The complete characterization of a reduced biomimetic [2 Fe-2 S] cluster

Article abstract of DOI:10.1002/anie.201100727

Cores and effect: A biomimetic [2 Fe-2 S] cluster is characterized crystallographically in both the [Fe^IIIFe^III] and the mixed-valent [Fe^IIIFe^II] forms-the [2 Fe-2 S] cores show only minor geometric differences.

Full text of DOI:10.1002/anie.201100727

DOI: 10.1002/anie.201100727
Iron–Sulfur Clusters
The Complete Characterization of a Reduced Biomimetic [2Fe-2S]
Cluster**
Antonia Albers, Serhiy Demeshko, Sebastian Dechert, Eckhard Bill, Eberhard Bothe, and
Franc Meyer*
Protein-bound iron–sulfur clusters of the ferredoxin and
Rieske types, including binuclear [2Fe-2S] sites, are ubiqui-
tous biological cofactors.[1] Their dominant function is elec-
tron transfer, where the Fe/S core shuttles between the [2Fe-
2S]2+ and [2Fe-2S]1+ states.[2] Synthetic analogues for thio-
lato-coordinated [2Fe-2S] cores are well established in
bioinorganic chemistry,[3] but well-characterized [2Fe-2S]
complexes with other terminal ligands are still relatively
rare;[4,5] a model complex for Rieske-type clusters comprising
a heteroleptic set of ligands was published only recently.[6]
Most reported analogues of [2Fe-2S] sites have been
synthesized exclusively in the all-ferric state, while the
mixed-valent [2Fe-2S]1+ state could, if at all, only be accessed
by electrochemical methods.[7] Gibson and Beardwood
reported some reduced [2Fe-2S] clusters that were generated
by chemical reduction in situ and investigated in solution.[8]
Furthermore they were able to isolate and characterize one
species in the [2Fe-2S]1+ state using a bidentate bis(benzimi-
dazolato) terminal ligand; it was studied by Mçssbauer
spectroscopy, and an S = 1/2 ground state with partially
delocalized mixed valence has been proposed for the
system.[9] However, neither has a crystal structure of any
[2Fe-2S] cluster in the mixed-valent [2Fe-2S]1+ state been
published nor have magnetic measurements of such reduced
clusters been performed; such measurements could confirm
the proposals based on Mçssbauer data. Herein we report the
first crystal structure and SQUID magnetic susceptibility data
of a synthetic mixed-valent [2Fe-2S] cluster, together with its
complete spectroscopic characterization.
We decided to also use a bidentate bis(benzimidazolato)
ligand since these heterocyclic systems have proven to
sufficiently stabilize the mixed-valent form. A phenyl group
was appended at the ligand backbone to improve solubility
and crystallization (Figure 1). The homoleptic all-ferric
Figure 1. Top: Schematic view of bis(benzimidazolate) coordinated
[2Fe-2S] clusters 1 and 2. Bottom: ORTEP plot of the molecular
structure of cluster 2 (thermal ellipsoids set at 50% probability). For
clarity all hydrogen atoms and counterions are omitted.
cluster 1 was synthesized in a standard ligand-exchange
reaction by addition of an excess of the deprotonated ligand
to (NEt4)2[Fe2S2Cl4].[10]
Redox properties of 1 were studied by cyclic voltammetry
in MeCN/0.1m nBu4NPF6 at room temperature (Figure 2,
top). Two reversible one-electron reduction processes are
assigned to the formation of the mixed-valent species at E1/2
=
À1.14 V and the all-ferrous species at E1/2 = À2.10 V vs. the
Fc/Fc+ couple (Fc = [(C5H5)2Fe]). The potentials are shifted
to more positive values compared to related thiolato-coordi-
nated complexes and are relatively high for synthetic [2Fe-
2S] clusters, a result of the electron withdrawing character of
the bis(benzimidazolato) capping ligands. Electrochemical
potentials of cysteine-coordinated [2Fe-2S] ferredoxines
usually lie in the range À1.05 V to À0.75 V versus the Fc/
Fc+ couple.[11] The large separation between the two half-
wave potentials revealed significant stabilization of the
mixed-valent species 2 (Kc = 1.7 ꢀ 1016), a fact that allowed
the chemical reduction of 1 (using decamethylcobaltocene)
and isolation of 2, which proved to be stable in the solid state
under nitrogen even at room temperature for several hours.
The UV/Vis spectrum (Figure 2, bottom) of 1 shows
two prominent bands at 411 nm (e = 7340mÀ1 cmÀ1) and
[*] A. Albers, Dr. S. Demeshko, Dr. S. Dechert, Prof. Dr. F. Meyer
Institut fꢀr Anorganische Chemie
Georg-August Universitꢁt Gçttingen
Tammannstrasse 4, 37077 Gçttingen (Germany)
E-mail: franc.meyer@chemie.uni-goettingen.de
Homepage: http://www.meyer.chemie.uni-goettingen.de
Dr. E. Bill, Dr. E. Bothe
Max-Planck-Institut fꢀr Bioanorganische Chemie
Stiftstrasse 34–36, 45470 Mꢀlheim an der Ruhr (Germany)
[**] Financial support by the DFG (International Research Training
Group GRK 1422 “Metal Sites in Biomolecules: Structures,
Regulation and Mechanisms”; see www.biometals.eu) and the
Cusanuswerk (PhD fellowship for A.A.) is gratefully acknowledged.
Supporting information for this article is available on the WWW
under http://dx.doi.org/10.1002/anie.201100727.
528 nm (e = 7020mÀ1 cmÀ1) and
a
minor band at
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Table 1: Selected interatomic distances [ꢂ] and angles [8] for 1 and 2.
d(Fe···Fe)
d(Fe–N)
d(Fe–S)
](N-Fe-N)
](S-Fe-S)
1
2
2.70
2.69
1.89/1.99
2.04/2.05
2.19/2.21
2.22/2.23
92.84
87.73
104.27
105.80
distinguishable, a result of partial delocalization of the
unpaired electron. The [2Fe-2S] rhombus remains almost
unchanged upon reduction: the Fe···Fe distances of both
clusters are similar (d(1) = 2.70 ꢁ vs. d(2) = 2.69 ꢁ) and the
bond lengths and angles between the iron and the sulfur
atoms differ only by 0.02 ꢁ and 1.58, respectively. In 2 the
bonds between iron and nitrogen atoms are elongated by d =
0.06 ꢁ, and therefore the N-Fe-N angles in 2 are smaller by
5.18. An overlay of both structures is in the Supporting
Information (Figure S14)
Magnetic susceptibility measurements (SQUID; Figure 3)
reveal strong antiferromagnetic coupling of the FeIII ions and
an S = 0 ground state for 1 (J = À179 cmÀ1 in a À2 JS1·S2
Figure 2. Top: Cyclic voltammogram of 1 in MeCN (c=1.0·10À3 m) at a
scan rate of 100 mVsÀ1. Bottom: Potentials are given in volts vs. the
Fc/Fc+ couple. Electronic absorption spectrum of 1 (c) and 2 (a)
recorded in DMF solution at room temperature. Inset: deconvolution
of the low-energy bands.
484 nm (e = 6100mÀ1 cmÀ1). In the course of reduction the
overall intensity in the visible region drops significantly. In the
spectrum of 2 the band at 531 nm (e = 2150mÀ1 cmÀ1) remains,
a shoulder at 583 nm (e = 1220mÀ1 cmÀ1) and two shoulders at
384 nm and 341 nm (e = 4000 and 6500mÀ1 cmÀ1) appear.
*
*
Figure 3. Temperature dependence of meff for 1 ( ) and 2 ( ) at a field
of B=0.5 T. The solid lines represent spin-Hamiltonian simulations.
model);[12] such behavior is typical for the [2Fe-2S]2+ core.
For the mixed-valent cluster 2 the magnetic moment meff was
also found to decrease upon lowering the temperature from
295 to 75 K owing to antiferromagnetic coupling, but below
75 K it remains constant at 1.82 mB in accordance with an S =
1/2 ground state. Also this behavior can be simulated with a
Heisenberg spin-coupling model by adopting S1 = 5/2 and S2 =
2 for the FeIII and the FeII ions in the mixed-valent [2Fe-2S]1+
core, and an effective coupling constant, Jeff, which comprises
the exchange interaction as well as the competing effects of
intrinsic electron transfer (double exchange)[13–15] and charge
localization[16] arising from the static and vibronic coupling to
the environment.[8,17] The effective coupling constant[18] is
determined to be Jeff = À134 cmÀ1, which is well within the
range found for Rieske and Rieske-type proteins (À65 cmÀ1
to À270 cmÀ1 with a median around À150 cmÀ1).[19,20]
Furthermore,
a
broad band at about 842 nm (e =
240mÀ1 cmÀ1) develops (Figure 2, inset). After exposing a
solution of 2 to oxygen the absorption spectrum appears to
revert almost to the spectrum of 1 (Supporting information,
Figure S3) with three isosbestic points at 359 nm, approx-
imately 730 nm and approximately 1200 nm. Differences to
the spectrum of cluster 1 can be explained by an absorption
band of the [Cp*2Co]+ ion at 339 nm (Cp* = C5Me5).
Crystals of 1 and 2 were obtained by slow diffusion of
diethyl ether into DMF solutions of the products, allowing the
molecular structures of biomimetic [2Fe-2S] complexes in
both relevant oxidation states to be compared by X-ray
crystallography for the first time.
Inspection of the core structures of all-ferric 1 (Supporting
information, Figure S12) and mixed-valent 2 (Figure 1) shows
only minor changes in geometric parameters. Relevant
distances and angles are collected in Table 1. Both com-
Unfortunately, we cannot probe directly the strength of
double exchange in 2, because no intervalence band can be
detected in the investigated range of the UV/Vis/NIR
spectrum (200–3000 nm). However, substantial charge deloc-
alization is clear from the Mçssbauer and EPR spectra of 2.
¯
pounds crystallize in the triclinic space group P1 with
crystallographically imposed inversion symmetry. Interest-
ingly the two iron atoms of the mixed-valent species 2 are not
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The EPR spectrum in frozen solution (Supporting informa-
tion, Figure S11) shows pronounced rhombic splitting with
g = (2.016, 1.935, 1.885), which is similar to those of the
Rieske-type proteins[21–23] and the related model complex.[6]
This result is in line with expectation as the g anisotropy is
mainly determined by the properties of the FeII sites of the
mixed-valent dimers,[22,23] which all have comparable {S2N2}-
coordination. However, the average g value of 2 (gav = 1.96) is
significantly closer to the free-electron value (g = 2.0023) than
those of the Rieske centers and the model compound (gav =
1.91 and 1.92, respectively). Mouesca and Orio have pointed
out that this behavior indicates significant partial valence
delocalization.[23]
delocalization is particularly clear for the FeIII subspectrum,
the isomer shift of which (dI = 0.47 mmsÀ1) clearly exceeds
that of the corresponding {FeIII}2 compound 1 (d = 0.27 mmsÀ1
at 4.2 K). The empirical correlation[24] d(x) = [1.43–
0.40x] mmsÀ1, found for d and the oxidation number (x) of
{FeS4} units, would predict a difference of 0.4 mmsÀ1 for fully
localized FeIII and FeII sites (I) and (II), whereas for 2 we find
only half as much (0.2 mmsÀ1).
The actual mixing of the electronic configurations [Fe2+-
Fe3+] (“A”) and [Fe3+-Fe2+] (“B”) was determined from a
comparison of the isomer shifts and magnetic hyperfine data
with those of the Rieske cluster and of the closely related
trianion [Fe2S2(DMBB)2]3À (A) (DMBB = dimethylmethane-
bisbenzimidazolato).[21,25] Since A and 2 show almost identical
Mçssbauer parameters,[9,12] we also adopt the same 20%
valence mixing for the partially delocalized states “A” and
“B” of 2 (coefficients a2 = 0.8, b2 = 0.2).[9] However, in
contrast to this similarity, the splitting of the spin doublet
ground state and the quartet excited state found for 2 deviates
considerably from that reported for A (DS = 402 cmÀ1 vs.
105 cmÀ1). We tend to assign the deviation to low accuracy of
the measurement of A (an intricate analysis of paramagnetic
relaxation rates).[9]
The zero-field Mçssbauer spectrum recorded at 4.2 K
(Figure 4, bottom) shows a superposition of two distinct
quadrupole doublets (I and II), as expected for a mixed-valent
dimer with fast spin relaxation in the solid state (collapsed
paramagnetic hyperfine splitting). The parameters, however,
dI = 0.47 mmsÀ1,
DEQI = 1.41 mmsÀ1,
dII = 0.69 mmsÀ1,
DEQII = 2.90 mmsÀ1, deviate from those expected for
valence-trapped FeIII and FeII ions in quasi tetrahedral
{S2N2}-coordination and indicate appreciable mixing of FeII
and FeIII characters for the individual sites. The partial
The magnetic and spectroscopic properties of 2 can be
rationalized by using
a phenomenological model that
describes the energies of the spin states of a mixed-valent
iron dimer in terms of the exchange coupling constant J, a
double exchange parameter B accounting for delocalization,
and an effective energy difference DAB of the configurations
“A” and “B” that summarizes the charge-localizing interac-
tions due to static site differences as well as vibronic coupling.
The corresponding double-exchange Hamiltonian[9,12,13,15,26]
cannot be solved with experimental data for only two
variables,[9] Jeff and a2. However, if in addition we adopt B =
700 cmÀ1 as determined by DFT calculations,[23] we can fit
parameters and obtain J = À341 cmÀ1, and DAB = 1050 cmÀ1.
The exchange coupling constant is in good agreement with J =
À360 cmÀ1 estimated from an analysis of the covalency in
[2Fe-2S]1+ clusters using ligand K edge X-ray absorption
spectroscopy.[27] Moreover, this set of parameters is consistent
with Mouesca and Orio’s combined DFT and EPR analysis
for [2Fe-2S]1+ clusters.[23] Our results predict an intervalence
band at 1750 cmÀ1 (5714 nm).[28] Apparently such transitions
are difficult to detect, and we didn’t find it for 2, but the result
rules out previous tentative assignments of intervalence bands
around 540 nm;[29] such large double-exchange splitting of
total spin states would not be consistent with the S = 1/2
ground state of [2Fe-2S]1+ clusters.
In summary, for the first time we have isolated, crystal-
lized, and thoroughly characterized a synthetic ferredoxin-
type [2Fe-2S] cluster in both relevant oxidation states,
namely the [2Fe-2S]2+ and mixed-valent [2Fe-2S]1+ forms.
Magnetic measurements confirm antiferromagnetic coupling
of the FeII and the FeIII ion in the mixed-valent complex
resulting in an S = 1/2 ground state with Jeff = À134 cmÀ1. This
value provides some solid experimental basis for predicting
the position of the intervalence band in the IR region. The
unpaired electron in the [2Fe-2S]1+ species is partially
delocalized over the cluster core, and the two iron ions are
Figure 4. Zero-field Mçssbauer spectra of 1 recorded at 80 K (top) and
of 2 recorded at 4.2 K (bottom). The solid lines are fits with Lorentzian
doublets to the experimental values using the following isomer shifts
and quadrupole splittings: d=0.24 mmsÀ1, DEQ =0.87 mmsÀ1 for 1,
and d=0.47 mmsÀ1, DEQ =1.41 mmsÀ1 for the “FeIII” contribution
and d=0.69 mmsÀ1, DEQ =2.90 mmsÀ1 for the “FeII” contributions of
2, respectively.
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Redox potentials of synthetic [2Fe-2S] clusters generally are
much lower than those of their biological counterparts.[3]
[12] For further details see Supporting Information.
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not distinguishable by X-ray crystallography. The [2Fe-2S]
core structure undergoes only minor geometric changes upon
reduction, which contributes to the high stability of the
mixed-valent species 2 and reflects the low reorganization
energies that make these [2Fe-2S] clusters preferred elec-
tron-transfer sites in biology. Future work will address
whether reduction of the [2Fe-2S] core can be coupled to
protonation of the backside N atoms of the benzimidazolates,
similar to what has been proposed for the imidazole ligands of
the natural Rieske cluster.[30]
Received: January 28, 2011
Revised: May 24, 2011
Published online: August 25, 2011
Keywords: bioinorganic chemistry · iron ·
.
mixed-valent compounds · structure elucidation · sulfur
[18] Jeff is defined as one third of the energy splitting DS between S =
1/2 and S = 3/2 states, which is 402 cmÀ1 for 2.
[19] Values converted to our notation H = À2 Jeff S1 S2.
[20] It should be noted that imidazole ligands are protonated and
neutral in reduced natural Rieske clusters, in contrast to the
anionic benzimidazolates used herein.[30]
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nane) cluster,[32] we obtain J = À419 cmÀ1
,
and DAB =
1448 cmÀ1, and Div = 2413 cmÀ1, or liv = 4144 nm. These values
may be considered for a conservative error estimate.
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