Pulsed and Parallel-Polarization EPR Characterization of the Photosystem II Oxygen-Evolving Complex

Britt, R. David; and, Jeffrey M. Peloquin; Campbell, Kristy A.

doi:10.1146/annurev.biophys.29.1.463

Cited by 128 publications

(133 citation statements)

References 90 publications

Supporting

Mentioning

120

Contrasting

Order By: Relevance

“…These two polypeptides in particular are known to affect the integer spin EPR signals from the manganese cluster that forms part of the catalytic site, possibly mediating some struc- tural interaction within the catalytic site (43,44). In support of this proposal are the results from BBY samples specifically depleted of the 16-and 23-kDa polypeptides by NaCl washing (Fig.…”

Section: Resultsmentioning

confidence: 76%

Substrate Water Exchange in Photosystem II Depends on the Peripheral Proteins

Hillier¹,

Hendry²,

Burnap³

et al. 2001

Journal of Biological Chemistry

View full text Add to dashboard Cite

The 18 O exchange rates for the substrate water bound in the S 3 state were determined in different photosystem II sample types using time-resolved mass spectrometry. The samples included thylakoid membranes, saltwashed Triton X-100-prepared membrane fragments, and purified core complexes from spinach and cyanobacteria. For each sample type, two kinetically distinct isotopic exchange rates could be resolved, indicating that the biphasic exchange behavior for the substrate water is inherent to the O 2 -evolving catalytic site in the S 3 state. However, the fast phase of exchange became somewhat slower (by a factor of ϳ2) in NaClwashed membrane fragments and core complexes from spinach in which the 16-and 23-kDa extrinsic proteins have been removed, compared with the corresponding rate for the intact samples. For CaCl 2 -washed membrane fragments in which the 33-kDa manganese stabilizing protein (MSP) has also been removed, the fast phase of exchange slowed down even further (by a factor of ϳ3). Interestingly, the slow phase of exchange was little affected in the samples from spinach. For core complexes prepared from Synechocystis PCC 6803 and Synechococcus elongatus, the fast and slow exchange rates were variously affected. Nevertheless, within the experimental error, nearly the same exchange rates were measured for thylakoid samples made from wild type and an MSP-lacking mutant of Synechocystis PCC 6803. This result could indicate that the MSP has a slightly different function in eukaryotic organisms compared with prokaryotic organisms. In all samples, however, the differences in the exchange rates are relatively small. Such small differences are unlikely to arise from major changes in the metal-ligand structure at the catalytic site. Rather, the observed differences may reflect subtle long range effects in which the exchange reaction coordinates become slightly altered. We discuss the results in terms of solvent penetration into photosystem II and the regional dielectric around the catalytic site.The oxidation of water during photosynthesis is catalyzed by the membrane-bound pigment protein complex photosystem II (PSII).1 In the net reaction, four electrons, four protons, and one molecule of O 2 are liberated from the splitting of two water molecules. A key insight into the reaction mechanism was the observation that the O 2 produced in brief, saturating light flashes follows a periodicity of four (1). The period four phenomenon is now universally interpreted in terms of the S-state model, in which the catalytic site cycles through five intermediary S n states (n ϭ 0 -4) (2). Beginning in S 0 and traversing to S 4 , each S n state is driven forward by a single quantum event at the PSII reaction center. Upon reaching the S 4 state (which may be equivalent to S 3 Y Z ⅐ ) O 2 is released, S 0 is regenerated, and the cycle begins anew. The catalytic site for water oxidation involves an inorganic metal cluster consisting of four manganese ions, one Ca 2ϩ ion, possibly one Cl Ϫ ion, and the redox-active Tyr-161 resid...

show abstract

Section: Resultsmentioning

confidence: 76%

Substrate Water Exchange in Photosystem II Depends on the Peripheral Proteins

Hillier¹,

Hendry²,

Burnap³

et al. 2001

Journal of Biological Chemistry

View full text Add to dashboard Cite

show abstract

“…In addition, simulations of the EPR signals from the S 2 state also provide insight into the absolute Mn oxidation states in the S 2 state. S 2 -state EPR multiline signal simulations by Hasegawa et al 96,97 and 55 Mn ENDOR spectroscopy on the S 2 state by Britt and co-workers 98,99 100,101 the 2nd derivative of the XANES spectrum for the S 1 state shows that its edge shape is unlike the edge shape observed for Mn(III) complexes; when the 2nd-derivative XANES spectrum for the S 1 state is fit using Mn(III) and Mn(IV) model compounds, it cannot be fit well using only Mn(III) model compounds. 18,102 Furthermore, inspection of the only available set of tetranuclear Mn complexes with all O ligation, four distorted Mn 4 (III 3 ,IV) cubanes, shows XANES IPE values at ~6551 eV for these complexes, 20 consistent with the S 0 -state XANES IPE of 6550.8 eV and lower than the S 1 -state XANES IPE of 6552.9 eV.…”

Section: S 1 → S 2 Transitionmentioning

confidence: 99%

Absence of Mn-Centered Oxidation in the S₂→ S₃Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

et al. 2001

View full text Add to dashboard Cite

A key question for the understanding of photosynthetic water oxidation is whether the four oxidizing equivalents necessary to oxidize water to dioxygen are accumulated on the four Mn ions of the oxygen-evolving complex (OEC), or whether some ligand-centered oxidations take place before the formation and release of dioxygen during the S 3 → [S 4 ] → S 0 transition. Progress in instrumentation and flash sample preparation allowed us to apply Mn Kβ X-ray emission spectroscopy (Kβ XES) to this problem for the first time. The Kβ XES results, in combination with Mn X-ray absorption near-edge structure (XANES) and electron paramagnetic resonance (EPR) data obtained from the same set of samples, show that the S 2 → S 3 transition, in contrast to the S 0 → S 1 and S 1 → S 2 transitions, does not involve a Mn-centered oxidation. On the basis of new structural data from the S 3 -state, manganese μ-oxo bridge radical formation is proposed for the S 2 → S 3 transition, and three possible mechanisms for the O-O bond formation are presented.

show abstract

“…A variety of techniques have been applied, including electron paramagnetic resonance (EPR) spectroscopy Boussac et al 1989;Britt et al 2004;Britt et al 2000;Kulik et al 2005a;Kulik et al 2005b;Kulik et al 2005c;Matsukawa et al 1999;Messinger et al 1997a;Messinger et al 1997b;Miller & Brudvig 1991;Mino & Kawamori 2001;Nugent et al 1997;Peloquin & Britt 2001;Peloquin et al 1998;Peloquin et al 2000;Poluektov et al 2005;Razeghifard & Pace 1999), X-ray absorption spectroscopy (XAS) (Dau et al 2001;Dau et al 2003;Dau et al 2004;Grabolle et al 2006;Hasegawa et al 1999;Haumann et al 2005a;Haumann et al 2005b;Iuzzolino et al 1998;Liang et al 2000;Mishra et al 2007;Riggs-Gelasco et al 1996;Robblee et al 2002;Sauer & Yachandra 2004;Sauer et al 2005;Stemmler et al 1997;Yachandra 2002;Yachandra et al 1986;Yachandra et al 1987;Yano et al 2006;Yano et al 2005b), Fourier transform infrared (FTIR) spectroscopy (Chu et al 2004;Debus et al 2005;…”

Section: Structure and Mechanism Of The Oecmentioning

confidence: 99%

Computational insights into the O2-evolving complex of photosystem II

et al. 2008

View full text Add to dashboard Cite

Mechanistic investigations of the water-splitting reaction of the oxygen-evolving complex (OEC) of photosystem II (PSII) are fundamentally informed by structural studies. Many physical techniques have provided important insights into the OEC structure and function, including X-ray diffraction (XRD) and extended X-ray absorption fine structure (EXAFS) spectroscopy as well as mass spectrometry (MS), electron paramagnetic resonance (EPR) spectroscopy and Fourier transform infrared spectroscopy applied in conjunction with mutagenesis studies. However, experimental studies have yet to yield consensus as to the exact configuration of the catalytic metal cluster and its ligation scheme. Computational modeling studies, including density functional (DFT) theory combined with quantum mechanics/molecular mechanics (QM/MM) hybrid methods for explicitly including the influence of the surrounding protein, have proposed chemically satisfactory models of the fully ligated OEC within PSII that are maximally consistent with experimental results. The inorganic core of these models is similar to the crystallographic model upon which they were based but comprises important modifications due to structural refinement, hydration and proteinaceous ligation which improve agreement with a wide range of experimental data. The computational models are useful for rationalizing spectroscopic and crystallographic results and for building a complete structure-based mechanism of water-splitting in PSII as described by the intermediate oxidation states of the OEC. This review summarizes these recent advances in QM/MM modeling of PSII within the context of recent experimental studies.

show abstract

Pulsed and Parallel-Polarization EPR Characterization of the Photosystem II Oxygen-Evolving Complex

Cited by 128 publications

References 90 publications

Substrate Water Exchange in Photosystem II Depends on the Peripheral Proteins

Substrate Water Exchange in Photosystem II Depends on the Peripheral Proteins

Absence of Mn-Centered Oxidation in the S₂→ S₃Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

Computational insights into the O2-evolving complex of photosystem II

Contact Info

Product

Resources

About

Pulsed and Parallel-Polarization EPR Characterization of the Photosystem II Oxygen-Evolving Complex

Cited by 128 publications

References 90 publications

Substrate Water Exchange in Photosystem II Depends on the Peripheral Proteins

Substrate Water Exchange in Photosystem II Depends on the Peripheral Proteins

Absence of Mn-Centered Oxidation in the S2→ S3Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

Computational insights into the O2-evolving complex of photosystem II

Contact Info

Product

Resources

About

Absence of Mn-Centered Oxidation in the S₂→ S₃Transition: Implications for the Mechanism of Photosynthetic Water Oxidation