A biomimetic model for the active site of iron-only hydrogenases covalently bonded to a porphyrin photosensitizer

Article abstract of DOI:10.1002/anie.200503602

(Chemical Equation Presented) Efficient communication: The first porphyrin-photosensitizer-containing biomimetic model for the active site of Fe-only hydrogenases has been synthesized and structurally characterized (see picture). Its fluorescence spectrum

Full text of DOI:10.1002/anie.200503602

Communications
Enzyme Models
DOI: 10.1002/anie.200503602
A Biomimetic Model for the Active Site of
Iron-Only Hydrogenases Covalently Bonded
to a Porphyrin Photosensitizer**
Li-Cheng Song,* Ming-Yi Tang, Fu-Hai Su, and
Qing-Mei Hu
Hydrogenases are highly efficient enzymes that catalyze the
production and consumption of hydrogen reversibly in a wide
variety of microorganisms.[1–3] Hydrogenases are generally
classified into two major groups depending on their metal
content, namely NiFe hydrogenases and Fe-only hydroge-
nases.[4] Although both groups of hydrogenases catalyze the
consumption and production of hydrogen, the Fe-only hydro-
genases have much greater reaction rates for H2 production
than NiFe hydrogenases.[5] Therefore, Fe-only hydrogenases
(hereafter referred to as FeHases) have received much more
attention than NiFe hydrogenases in biomimetic studies
[*] Prof. L.-C. Song, Dr. M.-Y. Tang, Dr. F.-H. Su, Prof. Q.-M. Hu
Department of Chemistry and
The State Key Laboratory of Elemento-Organic Chemistry
Nankai University
Tianjin 300071 (China)
Fax: (+86)22-2350-4853
E-mail: lcsong@nankai.edu.cn
[**] The authors are grateful to the NSF of China for financial support of
this work.
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aimed at synthesizing model compounds that can act as H2
production catalysts that are as effective as those found in the
natural systems.[6,7]
Recent X-ray crystallographic[8] and IR spectroscopic[9]
studies have indicated that the active site of FeHases, the H-
cluster, consists of two iron atoms that are within bonding
distance of each other and bridged by a dithiolate ligand.
These studies also indicated that there are three other ligands,
namely CO, CNÀ, and a cysteine-S-linked cubic 4Fe4S cluster,
coordinated to the two dithiolate-bridged iron atoms; the
cubic 4Fe4S cluster is actually the part of the electron transfer
chain that links the active site of FeHases. Numerous model
compounds have been successfully synthesized and structur-
ally characterized based on the above-mentioned structural
studies regarding the active site.[10]
We recently initiated a study on the possibility of linking a
porphyrin-type photosensitizer to this simple biomimetic
model in order to prepare a new type of light-driven model
compounds. Fortunately, we were able to synthesize one such
model compound, namely 3 (see Scheme 1), in which a
photosensitizing tetraphenylporphyrin group (TPP) is cova-
lently linked to the Natom of the diiron azadithiolate (ADT)
moiety [{(m-SCH2)2N}Fe2(CO)6]. It follows that our light-
driven model compound 3 is different from the previously
reported cationic model in which a RuII complex [Ru-
(terpy)2]2+ is the photosensitizer (terpy = terpyridyl).[11] We
chose TPP as the photosensitizer because: 1) TPP can absorb
as much as 46% of the energy of sunlight;[12] 2) the lifetime of
the excited state of TPP is much longer than those of common
RuII-based photosensitizers;[12] 3) [Ru(terpy)2]2+ is cationic,
while TPP is neutral; and 4) as a result of the above three
points, the expected photoinduced electron transfer in 3
should be easier than in the previously reported cationic
model. The ADT-bridged diiron moiety was selected to
constitute this model, because it has recently been suggested
that the ADT bridge plays an important role in H2 production
in the natural system.[13] In fact, diiron–ADT complexes have
proved to be some of the best simple models for the active site
of FeHases.[10c,f]
Scheme 1. a) (CH2O)n, CH2Cl2, room temperature, 5 h; b) SOCl2, room
temperature, 1 h; c) [(m-HS)2Fe2(CO)6], THF, room temperature, 12 h;
d) PhCHO, pyrrole, CF3CO2H, CH2Cl2, room temperature, 15 h; e) p-
chloranil, reflux, 1 h.
rings in the porphyrin unit,[17] and strong absorption bands at
2073, 2033, and 1996 cmÀ1 due to the terminal CO groups in
the diiron–ADT moiety. The 1H NMR spectrum of 3 displays
a singlet at d = 4.55 ppm for the CH2 groups in the diiron–
ADT moiety and another singlet at d = À2.76 ppm for the NH
groups of the porphyrin unit.[18] The electronic absorption
spectra of 3 and TPP were also recorded. As shown in
Figure 1, there is one Soret band at 419 nm in the near-UV
The synthetic route to 3 and its expected light-driven
process are briefly illustrated in Scheme 1. First, N,N-
di(chloromethyl)-4-formylaniline (1) is prepared by treat-
ment of p-aminobenzaldehyde with paraformaldehyde and
then with SOCl2.[14] Second, compound 1 was treated with di-
m-sulfanylbis(tricarbonyliron)[15] to afford the simple p-ben-
zaldehyde-substituted model 2. Finally, the target model 3 was
synthesized by treatment of 2 with pyrrole and benzaldehyde
in a 1:4:3 molar ratio followed by the oxidant p-chloranil.[16] In
the expected light-driven process, model 3 should first absorb
a photon at the photosensitizer TPP. This photoexcited TPP is
then oxidatively quenched by the diiron unit to give a reduced
iron species. After regeneration of the TPP by transfer of an
electron from an external donor, this process is repeated to
produce a doubly reduced diiron species that should be able
to drive the reduction of protons to hydrogen (Scheme 1).
The new compounds 1–3 were characterized by elemental
analysis and various spectroscopic techniques. The IR spec-
trum of 3 shows three absorption bands at 1558, 1472, and
1350 cmÀ1, assigned to the skeletal vibrations of the pyrrole
Figure 1. UV/Vis spectra of 3 and TPP in CH2Cl2 (3”10À6 m). The Soret
band absorptions have been normalized and the spectra amplified 10-
fold in the Q band region.
region and four Q bands at 516, 552, 592, and 647 nm in the
visible region.[19] These Soret and Q bands are red-shifted by
only 1–3 nm relative to the corresponding bands of TPP under
the same conditions.
The fluorescence emission spectrum of 3, along with those
of TPP and an equimolar mixture of TPP and [{(m-
SCH2)2NH}Fe2(CO)6], were also recorded. As shown in
Figure 2, the two fluorescence emission bands at 655 and
719 nm displayed by 3 are red-shifted by about 3 nm relative
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Communications
Figure 2. Fluorescence emission spectra (lex =425 nm) of 3, TPP, and
an equimolar mixture of TPP and [{(m-SCH2)2NH}Fe2(CO)6] in CH2Cl2
(3”10À5 m).
Figure 3. Structure of 3. Selected bond lengths [Š]: Fe1–Fe2 2.5000(9),
Fe1–S1 2.2630(13), Fe1–S2 2.2607(15), N1–C7 1.428(6), N1–C8
1.413(6), C12–C15 1.503(6), C16–N2 1.367(5), C27–N3 1.375(5), C38–
N4 1.373(5), C49–N5 1.370(6).
to the corresponding bands of TPP under the same conditions,
although their intensities are strongly quenched relative to
those of the TPP bands, with a quenching efficiency, Q, of
86.4%. Since the intensities of the two bands of the equimolar
mixture of TPP and [{(m-SCH2)2NH}Fe2(CO)6] are almost the
same as those of the corresponding TPP bands, we believe
that the remarkably decreased intensities of the two fluores-
cence bands of 3 relative to those of TPP are most likely due
to strong intramolecular electron transfer from the photo-
excited state of the porphyrin macrocycle of TPP to the
covalently bonded diiron–ADT moiety and not by an
intermolecular collision process between molecules of 3.[20]
It is interesting to note that such an intramolecular electron
transfer is one of the important steps required for the proton
reduction performed by biomimetic models.
The molecular structures of model 3 and its precursor 2
were confirmed by X-ray crystallography (Figures 3 and 4,
respectively).[21] Both 2 and 3 contain a diiron–ADT moiety in
which the six-membered ring Fe1-S1-C7-N1-C8-S2 has a boat
conformation and the other six-membered ring Fe2-S1-C7-
N1-C8-S2 adopts a chair conformation. The bond between the
disubstituted benzene ring and the N1 atom is axially oriented
in both 2 and 3, and all the iron nuclei in 2 and 3 have the
Figure 4. Structure of 2. Selected bond lengths [Š]: Fe1–Fe2 2.4956(9),
Fe1–S1 2.2542(12), Fe1–S2 2.2417(11), Fe2–S1 2.2486(11), N1–C7
1.424(4), N1–C8 1.431(4), N1–C9 1.387(4), O7–C15 1.193(4).
À
expected square-pyramidal coordination sphere. The Fe Fe
between the phenyl hydrogen atoms proximal to the porphy-
rin unit and the pyrrole rings. The twist angles between the
porphyrin plane and the benzene rings involving C12, C21,
C32, and C43 are 75.98, 99.18, 77.48, and 63.18, respectively.
In conclusion, we have synthesized and crystallographi-
cally characterized a novel light-driven-type model com-
pound (3) that contains a TPP photosensitizer covalently
bonded to the Natom of a diiron–ADT moiety. In view of the
strong coordination ability of porphyrin macrocycles with a
wide variety of metal ions[12] and the facile substitution of the
Fe-bound CO by other ligands,[23] we expect that we will be
able to further modify 3 in order to facilitate the electron
transfer from the photoexcited TPP to the diiron–ADT
moiety and thus finally accomplish the light-driven reduction
of protons to hydrogen. Further investigations in this area are
in progress.
bond lengths of 2.4956(9) Š for 2 and 2.5000(9) Š for 3 are in
good agreement with the corresponding lengths in similar
complexes.[10] The sum of the C-N-C angles around N1 is
356.88 for 2 and 355.38 for 3, which implies somewhat
interrupted p conjugation between the disubstituted benzene
ring and the p orbital of the nitrogen atom.
While 2 is a simple model compound where the nitrogen
atom is linked to an aromatic aldehyde system, the target
compound 3 is a novel light-driven-type model with a
porphyrin photosensitizer. The C Nbond lengths in the
pyrrole rings of the porphyrin unit of 3 are nearly the same
À
(1.364(5)–1.378(5) Š) and lie between those of normal single
and double C Nbonds. [22] The four benzene rings attached to
À
the porphyrin unit of 3 are planar and twisted relative to the
porphyrin plane in order to reduce the steric interactions
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6.37; H NMR (300 MHz, CDCl3): d = 5.54 (s, 4H; 2CH2), 7.31, 7.91
(2d, J = 8.7 Hz, 4H; C6H4), 9.94 ppm (s, 1H; CHO); IR (KBr disk):
n˜ = 1694 cmÀ1 (CHO).
2: A solution of Li(Et3BH) in THF (1m, 17.0 mL, 17.0 mmol) was
added to a solution of [(m-S2)Fe2(CO)6] (2.924 g, 8.5 mmol) in THF
(40 mL) at À788C. At the midpoint of the addition, the reaction
mixture turned from red to dark green; for the rest of addition it
remained green. CF3CO2H (1.3 mL, 17.0 mmol) was then added to
give a red solution of [(m-HS)2Fe2(CO)6].[15] Compound 1 (1.845 g,
8.5 mmol) was added to this solution and the mixture was stirred at
À788C for 0.5 h and at room temperature for 12 h. The volatiles were
removed under vacuum and the residue was separated by TLC using
CH2Cl2/petroleum ether (2:1, v/v) as eluent. Complex 2 was obtained
as
a red solid from the major, red band (1.320 g, 32%).
C15H9Fe2NO7S2: calcd. C 36.69, H 1.85, N2.85; found C 36.75, H
1.80, N3.02; 1H NMR (300 MHz, CDCl3): d = 4.36 (s, 4H; 2CH2),
6.83, 7.85 (2d, J = 8.4 Hz, 4H; C6H4), 9.86 ppm (s, 1H; CHO); IR
(KBr disk): n˜ = 2084, 2034, 2007, 1987, 1966 (C O), 1666 cm
(CHO).
À1
ꢀ
3: A mixture of benzaldehyde (0.182 mL, 1.8 mmol), 2 (0.295 g,
0.6 mmol), pyrrole (0.166 mL, 2.4 mmol), CF3CO2H (0.184 mL,
2.4 mmol), and CH2Cl2 (240 mL) was stirred at room temperature
in the dark for 15 h to give a purple-red solution. 2,3,5,6-Tetrachloro-
benzoquinone (p-chloranil; 0.443 g, 1.8 mmol) was added to this
solution and the new mixture was refluxed for 1 h to give a brown-
green solution. The solvent was removed under reduced pressure and
the residue was subjected to flash column chromatography (Al2O3,
CH2Cl2). The eluate was reduced to a suitable volume for TLC
separation with CH2Cl2/petroleum ether (1:1, v/v) as eluent. Tetra-
phenylporphyrin (0.052 g, 19%) was obtained from the first band as a
purple solid that was identified by comparison of its IR and 1H N MR
spectra with those of an authentic sample.[17,18] Complex 3 (0.138 g,
23%) was obtained as a purple-red solid from the second band.
C52H33Fe2N5O6S2: calcd. C 62.48, H 3.37, N7.01; found C 62.39, H
3.32, N7.04; 1H NMR (300 MHz, CDCl3): d = À2.76 (s, 2H; 2NH),
4.55 (s, 4H; 2CH2), 7.04, 7.07 (2s, 2H; 2m-H of C6H4), 7.74, 7.76 (2s,
9H; 6m-H of C6H5 and 3p-H of C6H5), 8.11, 8.14 (2s, 2H; 2o-H of
C6H4), 8.20, 8.23 (2s, 6H; 6o-H of C6H5), 8.85, 8.86 ppm (2s, 8H;
ꢀ
pyrrole rings); IR (KBr disk): n˜ = 3317 (NH), 2073, 2033, 1996 (C O),
À1
=
=
À
1558 (pyrrole C C), 1472 (pyrrole C N), 1350 cm (pyrrole C N);
ESI-MS: m/z 999.85 [M+]; UV/Vis (CH2Cl2) : lmax (loge) = 419 (5.61),
516 (4.24), 552 (3.93), 592 (3.72), 647 nm (3.74).
Received: October 12, 2005
Published online: January 3, 2006
Keywords: bioinorganic chemistry · enzyme models ·
.
hydrogenases · iron · porphyrinoids
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