Rationalizing the 1.9 A Crystal Structure of Photosystem II—A Remarkable Jahn-Teller Balancing Act Induced by a Single Proton Transfer

摘要

Green plants and algae oxidize water to molecular oxygen in photosystem II (PS II) within a calcium/tetramanganese site known as the water-oxidizing complex (WOC). Oxygen is generated by the WOC in a four-electron process involving a series of intermediate states (S states, labeled S0...S4) of increasingly higher mean oxidation level. Over the past decade, X-ray crystallographic (XRD) structures of PS II at progressively improved resolution have revealed much detail of the WOC. At present, only PS II from thermophilic cyanobacteria has been crystallized for XRD study and the enzyme is presumed to be in the dark stable S1 state. The first PS II structure (at 3.5 A resolution) to resolve side chain positions was presented by Barber and co-workers. Consistent with subsequent studies at higher resolution, it revealed the compact Mn3Ca "cube" structure of the WOC connected more distantly to a single Mn, referred to as the "dangler". More recent improved structures at 3.0 A and 2.9A, substantially clarified the metal- and protein-supplied ligand positions within the WOC, but were still of insufficient resolution to reveal the positions of bridging oxo groups and water molecules (including the substrate water molecules). Finally, Umena et al., using a new crystallization method, produced an atomic resolution structure at 1.9 A, the most resolved to date. Despite this remarkable achievement, revealing, for the first time, the positions of bridging O atoms within the Mn4Ca core of the WOC, aspects of the new structure have been met with scepticism. Central concerns over this structure involve 1) the identity and unexpected placement of the 0(5) moiety (Figure 1), which appears to be either a weakly bound oxo, hydroxo, or water ligand at distances of 2.4—2.7 A from four of the metal atoms in the WOC, and 2) the disparity in some key metal-metal distances when compared with earlier, high-precision extended X-ray absorption tine structure (EXAFS) results and the previous lower-resolution XRD structures (see Table 1). Although the Mn EXAFS data do not unambiguously assign the individual near (less than 3 A) metal-metal distances within the cluster, they clearly indicate that two Mn-Mn vectors of a magnitude of approximately 2.7 A exist within the functional WOC in the S1 and S2 states. These are totally consistent with the Mnl-Mn2 and Mn2-Mn3 distances of 2.65 A and 2.70 A in the 2.9 A resolution XRD structure, but are significantly shorter than the corresponding Mn-Mn distances of 2.80 A and 2.90 A seen in the 1.9 A resolution XRD structure.