11 research outputs found
Theory of Anisotropic Circular Dichroism of Excitonically Coupled Systems: Application to the Baseplate of Green Sulfur Bacteria
A simple exciton
theory for the description of anisotropic circular
dichroism (ACD) spectra of multichromophoric systems is presented
that is expected to be of general use for the analysis of structureāfunction
relationships of molecular aggregates such as photosynthetic light-harvesting
antennae. The theory is applied to the baseplate of green sulfur bacteria.
It is demonstrated that only the combined analysis of ACD and circular
dichroism (CD) spectra for the present baseplate bacteriochlorophyll
(BChl) <i>a</i> dimer allows for an unambiguous determination
of the parameters of the exciton Hamiltonian from experimental data.
The analysis of experimental absorption and linear dichroism spectra
suggests that either the NMR structure has to be refined or in addition
to the dimers seen in the NMR structure and in the CD and ACD spectra,
BChl <i>a</i> monomers are present in the baseplate carotenosome
sample. A refined dimer structure is presented, explaining all four
optical spectra
Hole-Burning Spectroscopy on Excitonically Coupled Pigments in Proteins: Theory Meets Experiment
A theory for the calculation of resonant
and nonresonant hole-burning
(HB) spectra of pigmentāprotein complexes is presented and
applied to the water-soluble chlorophyll-binding protein (WSCP) from
cauliflower. The theory is based on a non-Markovian line shape theory
(Renger and Marcus J. Chem. Phys. 2002, 116, 9997) and includes exciton delocalization, vibrational
sidebands, and lifetime broadening. An earlier approach by Reppert
(J. Phys. Chem. Lett. 2011, 2, 2716) is found to describe nonresonant HB spectra only. Here we present
a theory that can be used for a quantitative description of HB data
for both nonresonant and resonant burning conditions. We find that
it is important to take into account the excess energy of the excitation
in the HB process. Whereas excitation of the zero-phonon transition
of the lowest exciton state, that is, resonant burning allows the
protein to access only its conformational substates in the neighborhood
of the preburn state, any higher excitation gives the protein full
access to all conformations present in the original inhomogeneous
ensemble. Application of the theory to recombinant WSCP from cauliflower,
reconstituted with chlorophyll <i>a</i> or chlorophyll <i>b</i>, gives excellent agreement with experimental data by Pieper
et al. (J. Phys. Chem. B 2011, 115, 4053) and allows us to obtain an upper bound of the lifetime of the upper
exciton state directly from the HB experiments in agreement with lifetimes
measured recently in time domain 2D experiments by Alster et al. (J. Phys. Chem. B 2014, 118, 3524)
Electrostatic Asymmetry in the Reaction Center of Photosystem II
The
exciton Hamiltonian of the chlorophyll (Chl) and pheophytin
(Pheo) pigments in the reaction center (RC) of photosystem II is computed
based on recent crystal structures by using the PoissonāBoltzmann/quantum-chemical
method. Computed site energies largely confirm a previous model inferred
from fits of optical spectra, in which Chl<sub>D1</sub> has the lowest
site energy, while that of Pheo<sub>D1</sub> is higher than that of
Pheo<sub>D2</sub>. The latter assignment has been challenged recently
under reference to mutagenesis experiments. We argue that these data
are not in contradiction to our results. We conclude that Chl<sub>D1</sub> is the primary electron donor in both isolated RCs and intact
core complexes at least at cryogenic temperatures. The main source
of asymmetry in site energies is the charge distribution in the protein.
Because many small contributions from various structural elements
have to be taken into account, it can be assumed that this asymmetry
was established in evolution by global optimization of the RC protein
Revealing the Functional States in the Active Site of BLUF Photoreceptors from Electrochromic Shift Calculations
Photoexcitation with blue light of
the flavin chromophore in BLUF
photoreceptors induces a switch into a metastable signaling state
that is characterized by a red-shifted absorption maximum. The red
shift is due to a rearrangement in the hydrogen bond pattern around
Gln63 located in the immediate proximity of the isoalloxazine ring
system of the chromophore. There is a long-lasting controversy between
two structural models, named Q63<sub>A</sub> and Q63<sub>J</sub> in
the literature, on the local conformation of the residues Gln63 and
Tyr21 in the dark state of the photoreceptor. As regards the mechanistic
details of the light-activation mechanism, rotation of Gln63 is opposed
by tautomerism in the Q63<sub>A</sub> and Q63<sub>J</sub> models,
respectively. We provide a structure-based simulation of electrochromic
shifts of the flavin chromophore in the wild type and in various site-directed
mutants. The excellent overall agreement between experimental and
computed data allows us to evaluate the two structural models. Compelling
evidence is obtained that the Q63<sub>A</sub> model is incorrect,
whereas the Q63<sub>J</sub> is fully consistent with the present computations.
Finally, we confirm independently that a ketoāenol tautomerization
of the glutamine at position 63, which was proposed as molecular mechanism
for the transition between the dark and the light-adapted state, explains
the measured 10 to 15 nm red shift in flavin absorption between these
two states of the protein. We believe that the accurateness of our
results provides evidence that the BLUF photoreceptors absorption
is fine-tuned through electrostatic interactions between the chromophore
and the protein matrix, and finally that the simplicity of our theoretical
model is advantageous as regards easy reproducibility and further
extensions
Theory of FRET āSpectroscopic Rulerā for Short Distances: Application to Polyproline
FoĢrster
resonance energy transfer (FRET) is an important
mechanism for the estimation of intermolecular distances, e.g., in
fluorescent labeled proteins. The interpretations of FRET experiments
with standard FoĢrster theory relies on the following approximations:
(i) a point-dipole approximation (PDA) for the coupling between transition
densities of the chromophores, (ii) a screening of this coupling by
the inverse optical dielectric constant of the medium, and (iii) the
assumption of fast isotropic sampling over the mutual orientations
of the chromophores. These approximations become critical, in particular,
at short intermolecular distances, where the PDA and the screening
model become invalid and the variation of interchromophore distances,
and not just orientations, has a critical influence on the excitation
energy transfer. Here, we present a quantum chemical/electrostatic/molecular
dynamics (MD) method that goes beyond all of the above approximations.
The Poisson-TrEsp method for the ab initio/electrostatic calculation
of excitonic couplings in a dielectric medium is combined with all-atom
molecular dynamics (MD) simulations to calculate FRET efficiencies.
The method is applied to analyze single-molecule experiments on a
polyproline helix of variable length labeled with Alexa dyes. Our
method provides a quantitative explanation of the overestimation of
FRET efficiencies by the standard FoĢrster theory for short
interchromophore distances for this system. A detailed analysis of
the different levels of approximation that connect the present Poisson-TrEsp/MD
method with FoĢrster theory reveals error compensation effects,
between the PDA and the neglect of correlations in interchromophore
distances and orientations on one hand and the neglect of static disorder
in orientations and interchromophore distances on the other. Whereas
the first two approximations are found to decrease the FRET efficiency,
the latter two overcompensate this decrease and are responsible for
the overestimation of the FRET efficiency by FoĢrster theory
Red/Green Color Tuning of Visual Rhodopsins: Electrostatic Theory Provides a Quantitative Explanation
We present a structure-based theory
of the long-wavelength (red/green)
color tuning in visual rhodopsins and its application to the analysis
of site-directed mutagenesis experiments. Using a combination of electrostatic
and molecular-mechanics methods, we explain the measured mutant-minus-wild-type
absorption shifts and conclude that the dominant mechanism of the
color tuning in these systems is electrostatic pigmentāprotein
coupling. An important element of our analysis is the independent
determination of protonation states of titratable residues in the
wild type and the mutant protein as well as the self-consistent reoptimization
of hydrogen atom positions, which includes the relaxation of the hydrogen
bonding network and the reorientation of water molecules. On the basis
of this analysis, we propose a ādipole-orientation ruleā
according to which both the position and the orientation of a polar
group introduced in the protein environment determine the direction
of the transition energy shift of the retinal chromophore
Photosystem II Does Not Possess a Simple Excitation Energy Funnel: Time-Resolved Fluorescence Spectroscopy Meets Theory
The experimentally
obtained time-resolved fluorescence spectra
of photosystem II (PS II) core complexes, purified from a thermophilic
cyanobacterium Thermosynechococcus vulcanus, at 5ā180 K are compared with simulations. Dynamic localization
effects of excitons are treated implicitly by introducing exciton
domains of strongly coupled pigments. Exciton relaxations within a
domain and exciton transfers between domains are treated on the basis
of Redfield theory and generalized FoĢrster theory, respectively.
The excitonic couplings between the pigments are calculated by a quantum
chemical/electrostatic method (Poisson-TrEsp). Starting with previously
published values, a refined set of site energies of the pigments is
obtained through optimization cycles of the fits of stationary optical
spectra of PS II. Satisfactorily agreement between the experimental
and simulated spectra is obtained for the absorption spectrum including
its temperature dependence and the linear dichroism spectrum of PS
II core complexes (PS II-CC). Furthermore, the refined site energies
well reproduce the temperature dependence of the time-resolved fluorescence
spectrum of PS II-CC, which is characterized by the emergence of a
695 nm fluorescence peak upon cooling down to 77 K and the decrease
of its relative intensity upon further cooling below 77 K. The blue
shift of the fluorescence band upon cooling below 77 K is explained
by the existence of two red-shifted chlorophyll pools emitting at
around 685 and 695 nm. The former pool is assigned to Chl45 or Chl43
in CP43 (Chl numbering according to the nomenclature of Loll et al. <i>Nature</i> <b>2005</b>, <i>438</i>, 1040) while
the latter is assigned to Chl29 in CP47. The 695 nm emitting chlorophyll
is suggested to attract excitations from the peripheral light-harvesting
complexes and might also be involved in photoprotection
Calculating Optical Absorption Spectra of Thin Polycrystalline Organic Films: Structural Disorder and Site-Dependent van der Waals Interaction
We propose a new approach for calculating
the change of the absorption spectrum of a molecule when moved from
the gas phase to a crystalline morphology. The so-called gas-to-crystal
shift ĪE<i><sub>m</sub></i> is mainly caused by dispersion effects and depends
sensitively on the moleculeās specific position in the nanoscopic
setting. Using an extended dipole approximation, we are able to divide
ĪE<sub><i>m</i></sub>= ā<i>QW</i><sub><i>m</i></sub> in two factors, where <i>Q</i> depends only on the
molecular species and accounts for all nonresonant electronic transitions
contributing to the dispersion while <i>W</i><sub>m</sub> is a geometry factor expressing the site dependence of the shift
in a given molecular structure. The ability of our approach to predict
absorption spectra is demonstrated using the example of polycrystalline
films of 3,4,9,10-perylenetetracarboxylic diimide (PTCDI)
Normal Mode Analysis of the Spectral Density of the FennaāMatthewsāOlson Light-Harvesting Protein: How the Protein Dissipates the Excess Energy of Excitons
We report a method for the structure-based calculation
of the spectral
density of the pigmentāprotein coupling in light-harvesting
complexes that combines normal-mode analysis with the charge density
coupling (CDC) and transition charge from electrostatic potential
(TrEsp) methods for the computation of site energies and excitonic
couplings, respectively. The method is applied to the FennaāMatthewsāOlson
(FMO) protein in order to investigate the influence of the different
parts of the spectral density as well as correlations among these
contributions on the energy transfer dynamics and on the temperature-dependent
decay of coherences. The fluctuations and correlations in excitonic
couplings as well as the correlations between coupling and site energy
fluctuations are found to be 1 order of magnitude smaller in amplitude
than the site energy fluctuations. Despite considerable amplitudes
of that part of the spectral density which contains correlations in
site energy fluctuations, the effect of these correlations on the
exciton population dynamics and dephasing of coherences is negligible.
The inhomogeneous charge distribution of the protein, which causes
variations in local pigmentāprotein coupling constants of the
normal modes, is responsible for this effect. It is seen thereby that
the same building principle that is used by nature to create an excitation
energy funnel in the FMO protein also allows for efficient dissipation
of the excitonsā excess energy
Structure Prediction of Self-Assembled Dye Aggregates from Cryogenic Transmission Electron Microscopy, Molecular Mechanics, and Theory of Optical Spectra
Cryogenic transmission electron microscopy
(cryo-TEM) studies suggest
that TTBC molecules self-assemble in aqueous solution to form single-walled
tubes with a diameter of about 35 Ć
. In order to reveal the arrangement
and mutual orientations of the individual molecules in the tube, we
combine information from crystal structure data of this dye with a
calculation of linear absorbance and linear dichroism spectra and
molecular dynamics simulations. We start with wrapping crystal planes
in different directions to obtain tubes of suitable diameter. This
set of tube models is evaluated by comparing the resulting optical
spectra with experimental data. The tubes that can explain the spectra
are investigated further by molecular dynamics simulations, including
explicit solvent molecules. From the trajectories of the most stable
tube models, the short-range ordering of the dye molecules is extracted
and the optimization of the structure is iteratively completed. The
final structural model is a tube of rings with 6-fold rotational symmetry,
where neighboring rings are rotated by 30Ā° and the transition
dipole moments of the chromophores form an angle of 74Ā° with
respect to the symmetry axis of the tube. This model is in agreement
with cryo-TEM images and can explain the optical spectra, consisting
of a sharp red-shifted J-band that is polarized parallel to to the
symmetry axis of the tube and a broad blue-shifted H-band polarized
perpendicular to this axis. The general structure of the homogeneous
spectrum of this hybrid HJ-aggregate is described by an analytical
model that explains the difference in redistribution of oscillator
strength inside the vibrational manifolds of the J- and H-bands and
the relative intensities and excitation energies of those bands. In
addition to the particular system investigated here, the present methodology
can be expected to aid the structure prediction for a wide range of
self-assembled dye aggregates