Resolving the Differences Between the 1.9 Å and 1.95 Å Crystal Structures of Photosystem II: A Single Proton Relocation Defines Two Tautomeric Forms of the Water-Oxidizing Complex.
Great progress has been made in characterizing the water-oxidizing complex (WOC) in photosystem II (PSII) with the publication of a 1.9 Å resolution X-ray diffraction (XRD) and recently a 1.95 Å X-ray free-electron laser (XFEL) structure. However, these achievements are under threat because of perceived conflicts with other experimental data. For the earlier 1.9 Å structure, lack of agreement with extended X-ray absorption fine structure (EXAFS) data led to the notion that the WOC suffered from X-ray photoreduction. In the recent 1.95 Å structure, Mn photoreduction is not an issue, but poor agreement with computational models which adopt the 'high' oxidation state paradigm, has again resulted in criticism of the structure on the basis of contamination with lower S states of the WOC. Here we use DFT modeling to show that the distinct WOC geometries in the 1.9 and 1.95 Å structures can be straightforwardly accounted for when the Mn oxidation states are consistent with the 'low' oxidation state paradigm. Remarkably, our calculations show that the two structures are tautomers, related by a single proton relocation.
Research School of Chemistry, Australian National University, Canberra ACT 0200 (Australia).
Simon
S
Petrie
Research School of Chemistry, Australian National University, Canberra ACT 0200 (Australia). ron.pace@anu.edu.au.
Ron J
RJ
Pace
Research School of Chemistry, Australian National University, Canberra ACT 0200 (Australia). rob.stranger@anu.edu.au.
Rob
R
Stranger
D018360:Crystallography, X-Ray; D008345:Manganese / Q000737:chemistry; D008958:Models, Molecular; D010084:Oxidation-Reduction; D010100:Oxygen / Q000737:chemistry; D045332:Photosystem II Protein Complex / Q000737:chemistry*; D017434:Protein Structure, Tertiary; D011522:Protons; D014867:Water / Q000737:chemistry*
D045332:Photosystem II Protein Complex; D011522:Protons; D014867:Water; D008345:Manganese; D010100:Oxygen
density functional calculations; manganese; photosystem II; water splitting; water-oxidizing complex