Metal oxidation states in the oxygen-evolving complex: A computational challenge

V. Krewald, M. Retegan, N. Cox, J. Messinger, W. Lubitz, S. DeBeer, F. Neese and D.A. Pantazis,
Chemical Science 2015, early-view (Open-Access)
Contributed by Marcel Swart

The determination of oxidation states of metals in biological systems is not an easy task and can lead to surprises or controversies. This was for instance shown last year when an unusual molybdenum(III) oxidation state in the nitrogenase enzyme was reported [1], or the year before [2] for a Sc-capped iron-oxygen complex where the crystal structure shows a iron(III) oxidation state unlike the expected iron(IV) state based on solution data [3].
The situation is infinitely more complex when more than one metal ion is present, as is the case in the oxygen evolving complex (OEC) of photosystem II that is studied here through a combination of computational chemistry and spectroscopy. The OEC contains 4 manganese and 1 calcium as the active species to convert water into oxygen. Many studies have been performed on the five stages along the catalytic cycle, often with contradictory conclusions about the geometry, electronic structure, oxidation and protonation states involved.

Summary of the catalytic cycle with the five stages (reproduced with permission from Chem. Sci., 2015, Advance Article, DOI: 10.1039/C4SC03720K; Published by The Royal Society of Chemistry) 

A breakthrough was a recent atomic resolution crystal structure [4] that largely confirmed the theoretical predictions by Siegbahn [5] about the geometrical positioning of the manganese ions and the oxygens. Still, a detailed understanding of the oxidation states was lacking, which is being explored in the paper by Pantazis and co-workers through a combination of a variety of experimental and theoretical techniques.

Typical model system used in the calculations (reproduced with permission from Chem. Sci., 2015, Advance Article, DOI: 10.1039/C4SC03720K; Published by The Royal Society of Chemistry) 

It is this combination of both theory and experiment, and the systematic exploration of protonation states, open- vs. closed cubane structure, distribution of +3/+4 oxidation states over the different manganese ions that makes this a complete and convincing story for the assignment of high-valent (HV) oxidation states along the catalytic cycle.

One example of the different possible distributions of oxidation states (III or IV) and spin states (1/2, 5/2 or 13/2), for state 2 models (reproduced with permission from Chem. Sci., 2015, Advance Article, DOI: 10.1039/C4SC03720K; Published by The Royal Society of Chemistry) 

The HV assignments made are consistent with the experimental data obtained so far, including a very recent “radiation-damage-free” crystal structure [6], for the first three stages of the catalytic cycle (S1-S3). What remains to be explored is how the enzyme produces the dioxygen molecule in the S4 stage and returns back to the resting state S0. Without any doubt, further unexpected findings will be coming along for this intriguing catalytic cycle.

[1] Chem. Sci. 2014, 5, 3096-3103, DOI: 10.1039/C4SC00337C 
[2] Chem. Commun. 2013, 49, 6650-6652, DOI: 10.1039/c3cc42200c
[3] Nature Chem. 2010, 2, 756-759, DOI: 10.1038/nchem.731
[4] Nature 2011, 473, 55-60, DOI: 10.1038/nature09913
[5] Acc. Chem. Res. 2009, 42, 1871-1880, DOI: 10.1021/ar900117k
[6] Nature 2015, 517, 99-103, DOI: 10.1038/nature13991


This work is licensed under a Creative Commons Attribution 3.0 Unported License. 

Intrinsic Atomic Orbitals: An Unbiased Bridge between Quantum Theory and Chemical Concepts

Gerald Knizia J. Chem. Theory Comput. doi:10.1021/ct400687b (Article ASAP)
Contributed by J. Grant Hill.

Readers of Computational Chemistry Highlights are already aware of the power of quantum chemistry in determining/predicting physical observables, but familiar chemical concepts (including the covalent bond!) are, at best, loosely defined in quantum mechanics. This is neatly summarised in Knizia's paper:

"quantum chemistry methods can determine benzene's heat of formation with an accuracy of <2 kJ/mol; but, strictly speaking, they can neither determine the partial charges on benzene's carbon atoms, nor can they show that benzene has twelve localized sigma-bonds and a delocalized pi-system."

 A number of techniques including the quantum theory of atoms in molecules [1], natural bond orbitals [2] and modern valence bond theory [3], to name just a few, have all sought to connect quantum mechanics with concepts known to all chemists, including partial charges, electronegativity, Lewis structures etc. All have been successful to some degree, but often include some assumptions or have complicated programs that require specialist knowledge to run and interpret.

This work by Knizia defines a new method of intrinsic atom orbitals (IAOs) that can exactly express the occupied MOs of an accurate wave function. This is then combined with an orbital localization procedure to construct bond orbitals (IBOs). It is demonstrated that this method is insensitive to basis set size (unlike Mulliken charges), correctly predicts differences in electronegativities, produces the "correct" bond orbitals for some nontrivial cases and can calculate oxidation states of transition-metal complexes (building upon the work of Sit et al.[4]).

This initial implementation of the method shows great promise as an additional tool in the translation of quantum mechanical results into the chemical vernacular, and it will be interesting to observe how it may be applied. My own attraction to the method is due to it combining simplicity of approach with the natural emergence of Lewis structures in the absence of any bias/assumption.

Footnote: The IAO/IBO method will be included in the next public release of the MOLPRO program package, and a sample python implementation will be made available on the author's website (it had not yet been uploaded at the time of writing). Algorithm details are included in an appendix.

References

[1] R. F. W. Bader. A quantum theory of molecular structure and its applications. Chem. Rev. 1991, 91, 893.

[2] E. D. Glendening, C. R. Landis and F. Weinhold. Natural Bond Orbital Methods. WIREs Comput. Mol. Sci. 2012, 2, 1.

[3] J. Gerratt, D. L. Cooper, P. B. Karadakov and M. Raimondi. Modern valence bond theory. Chem. Soc. Rev. 1997, 26, 87; S. Shaik and P. C. Hiberty. A primer on qualitative valence bond theory - a theory coming of age. WIREs Comput. Mol. Sci. 2011, 1, 18.

[4] P. H.-L. Sit, R. Car, M. H. Cohen and A. Selloni. Simple, Unambiguous Theoretical Approach to Oxidation State Determination via First-Principles Calculation. Inorg. Chem. 2011, 50, 10259.