7 research outputs found
Spectroscopic Evidence for a Redox-Controlled Proton Gate at Tyrosine D in Photosystem II
Tyrosine D (TyrD) is one of two well-studied
redox active tyrosines
in Photosystem II. TyrD shows redox kinetics much slower than that
of its homologue, TyrZ, and is normally present as a stable deprotonated
radical (TyrD<sup>ā¢</sup>). We have used time-resolved continuous
wave electron paramagnetic resonance and electron spin echo envelope
modulation spectroscopy to show that deuterium exchangeable protons
can access TyrD on a time scale that is much faster (50ā100
times) than that previously observed. The time of H/D exchange is
strongly dependent on the redox state of TyrD. This finding can be
related to a change in position of a water molecule close to TyrD
FTIR Study of Manganese Dimers with Carboxylate Donors As Model Complexes for the Water Oxidation Complex in Photosystem II
The carboxylate stretching frequencies of two high-valent,
di-Ī¼-oxido
bridged, manganese dimers has been studied with IR spectroscopy in
three different oxidation states. Both complexes contain one monodentate
carboxylate donor to each Mn ion, in one complex, the carboxylate
is coordinated perpendicular to the Mn-(Ī¼-O)<sub>2</sub>-Mn
plane, and in the other complex, the carboxylate is coordinated in
the Mn-(Ī¼-O)<sub>2</sub>-Mn plane. For both complexes, the difference
between the asymmetric and the symmetric carboxylate stretching frequencies
decrease for both the Mn<sub>2</sub><sup>IV,IV</sup> to Mn<sub>2</sub><sup>III,IV</sup> transition and the Mn<sub>2</sub><sup>III,IV</sup> to Mn<sub>2</sub><sup>III,III</sup> transition, with only minor
differences observed between the two arrangements of the carboxylate
ligand versus the Mn-(Ī¼-O)<sub>2</sub>-Mn plane. The IR spectra
also show that both carboxylate ligands are affected for each one
electron reduction, i.e., the stretching frequency of the carboxylate
coordinated to the Mn ion that is not reduced also shifts. These results
are discussed in relation to FTIR studies of changes in carboxylate
stretching frequencies in a one electron oxidation step of the water
oxidation complex in Photosystem II
Stability of the S<sub>3</sub> and S<sub>2</sub> State Intermediates in Photosystem II Directly Probed by EPR Spectroscopy
The stability of the S<sub>3</sub> and S<sub>2</sub> states
of
the oxygen evolving complex in photosystem II (PSII) was directly
probed by EPR spectroscopy in PSII membrane preparations from spinach
in the presence of the exogenous electron acceptor P<i>p</i>BQ at 1, 10, and 20 Ā°C. The decay of the S<sub>3</sub> state
was followed in samples exposed to two flashes by measuring the split
S<sub>3</sub> EPR signal induced by near-infrared illumination at
5 K. The decay of the S<sub>2</sub> state was followed in samples
exposed to one flash by measuring the S<sub>2</sub> state multiline
EPR signal. During the decay of the S<sub>3</sub> state, the S<sub>2</sub> state multiline EPR signal first increased and then decreased
in amplitude. This shows that the decay of the S<sub>3</sub> state
to the S<sub>1</sub> state occurs via the S<sub>2</sub> state. The
decay of the S<sub>3</sub> state was biexponential with a fast kinetic
phase with a few seconds decay half-time. This occurred in 10ā20%
of the PSII centers. The slow kinetic phase ranged from a decay half-time
of 700 s (at 1 Ā°C) to ā¼100 s (at 20 Ā°C) in the remaining
80ā90% of the centers. The decay of the S<sub>2</sub> state
was also biphasic and showed quite similar kinetics to the decay of
the S<sub>3</sub> state. Our experiments show that the auxiliary electron
donor Y<sub>D</sub> was oxidized during the entire experiment. Thus,
the reduced form of Y<sub>D</sub> does not participate to the fast
decay of the S<sub>2</sub> and S<sub>3</sub> states we describe here.
Instead, we suggest that the decay of the S<sub>3</sub> and S<sub>2</sub> states reflects electron transfer from the acceptor side
of PSII to the donor side of PSII starting in the corresponding S
state. It is proposed that this exists in equilibrium with Y<sub>Z</sub> according to S<sub>3</sub>Y<sub>Z</sub> ā S<sub>2</sub>Y<sub>Z</sub><sup>ā¢</sup> in the case of the S<sub>3</sub> state
decay and S<sub>2</sub>Y<sub>Z</sub> ā S<sub>1</sub>Y<sub>Z</sub><sup>ā¢</sup> in the case of the S<sub>2</sub> state decay.
Two kinetic models are discussed, both developed with the assumption
that the slow decay of the S<sub>3</sub> and S<sub>2</sub> states
occurs in PSII centers where Y<sub>Z</sub> is also a fast donor to
P<sub>680</sub><sup>+</sup> working in the nanosecond time regime
and that the fast decay of the S<sub>3</sub> and S<sub>2</sub> states
occurs in centers where Y<sub>Z</sub> reduces P<sub>680</sub><sup>+</sup> with slower microsecond kinetics. Our measurements also demonstrate
that the split S<sub>3</sub> EPR signal can be used as a direct probe
to the S<sub>3</sub> state and that it can provide important information
about the redox properties of the S<sub>3</sub> state
Room-Temperature Energy-Sampling KĪ² Xāray Emission Spectroscopy of the Mn<sub>4</sub>Ca Complex of Photosynthesis Reveals Three Manganese-Centered Oxidation Steps and Suggests a Coordination Change Prior to O<sub>2</sub> Formation
In
oxygenic photosynthesis, water is oxidized and dioxygen is produced
at a Mn<sub>4</sub>Ca complex bound to the proteins of photosystem
II (PSII). Valence and coordination changes in its catalytic S-state
cycle are of great interest. In room-temperature (in situ) experiments,
time-resolved energy-sampling X-ray emission spectroscopy of the Mn
KĪ²<sub>1,3</sub> line after laser-flash excitation of PSII membrane
particles was applied to characterize the redox transitions in the
S-state cycle. The KĪ²<sub>1,3</sub> line energies suggest a
high-valence configuration of the Mn<sub>4</sub>Ca complex with MnĀ(III)<sub>3</sub>MnĀ(IV) in S<sub>0</sub>, MnĀ(III)<sub>2</sub>MnĀ(IV)<sub>2</sub> in S<sub>1</sub>, MnĀ(III)ĀMnĀ(IV)<sub>3</sub> in S<sub>2</sub>, and
MnĀ(IV)<sub>4</sub> in S<sub>3</sub> and, thus, manganese oxidation
in each of the three accessible oxidizing transitions of the water-oxidizing
complex. There are no indications of formation of a ligand radical,
thus rendering partial water oxidation before reaching the S<sub>4</sub> state unlikely. The difference spectra of both manganese KĪ²<sub>1,3</sub> emission and K-edge X-ray absorption display different
shapes for MnĀ(III) oxidation in the S<sub>2</sub> ā S<sub>3</sub> transition when compared to MnĀ(III) oxidation in the S<sub>1</sub> ā S<sub>2</sub> transition. Comparison to spectra of manganese
compounds with known structures and oxidation states and varying metal
coordination environments suggests a change in the manganese ligand
environment in the S<sub>2</sub> ā S<sub>3</sub> transition,
which could be oxidation of five-coordinated MnĀ(III) to six-coordinated
MnĀ(IV). Conceivable options for the rearrangement of (substrate) water
species and metalāligand bonding patterns at the Mn<sub>4</sub>Ca complex in the S<sub>2</sub> ā S<sub>3</sub> transition
are discussed
KĪ± Xāray Emission Spectroscopy on the Photosynthetic Oxygen-Evolving Complex Supports Manganese Oxidation and Water Binding in the S<sub>3</sub> State
The
unique manganeseācalcium catalyst in photosystem II (PSII)
is the natural paragon for efficient light-driven water oxidation
to yield O<sub>2</sub>. The oxygen-evolving complex (OEC) in the dark-stable
state (S<sub>1</sub>) comprises a Mn<sub>4</sub>CaO<sub>4</sub> core
with five metal-bound water species. Binding and modification of the
water molecules that are substrates of the water-oxidation reaction
is mechanistically crucial but controversially debated. Two recent
crystal structures of the OEC in its highest oxidation state (S<sub>3</sub>) show either a vacant Mn coordination site or a bound peroxide
species. For purified PSII at room temperature, we collected Mn KĪ±
X-ray emission spectra of the S<sub>0</sub>, S<sub>1</sub>, S<sub>2</sub>, and S<sub>3</sub> intermediates in the OEC cycle, which
were analyzed by comparison to synthetic Mn compounds, spectral simulations,
and OEC models from density functional theory. Our results contrast
both crystallographic structures. They indicate Mn oxidation in three
S-transitions and suggest additional water binding at a previously
open Mn coordination site. These findings exclude Mn reduction and
render peroxide formation in S<sub>3</sub> unlikely
Electronic Structure of Oxidized Complexes Derived from <i>cis</i>-[Ru<sup>II</sup>(bpy)<sub>2</sub>(H<sub>2</sub>O)<sub>2</sub>]<sup>2+</sup> and Its Photoisomerization Mechanism
The geometry and electronic structure of <i>cis</i>-[Ru<sup>II</sup>(bpy)<sub>2</sub>(H<sub>2</sub>O)<sub>2</sub>]<sup>2+</sup> and its higher oxidation state species up formally to Ru<sup>VI</sup> have been studied by means of UVāvis, EPR, XAS, and DFT and CASSCF/CASPT2 calculations. DFT calculations of the molecular structures of these species show that, as the oxidation state increases, the RuāO bond distance decreases, indicating increased degrees of RuāO multiple bonding. In addition, the OāRuāO valence bond angle increases as the oxidation state increases. EPR spectroscopy and quantum chemical calculations indicate that low-spin configurations are favored for all oxidation states. Thus, <i>cis</i>-[Ru<sup>IV</sup>(bpy)<sub>2</sub>(OH)<sub>2</sub>]<sup>2+</sup> (d<sup>4</sup>) has a singlet ground state and is EPR-silent at low temperatures, while <i>cis</i>-[Ru<sup>V</sup>(bpy)<sub>2</sub>(O)(OH)]<sup>2+</sup> (d<sup>3</sup>) has a doublet ground state. XAS spectroscopy of higher oxidation state species and DFT calculations further illuminate the electronic structures of these complexes, particularly with respect to the covalent character of the OāRuāO fragment. In addition, the photochemical isomerization of <i>cis</i>-[Ru<sup>II</sup>(bpy)<sub>2</sub>(H<sub>2</sub>O)<sub>2</sub>]<sup>2+</sup> to its <i>trans</i>-[Ru<sup>II</sup>(bpy)<sub>2</sub>(H<sub>2</sub>O)<sub>2</sub>]<sup>2+</sup> isomer has been fully characterized through quantum chemical calculations. The excited-state process is predicted to involve decoordination of one aqua ligand, which leads to a coordinatively unsaturated complex that undergoes structural rearrangement followed by recoordination of water to yield the <i>trans</i> isomer