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BY STEFAN WEBER
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1 Introduction
Abbreviations: BChl ulblg, bacteriochlorophyll ulblg; BPhe ulb, bacteriopheophytin ulb; Chl u,
chlorophyll u; CRPM, correlated radical pair mechanism; CW, continuous-wave; ENDOR,
electron-nuclear double resonance; EPR, electron paramagnetic resonance; ESE, electron spin
echo; ESEEM, electron spin echo envelope modulation; ESP, electron spin polarization; hf,
hyperfine; hfc, hyperfine coupling constant; HOMO, highest occupied molecular orbital; LUMO,
lowest unoccupied molecular orbital; MO, molecular orbital; RC, reaction centre; RF, radio
frequency; TRIPLE, electron-nuclear-nuclear triple resonance.
/
Light
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LH2
new millennium. As will be shown in this overview, EPR did and does
significantly contribute with its unique features: (1) Its high specificity for
reactants, intermediates or products that carry unpaired electron spins makes
it favorably suited to detect the working states in primary photosynthetic
charge separation; (2) Decisive evidence for the identity of photoproducts as
well as information on the molecular structure and relative spatial arrangement
of intermediates is obtained by EPR due to its high spectral and temporal
resolution; (3) From electron spin polarization (ESP) phenomena important
information is obtained on mechanistic aspects of the primary photosynthetic
charge separation. Many excellent review articles on various subjects relevant
to EPR in photosynthesis have been published in the last couple of year^.^^-^^
In this monograph series, the article EPR Studies of Photosynthesis by Klaus
Mobius was published back in 1994. At the beginning of the third millennium
it is now time to present an update covering selected EPR studies on bacterial
photosynthesis published in the last five to six years. In order to keep this
article and the references list reasonably short, work published before then is
only sparingly mentioned and the reader is referred to earlier reviews for a
glimpse deeper into the past. Also, where possible, preference was given to
include full research articles rather than conference proceedings because the
latter are typically hard to obtain for non-attendees of the respective meetings
and sometimes contain preliminary work that is later often revised.
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principles, the spatial structure of the system alone is not sufficient, but
additional knowledge of the electronic structure of all the pigments, including
their surrounding, in the initial and charge separated states is required.
Electronic wavefunctions - and their respective orbital energies - can, in
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the spatial andlor electronic structure of the dimer and its surrounding upon
freezing the RC so that there exist two distinct conformational states of P&
(see below).
Very different electron spin density distributions for the primary donors of
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RCs from four different species of purple photosynthetic bacteria, Rb. sphaer-
oides, Rb. capsulatus, Rhodospirillum rubrum (Rs.rubrum) and Rs. centenum,
were obtained from an analysis of proton hfcs measured in EPR and ENDOR/
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The electronic structure of the primary donor cation radical can also be
dramatically influenced by altering the amino acid environment in order to
change the hydrogen-bond situation of P'+.This has been shown in a series of
ENDOWTRIPLE studies on single and double mutants of RCs from Rb.
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2-acetyl groups of the dimer and at sites M160, and L13 1, in the vicinity of the
9-keto carbonyls of the dimer. The changes in the hydrogen bond situation of
the primary donor were accompanied by changes in the dimer oxidation
midpoint potentials. The Special TRIPLE resonance spectra showed that the
asymmetric spin density distribution in the wild type is mainly caused by the
hydrogen bond between His L168 and the acetyl oxygen of PL. Depending on
the different combinations of hydrogen bonds to PL and PM,the spin density
in Irg's5 can be shifted almost completely from PL to PM. The observed shifts
have been explained by an asymmetric dimer model, relating the spin density
ratio p ~ / to p ~the difference of the energies of the valence orbitals of the
monomers PL and PM which are affected by the hydrogen bonds and the
interaction energy between PL and PM .58
A simple relationship between the oxidation potential and the electron spin
density of the primary electron donor in RCs from Rb. sphaeroides was found
by Artz and co-workers in a study of a series of eight RC mutants with
different amino acids replacing leucine at the M 160 position.59The P865/P&
midpoint potentials, Em,were measured by electrochemical titrations and the
fraction of spin density on PL, p ~ was, calculated from the l-methyl and 5-
methyl group hfc's of PL and PM as obtained from ENDORBpecial TRIPLE
experiments. A plot of AE, (the change of the midpoint potential when going
from the wild type to the mutant, i.e. E,(wildtype) - E,(mutant)) as a
function of A ~ (theL change in spin density on PL when going from the wild
type to the mutant, i.e. pL(wi1dtype) - pl(mutant)) yields a linear relationship,
AE, = VAPL, (1)
where V is the potential required to move an electron from PL to PM.For the
M160 mutants, V = 280 f 40 mV, a value that is consistent with an approx-
imate value that can be estimated based on the RC structure. These results
demonstrate, that the midpoint potential can be fine-tuned by electrostatic
interactions with amino acids near the dimer and show that the properties of
the electronic structure of a donor or acceptor in a protein complex can be
directly related to functional properties, such as the oxidation-reduction
midpoint potential.
In contrast to the oxidized primary electron donors P& from Rb. sphaer-
oides and P& from Rps. viridis the primary donor radical cation P& from the
green sulfur bacterium Chlorobium limicola J: sp. thiosulfatophilum consisting
of two BChl a molecules shows only very small deviations from a 1:l electron
spin density distribution over the dimer as has been revealed by ENDOR and
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to the ring nitrogens by 14N ESEEM6*gives results that are in agreement with
those obtained by ENDOR measurements of large hfcs to the methyl group
protons.60
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2.2 The Electronic Structure of Pa+, Part 11: g-Tensor. - Since the breakage of
C2 symmetry in the electronic structure of the primary donor cation radical P
might represent an important functional factor in controlling the vectorial
properties of photoinduced electron transfer in bacterial RCs, such as the high
quantum yield and the unidirectionality along the L protein branch, other
independent probes for the electronic structure of P have lately found
increasing attention. Such a probe is the electronic g-tensor contained in the
leading Zeeman interaction term of the spin Hamiltonian describing an EPR
experiment. In contrast to hfc constants, which probe the electronic wavefunc-
tion locally and directly reflect the unpaired electron spin density at the
magnetic nuclei, the g-tensor reflects the more global properties of the
wavefunction, and thus, can also serve as a sensitive probe for the symmetry
characteristics of the electronic structure of P . Furthermore, the principal
+
components and the orientation of the principal axes of the g-tensor play a
crucial role in the interpretation and correct simulation of the spin-polarized
EPR spectra of the light-induced radical pairs that occur upon the primary
photosynthetic charge separation (see below). Since the g-anisotropy of F +is
on the order of only it is necessary to perform an EPR experiment at
high magnetic field in order to fully resolve the g-tensor whose spectral features
are often obscured by a Gaussian envelope dominated by unresolved hf
splittings. Here, high field means that
Table 1 Principal values of the g-tensors of P+in various organisms and the
monomeric BChl a*+
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P& relative to the crystal axes of the unit cell could be determined.63 Even the
magnetically inequivalent sites in the unit cell of the RC crystal could be
resolved. With the recent availability of EPR at yet higher magnetic fields and
mw frequencies the g-tensor of P& has been revisited by Bratt and co-
w o r k e r ~ . ~An
~ ~EPR
~ * experiment 'beyond the limits of superconducting
magnets' at 670 GHz/23.9 T has been performed on light-induced and
chemically oxidized P&. A Bitter magnet providing up to 25 T with high
magnetic field homogeneity was used in these experiments. As expected, the
spectra show excellent resolution, where the gYY and gzzprincipal components
of the g-tensor are completely resolved. The g-values reported from this study,
however, are only marginally different from the ones reported pre-
viously62-66y69and closely resemble those of monomeric BChl a*ksee Table 1.
This is evidence for the very asymmetric 5:l spin density distribution over the
dimer.44
High-field EPR (95 GHz) on RC single crystals was also used to characterize
the g-tensor of P& in the heterodimer mutant HL(M202).66In this RC the
histidine at position M202 is replaced by a leucine, resulting in a primary
electron donor in which the BChl is on the L side and the BPhe at the M side.
Since in this mutant the unpaired electron of P& is localized on the BCh1,52
the g-tensor reflects the monomer properties. The directions of the principal
axes of the g-tensor are similar for the mutant and the wild type RC.
No spectral differences have been observed between the different prepara-
tions - light induced versus chemically oxidized - of the donor cation radical.
A decrease of the g-anisotropy when going from cryogenic temperatures to
room temperature that has been reported for the primary donor P;b, of plant
photosystem 170 could not be observed in P&.67 This apparent insensitivity of
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2.3 The Primary Electron Donor Triplet State. - The state of the primary
donor most thoroughly investigated is the cation radical P t in which the
unpaired electron resides in the HOMO of P. In most primary donor cation
radicals an asymmetry of the electron spin density distribution over the two
dimer halves was found. For the forward electron-transfer reactions knowledge
of the spin density distribution of the LUMO is important, however. The
distributions of both electrons in the HOMO and the LUMO determine the
electronic properties, e.g. the charge transfer character of the excited state, *P.
Unfortunately the excited singlet state is diamagnetic and short-lived and not
accessible by EPR techniques. However, information about the orbital coeffi-
cients of the HOMO and the LUMO can be obtained from the triplet state, 3P,
which is formed by recombination of the primary radical pair P t@i in pre-
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two electrons, which results in the zero-field splitting tensor, D. Detailed data
were obtained from the determination of the zero-field splitting tensor
principal axes of 3P86S by EPR on RC single crystals of Rb. sphaeroides. The
triplet z-axis of 3P865 was found to agree within 5 degrees with the normal
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within the range 10K 5 T 5 SOK. In non-treated RCs of Rb. sphaeroides and
even more pronounced in Rps. viridis RCs, however, a temperature-depen-
dence was observed which was ascribed to the magnetic interaction between
the primary radical pair, P'+@i, and the [QiFe2+]complex, which causes a
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(DJ= 727.5MHz and IEI = 254.5MHz. The small value of /El suggests that the
BChls of P are monoligated. Several triplet states of the antenna have also
been observed which are located on BChl g molecules absorbing at longer
wavelength than the primary donor.
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oides, for example, the primary and secondary quinones, QA and QB, act as
one- and two-electron gates, respectively. QX just passes its extra electron to
QB which, in a second photo-induced electron-transfer step, becomes double
reduced, takes up protons from the environment and leaves the RC to serve as
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The axis with the smallest principal value g,= is oriented perpendicular to the
quinone plane (z-axis), the axis of the largest value gXx is along the line
connecting the two carbonyl groups (x-axis), and the axis of the third principal
value of g is perpendicular to the carbonykarbonyl axis lying in the quinone
plane (y-axis) (see e.g. 64-113), The g-tensor values for the semiquinone anion
radicals QA and QB of Zn-substituted RCs of Rb. sphaeroides in frozen
solution and single crystals have been determined some time a g 0 . ~ 7 " Re- ~
cently, Zn-substituted RCs have also been obtained from Rps. viridis in which
QA is a menaquinone-9 and Q B is a ubiquinone-9l l 4 see Table 2.
A comparison of the g-matrices of QX in frozen RC solution with that of a
menaquinone-4 anion radical in 2-propanol shows an increase of the g,,-value
of QX: this indicates a similar bonding for QA in Rb. sphaeroides and Rps.
viridis. g-tensor data for Qi- in RCs of Rps. viridis are not yet available.
Reliable calculations of the rather small shifts of the principal values of the
g-tensor of organic radicals are difficult, mainly due to the problem of
accurately accounting for the excited states that play a role in calculating the g-
tensor. Recently, Torring and co-workers have proposed new expressions for
the calculation of g-matrices from RHF MO calculations using a Rayleigh-
Schrodinger perturbation theory approach. Their expressions differ signifi-
cantly from those found previously in the literature, mostly due to the explicit
inclusion of a class of excitations where the total spin is reversed in the
excitation. Model calculations were presented for the para-benzosemiquinone
anion radical. The calculated principal values of its g-tensor showed very good
agreement with experimental data.64
All major hfc constants for the protons, carbonyl oxygens and carbons have
been determined from EPR and ENDOR experiments, see Table 3. Again, in
vitro model systems l 2 *3 as well as numerous model calculations 23- 33 on
22y1
60
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position. 13* Isolated RCs from Rb. sphaeroides that bind Zn2+ stoichiometri-
cally and in a site distinct from the non-heme high-spin Fe2+ site have been
investigated using Q-band EPR and optical absorption spectroscopy. When
Zn2+ is bound to this surface metal site, electron transfer QAQB QAQRis --+
5 Radical Pairs
5.1 The Primary Radical Pair, P t@i. - The first successful EPR observation
of the primary radical pair P"@i was reported by Proskuryakov and co-
workers.150RCs from Rb. sphaeroides and Rps. viridis have been examined
where the forward electron transfer beyond @A was blocked by quinone
depletion and photoreduction of the primary quinone acceptor, respectively. A
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new transient signal in the g = 2.0 region was found with AE polarization
(absorptive at low magnetic field, emissive at high magnetic field) and a peak-
to-peak separation of ~ 3 . 8 5mT in Rb. sphaeroides and 4 x 8 mT in Rps.
viridis. The disappearance of these new signals paralleled the formation of the
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5.2 The Secondary Radical Pair, P.+QA* . - The secondary radical pairs in
bacterial photosynthesis have been predominantly examined using time-
resolved CW EPR and ESE-detected EPR after laser flash excitation. Here,
similar to the EPR studies of the primary donor cation radical and the quinone
anion radicals, higher mw frequencies and correspondingly higher magnetic
fields are increasingly used to enhance resolution and to separate the spectral
contributions of Pt and Qfi in the radical pair P''QA EPR spectra.
5.2.I Radical Pair EPR Spectra. Time-resolved W-band (95 GHz) EPR
spectroscopy has been applied to examine the secondary radical pair state in
Zn-substituted protonated and fully deuterated RCs of Rb. sphaeroides, 57 The
ambiguity in the orientation of the g-tensor principal axes of the primary
donor P8k, with respect to its molecular axes system, that was left from single
crystal CW EPR studies at W-band,63 could be removed due to the high
spectral resolution at W-band. In a subsequent multi-frequency EPR study
including spectra taken at X-, K-, and W-band frequencies, clear differences
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to the stronger anisotropic Zeeman interaction and one may have to consider a
sequential electron-transfer model even for the case of a relatively short-lived
precursor radical pair. 165 This has been demonstrated experimentally by
Utschig and co-workers and Tang and co-workers in a comparative EPR
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ences between the spin-polarized transient EPR spectra of the samples with
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slow and fast electron transfer are observed at X-band frequency, become
more pronounced at Q-band and W-band. In contrast to studies by Till and
co-workers 155 and Hulsebosch and co-workers 5 1 a positive value for the
exchange interaction, Jpa = 0.7 mT, between Ft and Pi in the precursor
radical pair state was used for the spectral simulations, together with a dipolar
coupling of Dpa = -0.45 mT.169
The necessity to utilize a sequential electron-transfer model has also been
demonstrated by Hulsebosch and co-workers in a multi-frequency EPR study
of Zn-substituted RCs from Rb. sphaeroides where the lifetime of the primary
radical pair Pi;, @i was manipulated by replacing the native ubiquinone- 10
with duroquinone or 2-ethyl anthraquinone. 51 Relatively long lifetimes for
P8k5@i of 33 ns and 3.3 ns were obtained with 2-ethyl anthraquinone and
duroquinone as secondary electron acceptors, respectively. From spectral
simulations of the X-, Q- and D-band (130 GHz) EPR spectra information on
the magnetic interactions and dynamics of the intermediate primary radical
pair P&@i was obtained. When the lifetime of P&@x is longer than a few
nanoseconds, the influence of the magnitude and sign of the exchange interac-
tion J p on the shape of the observed EPR spectrum is significant. A value of
J p = - (0.9f 0.1) mT for both duroquinone and 2-ethyl anthraquinone-recon-
stituted RCs was obtained, which is not significantly different from that
extracted from a simulation of the EPR spectrum of the primary radical pair
P&@A in pre-reduced RCs of Rb. sphaeroides (Jpa = -(0.7 f 0.1) mT).155A
small but non-zero exchange interaction, JPQ = -(0.2 f 0.1) pT and
-(0.5 f 0.2) p T between and the radical anions of duroquinone and 2-
ethylanthraquinone, respectively, was obtained from the simulations. 5 1 Tran-
sient K-band EPR spectra of the secondary radical pair in Zn-substituted RCs
from Rb. sphaeroides with duroquinone d12 or naphthoquinone db replacing
the native ubiquinone-10 have been reported previously by van der Est and co-
worker~.'~'It was concluded from spectral simulations that substitution of QA
does not have a measurable effect on the quinone orientation in the QA-site,
although the agreement between the experimental and calculated spectra was
only mediocre and would allow for a slight quinone reorientation. However, in
their calculations no sequential electron transfer model was used, and conse-
quently the observed secondary radical pair was considered to be initially in a
pure singlet state without any admixture of triplet character from the precursor
radical pair.
Quinone-substituted non-heme iron-containing RCs from Rb. sphaeroides
have been examined by Morris and co-workers in a time-resolved X- and Q-
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band EPR study. 152 Replacing the native ubiquinone-10 with various anthra-
quinones and naphthoquinones alters both the free energy and the rate of
electron trpsfer from @A to [QFe2']. A characteristic AEA polarization
pattern was observed for Fe2+-containing RCs which has been attributed to
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the P& part of the spin-correlated radical pair Fe2+]because the EPR
signal of the polarized [aA Fe2+]radical is much too broad to be observed. The
spin-polarized EPR spectrum was described by the sequential electron-transfer
polarization model in which the chemically induced dynamic electron polariza-
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tion developed in the primary radical pair was projected onto the correlated
radical pair polarization developed in P& [a. Fe2+]. The contribution gave
rise to criticism, 171 however, mainly because the strong g-anisotropy of
[QiFe2+]was neglected and an unrealistically large value for the exchange
interaction between P& and [QXFe2'] had to be assumed ( J ~ ~ Q 2 . pT).
5 Van
den Brink and co-workers have demonstrated that an extended CRPM model
to account for the g-anisotropies of P& and [QXFe2' yields accurate
[Qx
simulations of the spin-polarized EPR signals of Pt FJ'] for both Rps.
viridis and Rb. sphaeroides, without taking recourse to a large value for
Furthermore, the orientation of the principal axes of the g-tensor of the
[QAFe2+]complex with respect to the crystal axes had been assessed. It was
concluded that the z-axis of the g-tensor is parallel to the axis between Fe2+
and N E of ~ His at M266 in Rb. sphaeroides (M264 in Rps. viridis) and the y -
axis almost parallel to the axis between Fe2+ and 0 1 of Glu at M234 in Rb.
sphaeroides (M232 in Rps. viridis). The rapid decay of the spin-polarized EPR
signal was discussed in terms of the relaxation of the quinone-iron complex
and it was shown that it probes the cross-relaxation of Q i and Fe2+.
Low-temperature spin-polarized X- and K-band transient EPR spectra of
Mn-substituted RCs of Rb. sphaeroides Y have been examined by van der Est
and c o - w o r k e r ~ . A
' ~ ~strong component with a spectral width of -0.4 mT
appears near g = 2 and a weak component with a width of ~ 5 7 0mT is
observed in the spectral range 1 5 g 5 6. The narrow spectrum is primarily
due to P& and the broad component was assigned to [QIMn2']. Both signals
are polarized as a result of the correlation of the unpaired spins on P& and
[QAMn2']. The effect of the magnetic properties of the metal on the spin
polarization and the expected differences between the spectra of P& [aA Mn2+]
and Pi165[qA Fe2'] were discussed.
presented for the secondary radical pair of Zn-substituted RCs from Rb.
sphaeroides using time-resolved EPR at X- and K-band (24G H z ) . ' Additional
~~
oscillations in the frequency ranges 1.5-2.0 MHz and 2.5-3.0MHz have also
been observed which have been attributed to the interaction between the nuclear
spins and the unpaired electron spins. This attribution was later confirmed by
Weber and co-workers in a comparative study of 14N and I5N enriched
photosystem I RCs where significant differences in the modulation patterns of
both samples were observed' 78 (see also'79). A theoretical treatment of light-
initiated nuclear modulations in the time course of transient EPR signal was
presented by Weber and co-workers180and Jeschkelsl (see also ref. 182).
Quantum beat oscillations may also be observed as a change of the Hahn
echo shape in a two-pulse electron spin echo experiment following the
photogenerating laser flash (flash - t - pulse 1 - 7 - pulse 2). This has been
demonstrated experimentally by Dzuba and co-workers who have examined
protonated Zn-substituted RCs from Rb. ~phaeroides'~~ In their experiment,
the transient echo signal shape after the laser flash and mw pulse application
was measured as a function of the delay time t . Significant changes in the shape
and intensity of the first echo appearing at T = r were observed for t < 40 ns.
In addition, a second echo signal was found when t was chosen to be strictly
identical to the delay time T between the two mw pulses. This echo signal
appears at time 27 after the second mw pulse and is ascribed to a double-
quantum coherence appearing after the first mw pulse. The existence of
multiple-quantum coherence in a spin-correlated radical pair was noted by
Tang and Norris. 184
For a two-pulse echo experiment following a laser pulse to generate a spin-
polarized radical pair, Salikhov and co-workers have predicted an unusual
out-of-phase ESE showing a deep envelope modulation (ESEEM) as a
function of the delay time between the two mw pulses.185The modulation
frequency of the echo amplitude is dominated by the spin-spin coupling
between the two halves of the radical pair. This coupling can be divided into
two parts: the anisotropic dipolar coupling D which reflects the magnetic
dipole interaction between the two involved electron spins, and the isotropic
coupling J describing the overlap of the two electronic wavefunctions. Since
the dipolar coupling D is directly related to the distance between the two
electron spins,
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it is possible to deduce the distance between the two radical pair halves from a
pulsed EPR experiment on the spin-polarized signal of the light-induced
radical pairs of photosynthesis. In weakly coupled radical pairs, D is typically
much smaller than the inhomogeneous linewidth dominated by unresolved hf
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>
I I I I I
light frozen
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A
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! I
dark frozen
Zn-bRCs
Rb. 8 p h - m R-26
Figure 5 Out-of-phase echo modulation pattern for protonated Zn-substituted RCs of Rb.
sphaeroides mutant HC(M266) frozen in the dark (lower trace) or under
illumination (upper trace) measured at X-band and at a temperature of 80 K
For details see196
6 Concluding Remarks
In conclusion it is fair to say that many questions about the structure and
function of the bacterial photosynthetic RC have been answered with the help
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methods not yet fully exploited and with the availabilty of ever new types of
modified RCs, we can be certain that these remaining challenges will finally
also be tackled. And maybe, in one of the next reviews on bacterial photo-
synthesis, answers will be given to questions that today, at the beginning of the
third millennium, no-one ever dared to ask. . . .
Acknowledgements
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