Differences in the Active Site of Water Oxidation among Photosynthetic Organisms

Abstract

The site of biological water oxidation is highly conserved across photosynthetic organisms, but differences of unidentified structural and electronic origin exist between taxonomically discrete clades, revealed by distinct spectroscopic signatures of the oxygen-evolving MnCaO cluster and variations in active-site accessibility. Comparison of atomistic models of a native cyanobacterial form (Thermosynechococcus vulcanus) and a chimeric spinach-like form of photosystem II allows us to identify the precise atomic-level differences between organisms in the vicinity of the manganese cluster. Substitution of cyanobacterial D1-Asn87 by higher-plant D1-Ala87 is the principal discriminating feature: it drastically rearranges a network of proximal hydrogen bonds, modifying the local architecture of a water channel and the interaction of second coordination shell residues with the manganese cluster. The two variants explain species-dependent differences in spectroscopic properties and in the interaction of substrate analogues with the oxygen-evolving complex, enabling assignment of a substrate delivery channel to the active site.

Substrate water exchange in the S2 state of photosystem II is dependent on the conformation of the Mn4Ca cluster

“…W2, here assumed to be a hydroxide, can be expected to exchange in the S HS 2 = S B 2 state readily with bulk water (lower panel in Scheme 3) since Mn4(III) is placed near the exit of two proposed water channels (O4 and Cl channels) and is also in reach of W3 that is connected to the O1 water channel. 3,[105][106][107][108][109][110][111][112] Water exchange in the S LS 2 = S A 2 state would then occur via the equilibrium with the S B 2 conformation (Scheme 3 and pathway II in Fig. 4).…”

The S3 State of the Oxygen-Evolving Complex: Overview of Spectroscopy and XFEL Crystallography with a Critical Evaluation of Early-Onset Models for O–O Bond Formation

“…Furthermore, the S3 B state might be silent in X-band because of the high zero-field splitting associated with the five-coordinate Mn4 [104,107], but this has not been explicitly demonstrated yet. Binding of water at Mn4 through a channel associated with the interaction of small molecules such as methanol and ammonia [4,[110][111][112][113][114][115][116][117][118][119] completes the coordination sphere of this ion leading to the structure labeled S3 B,W in Figure 5 (where the superscript W indicates binding of an extra water molecule). This isomerizes to S3 A,W by a simple bond rearrangement [120].…”

“…This pathway for water delivery is plausible, but the water movement and the deprotonation of Ca-bound water were both predicted to be energetically disfavored [104,106,123] or could not be independently reproduced in computer simulations [101]. Additionally, access to the OEC of methanol and ammonia likely proceeds through a different channel [4,[110][111][112][113][114][115][116][117][118], rendering this water delivery mechanism rather unexpected. Finally, this scenario does not involve intermediates that can obviously explain the EPR and NIR phenomenology described above, either in terms of which S 2 -state EPR signals correspond to species able to progress to the S 3 state, or in terms of the spectroscopic behavior of the S 3 state itself.…”

“…The particular form (S 3 B ), which according to the above scenario is the first structural component of the S 3 state, provides a natural explanation of the NIR absorption: this is attributed to a d xz -d z Binding of water at Mn4 through a channel associated with the interaction of small molecules such as methanol and ammonia[4,[110][111][112][113][114][115][116][117][118][119] completes the coordination sphere of this ion leading to the structure labeled S 3 B,W inFigure 5(where the superscript W indicates binding of an extra water molecule). This isomerizes to S 3 A,W by a simple bond rearrangement[120].According to the above hypothesis, the prevalent structural form of the S 3 state might be represented by S 3 A,W , but this may coexist with the S 3 B,W isomer as well as with a form of the latter that lacks a sixth ligand at the terminal Mn4 (S 3 B ).…”

Water Network Dynamics Next to the Oxygen-Evolving Complex of Photosystem II

“…Force fields require significant parameterization, especially for nonstandard residues and metal-containing systems, such as the OEC. Classical molecular dynamics simulations have been performed on PSII and get around the parameter problem by making the OEC and other metal cofactors static [11,12]. Valence charges are assigned to a non-bonded model of the OEC and the complex and its ligating residues are locked into their crystal structure or QM-calculated coordinates.…”