On Ammonia Binding to the Oxygen‐Evolving Complex of Photosystem II: A Quantum Chemical Study

Abstract

A recent EPR study (M. Perrez Navarro et al., Proc. Natl. Acad. Sci. 2013, 110, 15561) provided evidence that ammonia binding to the oxygen-evolving complex (OEC) of photosystem II in its S2 state takes place at a terminal-water binding position (W1) on the "dangler" manganese center MnA. This contradicted earlier interpretations of (14)N electron-spin-echo envelope modulation (ESEEM) and extended X-ray absorption fine-structure (EXAFS) data, which were taken to indicate replacement of a bridging oxo ligand by an NH2 unit. Here we have used systematic broken-symmetry density functional theory calculations on large (ca. 200 atom) model clusters of an extensive variety of substitution patterns and core geometries to examine these contradictory pieces of evidence. Computed relative energies clearly favor the terminal substitution pattern over bridging-ligand arrangements (by about 20-30 kcal mol(-1)) and support W1 as the preferred binding site. Computed (14)N EPR nuclear-quadrupole coupling tensors confirm previous assumptions that the appreciable asymmetry may be accounted for by strong, asymmetric hydrogen bonding to the bound terminal NH3 ligand (mainly by Asp61). Indeed, bridging NH2 substitution would lead to exaggerated asymmetries. Although our computed structures confirm that the reported elongation of an Mn-Mn distance by about 0.15 Å inferred from EXAFS experiments may only be reproduced by bridging NH2 substitution, it seems possible that the underlying EXAFS data were skewed by problems due to radiation damage. Overall, the present data clearly support the suggested terminal NH3 coordination at the W1 site. The finding is significant for the proposed mechanistic scenarios of OEC catalysis, as this is not a water substrate site, and effects of this ammonia binding on catalysis thus must be due to more indirect influences on the likely substrate binding site at the O5 bridging-oxygen position.

Interaction of methanol with the oxygen-evolving complex: atomistic models, channel identification, species dependence, and mechanistic implications

“…Comparison of PS-II amino acid sequences from plants and cyanobacteria reveal a conserved difference close to the proposed site of interaction, offering a structure-based explanation for the species-dependent response to methanol. By combining the present results with recent studies of ammonia interaction with the OEC 44,64,66,83 it is possible to assign a unique channel as active in delivery of substrate analogues to the OEC. Taking into account the studies of the S 2 –S 3 transition and the associated “pivot” mechanism for water binding, 73 we conclude that the dangler manganese (Mn4) is the only directly accessible Mn ion of the cluster and that substrate inclusion to the OEC occurs through initial binding at this site.…”

“…35,135 Although this idea is not implausible, 135 it seems to us improbable for three reasons: (a) explicit calculation of protonation patterns by a wide variety of methods 72,118,119 suggests that O4 protonation is unfavorable in S 0 , therefore the basis for these computational constructs is questionable; (b) the involvement of this channel in the delivery of methanol (identified here), of ammonia (as a ligand to Mn4), 44,64,66,83 as well as of water in the S 3 state 73 would necessitate an unlikely dual role for this channel; and (c) residue D1-Asn87 would have to be involved in the hypothetical proton transfer, so models that might be valid for T. vulcanus would not be transferable to D1-Ala87 organisms, which is implausible for a function as critical as proton removal from the water oxidation site. Proton egress instead is most likely to occur via the other channel associated with D1-Asp61, as previously assigned by Knapp and co-workers based on the monotonic increase of calculated p K a values of titratable residues, 34 and by FTIR and mutation studies.…”

“…25 Moreover, recent experimental and theoretical work has demonstrated that NH 3 binds to Mn4 in the place of W1 in the S 2 state of the OEC. 44,64,66,83 Although the interaction modes of NH 3 and MeOH are fundamentally different—the first one acting as a direct ligand to Mn4, the latter interacting from the second coordination sphere—access of methanol coincides with access of ammonia. This is consistent with competition studies that showed interrelations between the binding of these substrate analogues 56 and reinforces the assignment of the O4 channel as the one involved in delivery of substrate analogues, and, by extension, of substrate water.…”

A five-coordinate Mn(iv) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding

“…Importantly, this type of water binding is not only favorable based on computed energetics, but is also aligned with recent experimental and theoretical studies of ammonia interaction with the OEC. 53 , 55 , 113 , 114 These studies suggest that NH 3 interacts with the inorganic cluster in the S 2 state through coordination at Mn4, from precisely the same side of the cluster and at the same coordination site, that is, by displacement of W1. This supports the notion that NH 3 accesses the cluster through the same water channel (referred to in the literature as “narrow channel” 106 or “channel 2” 111 ) suggested here to be involved in the delivery of W new during the S 2 –S 3 transition.…”

Structural models of the biological oxygen-evolving complex: achievements, insights, and challenges for biomimicry

“…182 Attachment of a "dangler" ion Critical roles have been attributed to the fourth manganese of the OEC in the bioassembly of the cluster, solvent/substrate attachment, and catalytic function. 49,52,84,91,[183][184][185][186][187][188][189][190][191][192][193] Although an architecture containing a Mn 3 CaO 4 cubane attached to another manganese ion was discussed already (Fig. 8), these complexes had overall much higher nuclearity than the biological cluster.…”