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

ABSTRACT: Among the four photo-driven transitions of the water-oxidizing tetramanganese-calcium cofactor of biological photosynthesis, the second-last step of the catalytic cycle, that is the S2 to S3 state transition, is the crucial step that poises the catalyst for the final O-O bond formation. This transition, whose intermediates are not yet fully understood, is a multi-step process that involves the redox-active tyrosine residue and includes oxidation and deprotonation of the catalytic cluster, as well as the binding of a water molecule. Spectroscopic data has the potential to shed light on the sequence of events that comprise this catalytic step, which still lacks a structural interpretation. In this work the S2-S3 state transition is studied and a key intermediate species is characterized: it contains a Mn3O4Ca cubane subunit linked to a five-coordinate Mn(iv) ion that adopts an approximately trigonal bipyramidal ligand field. It is shown using high-level density functional and multireference wave function calculations that this species accounts for the near-infrared absorption and electron paramagnetic resonance observations on metastable S2-S3 intermediates. The results confirm that deprotonation and Mn oxidation of the cofactor must precede the coordination of a water molecule, and lead to identification of a novel low-energy water binding mode that has important implications for the identity of the substrates in the mechanism of biological water oxidation.

SUBMITTER: Retegan M

PROVIDER: S-EPMC5950799 | biostudies-other | 2016 Jan

REPOSITORIES: biostudies-other

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

Retegan Marius M Krewald Vera V Mamedov Fikret F Neese Frank F Lubitz Wolfgang W Cox Nicholas N Pantazis Dimitrios A DA

Chemical science 20151117 1

Among the four photo-driven transitions of the water-oxidizing tetramanganese-calcium cofactor of biological photosynthesis, the second-last step of the catalytic cycle, that is the S<sub>2</sub> to S<sub>3</sub> state transition, is the crucial step that poises the catalyst for the final O-O bond formation. This transition, whose intermediates are not yet fully understood, is a multi-step process that involves the redox-active tyrosine residue and includes oxidation and deprotonation of the cat ...[more]

PMID: 29861966

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Project description:A central question in biological water splitting concerns the oxidation states of the manganese ions that comprise the oxygen-evolving complex of photosystem II. Understanding the nature and order of oxidation events that occur during the catalytic cycle of five S i states (i = 0-4) is of fundamental importance both for the natural system and for artificial water oxidation catalysts. Despite the widespread adoption of the so-called "high-valent scheme"-where, for example, the Mn oxidation states in the S2 state are assigned as III, IV, IV, IV-the competing "low-valent scheme" that differs by a total of two metal unpaired electrons (i.e. III, III, III, IV in the S2 state) is favored by several recent studies for the biological catalyst. The question of the correct oxidation state assignment is addressed here by a detailed computational comparison of the two schemes using a common structural platform and theoretical approach. Models based on crystallographic constraints were constructed for all conceivable oxidation state assignments in the four (semi)stable S states of the oxygen evolving complex, sampling various protonation levels and patterns to ensure comprehensive coverage. The models are evaluated with respect to their geometric, energetic, electronic, and spectroscopic properties against available experimental EXAFS, XFEL-XRD, EPR, ENDOR and Mn K pre-edge XANES data. New 2.5 K 55Mn ENDOR data of the S2 state are also reported. Our results conclusively show that the entire S state phenomenology can only be accommodated within the high-valent scheme by adopting a single motif and protonation pattern that progresses smoothly from S0 (III, III, III, IV) to S3 (IV, IV, IV, IV), satisfying all experimental constraints and reproducing all observables. By contrast, it was impossible to construct a consistent cycle based on the low-valent scheme for all S states. Instead, the low-valent models developed here may provide new insight into the over-reduced S states and the states involved in the assembly of the catalytically active water oxidizing cluster.

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

Publications

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

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