X-ray Emission Spectroscopy of Mn Coordination Complexes Toward Interpreting the Electronic Structure of the Oxygen-Evolving Complex of Photosystem II

Davis, Katherine M.; Palenik, Mark C.; Yan, Limei; Smith, Paul F.; Seidler, Gerald T.; Dismukes, G. Charles; Pushkar, Yulia

doi:10.1021/acs.jpcc.5b10610

Cited by 24 publications

(32 citation statements)

References 55 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Overall, and while acknowledging the existence of alternative interpretations (e.g., [75][76][77][78][79]), the available information from spectroscopy is most consistent with Mn-centered oxidation in the S 2 -S 3 transition resulting in an all-Mn(IV) cluster, accompanied by a structural change that renders all Mn ions six-coordinate.…”

Section: Geometric and Electronic Information On The S 3 Statementioning

confidence: 82%

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

Pantazis

2019

Inorganics

View full text Add to dashboard Cite

The catalytic cycle of the oxygen-evolving complex (OEC) of photosystem II (PSII) comprises five intermediate states Si (i = 0–4), from the most reduced S0 state to the most oxidized S4, which spontaneously evolves dioxygen. The precise geometric and electronic structure of the Si states, and hence the mechanism of O–O bond formation in the OEC, remain under investigation, particularly for the final steps of the catalytic cycle. Recent advances in protein crystallography based on X-ray free-electron lasers (XFELs) have produced new structural models for the S3 state, which indicate that two of the oxygen atoms of the inorganic Mn4CaO6 core of the OEC are in very close proximity. This has been interpreted as possible evidence for “early-onset” O–O bond formation in the S3 state, as opposed to the more widely accepted view that the O–O bond is formed in the final state of the cycle, S4. Peroxo or superoxo formation in S3 has received partial support from computational studies. Here, a brief overview is provided of spectroscopic information, recent crystallographic results, and computational models for the S3 state. Emphasis is placed on computational S3 models that involve O–O formation, which are discussed with respect to their agreement with structural information, experimental evidence from various spectroscopic studies, and substrate exchange kinetics. Despite seemingly better agreement with some of the available crystallographic interpretations for the S3 state, models that implicate early-onset O–O bond formation are hard to reconcile with the complete line of experimental evidence, especially with X-ray absorption, X-ray emission, and magnetic resonance spectroscopic observations. Specifically with respect to quantum chemical studies, the inconclusive energetics for the possible isoforms of S3 is an acute problem that is probably beyond the capabilities of standard density functional theory.

show abstract

Section: Geometric and Electronic Information On The S 3 Statementioning

confidence: 82%

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

Pantazis

2019

Inorganics

View full text Add to dashboard Cite

show abstract

“…Although the proposed Mn oxidation to form Mn 4 IV in the S 3 state [39–43] Figure 1A, at its most basic, suggests a comparable XES shift for S 1 → S 2 and S 2 → S 3 transitions, we now know that the OEC undergoes a major structural change during the S 2 → S 3 transition from both extended x-ray fine structure (EXAFS) [36], femtosecond (fs) x-ray crystallography [9–11], and electron paramagnetic resonance (EPR) [42]. Studies on model compounds indicate that changes to the local spin densities associated with structural rearrangements, such as changes to the ligand environment, could obscure a Mn-centered oxidative shift [29,44,45]. Minimal changes to the emission spectra, observed upon the S 2 → S 3 transition in previous studies, were attributed to ligand-centered oxidation [35].…”

Section: S2 To S3 State Transitionmentioning

confidence: 99%

Rapid Evolution of the Photosystem II Electronic Structure during Water Splitting

et al. 2018

Self Cite

View full text Add to dashboard Cite

Photosynthetic water oxidation is a fundamental process that sustains the biosphere. A Mn4Ca cluster embedded in the photosystem II protein environment is responsible for the production of atmospheric oxygen. Here, time-resolved x-ray emission spectroscopy (XES) was used to observe the process of oxygen formation in real time. These experiments reveal that the oxygen evolution step, initiated by three sequential laser flashes, is accompanied by rapid (within 50 μs) changes to the Mn Kβ XES spectrum. However, no oxidation of the Mn4Ca core above the all MnIV state was detected to precede O−O bond formation, and the observed changes were therefore assigned to O−O bond formation dynamics. We propose that O−O bond formation occurs prior to the transfer of the final (4th) electron from the Mn4Ca cluster to the oxidized tyrosine YZ residue. This model resolves the kinetic limitations associated with O−O bond formation, and suggests an evolutionary adaptation to avoid releasing of harmful peroxide species.

show abstract

“…129,152 Theoretical studies have described the electronic structure and magnetic properties of these complexes, as well as the possible pathways for dioxygen evolution. [153][154][155] Another example of the butterfly type of complex is the series oxidation states from Mn(II) 2 Mn(III) 2 to Mn(III) 4 , which contains a non-planar Mn 4 unit, with two Mn atoms forming a central Mn 2 O 2 diamond core and the other two Mn ions being ligated to the oxo bridges ( Fig. 6).…”

Section: Tetramanganese Complexesmentioning

confidence: 99%

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

2017

View full text Add to dashboard Cite

show abstract

X-ray Emission Spectroscopy of Mn Coordination Complexes Toward Interpreting the Electronic Structure of the Oxygen-Evolving Complex of Photosystem II

Cited by 24 publications

References 55 publications

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

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

Rapid Evolution of the Photosystem II Electronic Structure during Water Splitting

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

Contact Info

Product

Resources

About