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Photosynthesis
(4)
Molecular Dynamics and Structure
Correlations in Photoinduced Electron
Transfer
The long-term objective of this project is to reveal the factors that
govern solar energy conversion and storage at molecular levels. A better
understanding of these factors will help to design molecular systems mimicking
the high efficiency of solar energy conversion in natural photosynthesis.
The fundamental reactions in solar energy conversion and storage are photoinduced
electron transfer (ET) and charge separation between or within molecules.
Such photoinduced electron movement at molecular levels will cause nuclear
movements in order to adopt the electron density redistribution in molecules,
leading to molecular structural changes, or reorganization. According
to modern electron transfer theory, the capability of molecules to arrange
themselves as a result of photoinduced electron movement is one of the
most important factors in determining the rate of the reaction, thus efficiencies
of solar energy conversion. Therefore, the project will focus on capturing
molecular structures for photoinduced charge separate species to identify
particular nuclear responses to the electron movement and their correlation
to the kinetics of the electron transfer reactions. Once we understand
the mechanism for a particular nuclear movement that assists the charge
separation, we can rationally design and identify molecular systems with
high efficiencies for solar energy conversion as well as other potential
applications.
Recent
Research
Structure-function Relationships in Bacterial
Photosynthetic Reaction Center Proteins Probed by
Metal Binding Sites.
The nonheme Fe2+ site, chelated with four histidines and one
glutamic acid of the RC protein, is situated in the middle of a putative
path from QA to QB. Thus, the Fe2+ binding
site is likely to be sensitive to structural changes in the protein matrix
and used as a probe for structural changes near the quinones in the ET
process. We carried out a series of X-ray absorption fine structure (XAFS)
measurements to obtain accurate local structures around the Fe(II) with
a resolution about one order of magnitude better than from X-ray diffraction
of the RC protein. Differences in the average nearest neighbor distances
from the metal were observed by XAFS studies. Meanwhile, the ET rates
from the QA to QB were measured by Tiede and Utschig,
showing a variation of the rate constants among various RC proteins, which
prompted us to seek correlations between the structures of the Fe(II)
site with the ET rate constants.
XAFS spectra at the Fe K-edge were measured for the Fe-binding site in
RCs from different species, Rhodobacter sphaeroides R-26, Rhodobacter
sphaeroides PUC 705BA, and Rhodobacter capsulatus. The nearest
neighbor distances for Fe(II) sites of all three species are similar,
but Rb. capsulatus RC shows significantly more diversity in the
distances than the other two. The results indicate that minor structural
differences at the Fe(II) sites between species are possible, even the
amino acids directly bound to Fe(II) are conserved.
XAFS spectra were also taken for RCs at different preparative conditions.
Isolated RC of Rb. sphaeroides PUC has a 0.05Å longer average nearest
neighbor distance at the Fe(II) site than the RC before some accessory
proteins were removed. These structural changes are correlated to earlier
findings by Tiede et al. for rates of ET from QA to QB
in RCs under various preparative conditions, where the fastest rate was
found for the RC in native chromatophores and the slowest in isolated proteins. The elongation of
the nearest neighbor distance for Fe(II) in the isolated RC and the decrease
of the ET rate are direct evidence that the ET dynamics has been slowed
down when the protein matrix becomes loose during prolonged purification.
In order to characterize the role of the Fe(II) in the RC, other divalent
metals were chelated at the same site. The XAFS results show that variations
on the average nearest neighbor distances for Zn(II), Fe(II), and Mn(II)
sites in RCs follow that for ionic radii of the metals. The results imply
that the local protein matrix is capable of adapting metals of different
sizes. Meanwhile, kinetic results for ET from QA to QB
among these metal-substituted RCs show that a slower rate constant is
associated with a larger average nearest neighbor distance, thus a larger
metal ion. XAFS spectra of the Mn(II) site in substituted RCs at 290 K and 25 K showed no significant
changes with temperature.
The results from our XAFS study suggest that metal ion binding site structures
in RCs are sensitive to the protein local environment and are correlated
to the kinetics of electron transfer reactions in that region. We have
found a clear correlation between the structure and the kinetics of ET
from QA to QB.
Transient Molecular Structure Determination
in Photoinduced Electron Transfer Reactions. During past
years, we have developed a laser-pump, X-ray-probe, time-domain XAFS facility
at BESSRC-CAT, Advanced Photon Source (APS) at Argonne. The goal of our
ongoing research is to capture transient molecular structures involved
in photoinduced electron and energy transfer, which are important for
solar energy conversion and storage. Knowing the nuclear coordinates of
reaction intermediates is important for a fundamental understanding of
reaction mechanisms and molecular reactivities, and serves as references
for theoretical calculation.
We have conducted two preliminary laser-pump, X-ray-probe, time-domain
XAFS experiments at our new facility during the special operating mode
that provided a timing sequence of X-ray pulses to allow gating the X-ray
absorption signal solely from the laser-excited molecules. A transient
molecular intermediate is created by a laser pulse and monitored by an
X-ray pulse(s) at an instant when its population is optimal. Therefore,
structural information on the intermediate can be obtained. A multielement
X-ray detector is gated for the X-ray pulse(s) that overlaps with the
laser pulse in time and space. One of the key obstacles of the experiment
is incompatibility between the repetition rates of the laser and the X-ray.
In order to convert a high fraction of the molecules to the transient
state, reasonably high pulse energy of the laser is required that limits
the repetition rate of the laser to a few KHz, whereas the repetition
rate of X-ray pulses are on an order of 10 MHz. This implies that less
than 1/1000 of the total X-ray photons can be used to detect transient
molecular structure. Therefore, it is possible to conduct such an experiment
only with the latest third-generation synchrotron sources.
We have successfully obtained initial XANES at Ni K-edge for 2mM nickel
tetraphenyl porphyrin (NiTPP) with two axial ligands, using a sextet X-ray
pulse cluster at 1 KHz. This gives a 14.2 ns time resolution for capturing
transient molecular species. The preliminary XANES spectra proved the
feasibility of the experiment, and we observed XANES spectra for photodissociated
NiTPP with a 20 ns lifetime. We believe that the results can be further
improved when the beamline is completely optimized. We have planned studies
for detecting charge-separated transient species in the future.
Future
Research
We will continue seeking direct correlations between the metal-site structures
and the kinetics of ET from QA to QB, using steady-state
XAFS and optical transient absorption. In addition to complete publication
of previous work, we will investigate the metal-site structures of RC
proteins with mutations in the region (with Hanson and Laible), as well
as the second metal ion binding site in the RC. The results of the structures
for the metal sites will be correlated with the ET rate constants for
the quinones. Moreover, the structural changes around the metal site for
the P+QAQB- charge separation
states induced by photoillumination will be measured by XAFS. This study
will further our understanding of the correlations between the structures
and functions in the RC proteins as well as ET in general.
Structural change in the RC proteins induced by ET may occur at different
structural levels. XAFS measurements probe local structures of the metal
binding site, but not global structural changes of the protein, such as
the volume change due to secondary or tertiary rearrangements. It is important
to know whether such global structural changes occur, because these changes
are factors that interfere with ET in the RC. The optical transient grating
technique is sensitive in detecting the index of refraction changes due
to the volume change of the proteins induced by light, which was applied
to myoglobins and hemoglobins. However, no experiment has been done on
the RC proteins even though there was evidence that the volume of the
protein may be altered by ET. The results of this experiment can be compared
to X-ray and neutron scattering studies by Tiede et al. where global structural
change of proteins is investigated.
Using laser-pump, X-ray-probe, time-resolved XAFS, we will measure molecular
structural changes due to ET in model systems as well as in two electron
donor-acceptor complexes. The first system is a bis-porphyrin complex
with a free base porphyrin as the electron donor and an iron(III) porphyrin
as the electron acceptor. Our earlier study with a similar system with
Zn(II) porphyrin as the donor in a glass at 70 K indicated that ET in
such a system may be a gated process, where the axial ligation of Fe was
weakened or broken as Fe(III) was reduced to Fe(II). It was an important
result in understanding influences of molecular structures to the ET reaction.
However, the time resolution and detection sensitivity were not sufficient
for getting Fe-to-ligand bond distances. Thus, we designed a new complex
having the same electron acceptor Fe(III) porphyrin with an axial ligand.
Using the new XAFS facility, we will investigate whether this axial ligation
changes once an electron is temporarily transferred to Fe(III). The second
molecular system is a Cu(I)(dmp)2 complex that functions as
either the photosensitizer in energy transfer or the electron acceptor
in ET processes. The metal-to-ligand-charge-transfer (MLCT) transitions
were involved in its functions, which move the electron density from Cu(I)
to the ligands, creating transient Cu(II)-like species. However, the exact
transient structure of Cu(I) complexes in numerous energy and electron
transfer processes has not been well-characterized. It is known that Cu(I)
and Cu(II) adopt different coordination geometries, which can be easily
observed using XAFS as we did in our unpublished work on electrochemically
induced structural changes of Cu(I/II) complexes in redox reactions. Collaborating
with Meyer, we will measure the structural changes in various photochemical
processes for Cu(I) complexes at the time-resolved XAFS facility of APS.
Other model systems include studies of charge separation kinetics in
dye-sensitized TiO2 nanoparticles in collaboration with Rajh
who will develop chemical methods in connecting molecular wire (e.g.,
oligomers of phenylenevinylene) or chromophores (e.g., porphyrins) to
the surfaces of the nanoparticles. Photoinduced electron transfer and
charge separation in such systems will be investigated.
Contact:
L. X. Chen
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