydrogen-bond networks around W3 and Mulliken charges of central atoms following the oxidation of the S2

+Yz state. Mulliken charge of the Ca atom is shown in blue. Only the atoms contributing to this network are shown with Ca (in yellow), O (in red), H (in white), N (in blue), C (in gray), Mn (in green). All the distances are given in Å and only the important distances are shown. The two major changes of hydrogen bonds in two states are shown with green lines.

Figure S4. Approximate transition structure of the O-O bond formation between O5 and W3, located ca. 5 kcal mol-1 above the S4O---O state (Figure 2, main text). Only the atoms contributing to this network are shown. Color scheme as reported in Figure S1.

SI References

[1] J. Yano, Y. Pushkar, P. Glatzel, A. Lewis, K. Sauer, J. Messinger, U. Bergmann, V. Yachandra, High-Resolution Mn EXAFS of the Oxygen-Evolving Complex in Photosystem II:  Structural Implications for the Mn4Ca Cluster, Journal of the American Chemical Society, 127 (2005) 14974-14975.[2] M. Haumann, C. Müller, P. Liebisch, L. Iuzzolino, J. Dittmer, M. Grabolle, T. Neisius, W. Meyer-Klaucke, H. Dau, Structural and Oxidation State Changes of the Photosystem II Manganese Complex in Four Transitions of the Water Oxidation Cycle (S0 → S1, S1 → S2, S2 → S3, and S3,4 → S0) Characterized by X-ray Absorption Spectroscopy at 20 K and Room Temperature†, Biochemistry, 44 (2005) 1894-1908.[3] C. Glöckner, J. Kern, M. Broser, A. Zouni, V. Yachandra, J. Yano, Structural changes of the oxygen-evolving complex in photosystem II during the catalytic cycle, Journal of Biological Chemistry, 288 (2013) 22607-22620.[4] P.E.M. Siegbahn, Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O―O bond formation and O2 release, Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1827 (2013) 1003-1019.