Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting
- 12 February 2008
- journal article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences
- Vol. 105 (6) , 1879-1884
- https://doi.org/10.1073/pnas.0707092105
Abstract
Photosynthetic water oxidation, where water is oxidized to dioxygen, is a fundamental chemical reaction that sustains the biosphere. This reaction is catalyzed by a Mn4Ca complex in the photosystem II (PS II) oxygen-evolving complex (OEC): a multiprotein assembly embedded in the thylakoid membranes of green plants, cyanobacteria, and algae. The mechanism of photosynthetic water oxidation by the Mn4Ca cluster in photosystem II is the subject of much debate, although lacking structural characterization of the catalytic intermediates. Biosynthetically exchanged Ca/Sr-PS II preparations and x-ray spectroscopy, including extended x-ray absorption fine structure (EXAFS), allowed us to monitor Mn-Mn and Ca(Sr)-Mn distances in the four intermediate S states, S0 through S3, of the catalytic cycle that couples the one-electron photochemistry occurring at the PS II reaction center with the four-electron water-oxidation chemistry taking place at the Mn4Ca(Sr) cluster. We have detected significant changes in the structure of the complex, especially in the Mn-Mn and Ca(Sr)-Mn distances, on the S2-to-S3 and S3-to-S0 transitions. These results implicate the involvement of at least one common bridging oxygen atom between the Mn-Mn and Mn-Ca(Sr) atoms in the O-O bond formation. Because PS II cannot advance beyond the S2 state in preparations that lack Ca(Sr), these results show that Ca(Sr) is one of the critical components in the mechanism of the enzyme. The results also show that Ca is not just a spectator atom involved in providing a structural framework, but is actively involved in the mechanism of water oxidation and represents a rare example of a catalytically active Ca cofactor.Keywords
This publication has 47 references indexed in Scilit:
- cis,cis-[(bpy)2RuVO]2O4+ Catalyzes Water Oxidation Formally via in Situ Generation of Radicaloid RuIV−O•Journal of the American Chemical Society, 2006
- Evidence from Biosynthetically Incorporated Strontium and FTIR Difference Spectroscopy that the C-Terminus of the D1 Polypeptide of Photosystem II Does Not Ligate CalciumBiochemistry, 2005
- Biosynthetic Ca2+/Sr2+ Exchange in the Photosystem II Oxygen-evolving Enzyme of Thermosynechococcus elongatusJournal of Biological Chemistry, 2004
- An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signaturesJBIC Journal of Biological Inorganic Chemistry, 2001
- Effects of Sr2+-Substitution on the Reduction Rates of Yz• in PSII MembranesEvidence for Concerted Hydrogen-Atom Transfer in Oxygen EvolutionBiochemistry, 2000
- Identification of a Mn−O−Mn Cluster Vibrational Mode of the Oxygen-Evolving Complex in Photosystem II by Low-Frequency FTIR SpectroscopyBiochemistry, 2000
- Evidence for the Proximity of Calcium to the Manganese Cluster of Photosystem II: Determination by X-ray Absorption SpectroscopyBiochemistry, 1995
- Structural and Magnetic Effects of Successive Protonations of Oxo Bridges in High-Valent Manganese DimersJournal of the American Chemical Society, 1994
- Ca2+ binding to the oxygen evolving enzyme varies with the redox state of the Mn clusterFEBS Letters, 1988
- Nature of the inhibition of the oxygen-evolving enzyme of photosystem II induced by sodium chloride washing and reversed by the addition of calcium(2+) or strontium(2+)Biochemistry, 1988