Assignment of the μ4-O5 atom in catalytic center for water oxidation in photosystem II

Abstract

The detailed structure of catalytic center of water oxidation, Mn 4 Ca-cluster, in photosystem II (PSII) has been reported recently. However, due to the radiation damage induced by X-ray and the complexity of the Mn 4 Ca-cluster, the assignment of the  4 -O5 atom coordinated by three Mn and one Ca 2+ ions is still lack of essential evidences. In this article, we synthesized one Mn complex containing two  4 -O atoms. It is found that the lengths of all  4 -O-Mn bonds in this Mn complex are in the range of 1.89-2.10 Å, which are significantly shorter than 2.40-2.61 Å distance of  4 -O5-Mn bonds in Mn 4 Ca-cluster observed in the crystal structure of PSII. In addition, DFT calculations have been carried out on the Mn 4 Ca-cluster. It is found that the O atom of  4 -O or  4 -OH always trends to deviate from the center position of four metal ions, resulting in unequal bond lengths of four  4 -O-M (M=Mn or Ca), which is obviously different with larger and nearly equal distances between  4 -O and four metal ions observed in the crystal structure. Based on these results, we suggest that the  4 -atom in Mn 4 Ca-cluster of PSII is unlikely to be a Recently, Umena et al. [7] have reported the crystal structure of PSII at a resolution of 1.9 Å, which revealed the detailed structure of the Mn 4 Ca-cluster. The core of the Mn 4 Ca-cluster is shown in Figure 1, wherein four Mn and one Ca ions are connected by five -O atoms. The distances between  3 -O/ 2 -O and Mn ions are all in the range of 1.8-2.1 Å; while the lengths of three  4 -O5-Mn bonds are in the range of 2.4-2.61 Å. The latter is significant longer than those of  2 -O-Mn or  3 -O-Mn bonds. The apparently larger and nearly equal lengths of three  4 -O-Mn bonds indicate that the  4 -O5 atom is very special. In fact, this  4 -O5 atom has attracted extensive attentions by theoretical studies recently, and several groups [8][9][10] suggested that the  4 -O5 atom may play crucial roles to provide one oxygen source for the O-O bond formation. However, due to radiation damage induced by X-ray [11,12] and the complexity of the Mn 4 Ca-cluster, especially the assignment of this  4 -O5 atom was suffered by its weak electron density compared with all other O atoms in Mn 4 Ca-cluster in X-ray diffraction data [7]. Therefore, the assignment of  4 -O5 is still an open question. Here, we have carried out DFT calculations on Mn 4 Ca-cluster to check the rationality of the assignment of  4 -O5 atom. In addition, we have also synthesized a manganese complex containing  4 -O atom. The structural analysis on this compound further provides a clue to demonstrate the possible structure characters of the  4 -O in

A synthetic model for the oxygen-evolving complex in Sr2+-containing photosystem II

“…The lengths of the two m 4 -O-Mn in complex 1 are in the range of 1.84 Å to 1.87 Å with an average of 1.86 Å, which is a common distance for m 4 -O 2À -Mn in most multinuclear Mn complexes and heteronuclear MnSr or MnCa complexes. 24,25,35,39 However, the length of 1.86 Å is remarkably shorter (by 0.64 Å) than the average value of 2.5 Å in the OEC of Ca 2+ or Sr 2+ containing PSII. 4,5 It is important to point out that the m 4 -O5 atom in the OEC has attracted extensive attention in the studies of water oxidation in PSII recently.…”

“…4,5 It is important to point out that the m 4 -O5 atom in the OEC has attracted extensive attention in the studies of water oxidation in PSII recently. 14,16,17,[39][40][41][42][43] Theoretical studies 16,17 have suggested that the m 4 -O5 atom may act as a source of oxygen atoms for the formation of O-O bonds in the higher S-state (e.g. S 3 , S 4 ) of the OEC, in which the valences for all Mn ions are most likely to be +4, 8,9 similar to that in complex 1.…”

“…It is important to mention that the assignment of this m 4 -O5 atom was not unambiguous due to its much weaker electron density than all other bridging oxido moieties in the X-ray diffraction data of the OEC. 4,5,39 The structural characteristics of the m 4 -O 2À in complex 1 and various MnSr-MnCa complexes 24,25,35 could be considered as structural pieces of evidence to argue that the binding and the function of the m 4 -O5 atom in the OEC is worth being addressed in the future.…”

Artificial synthetic MnIVCa–oxido complexes mimic the oxygen-evolving complex in photosystem II

“…The turnover of the OEC for water-splitting involves five different S-states (S n , n = 0-4). Due to the involvement of a large protein matrix and the structural complexity and uncertainty of the OEC in higher S-states, [9][10][11][12][13][14][15] the mechanism of O-O bond formation [16][17][18][19][20][21] and functional roles of Ca 2+ (ref. [22][23][24][25] remain debatable.…”

Artificial bioconversion of carbon dioxide

“…PSII is a photoactive complex located on thylakoid membrane (TK) in green plants, cyanobacteria, and microalgae [51,52]. It can convert solar energy into chemical fuels and provide the materials and energy for almost all living creatures, including humans.…”