A synthetic model for the oxygen-evolving complex in Sr2+- containing photosystem II

Article abstract of DOI:10.1039/c4cc02349h

A novel heterometallic MnSr complex containing the Mn₃SrO ₄ cuboidal moiety and all types of μ-O^2- moieties observed in the oxygen-evolving complex (OEC) in Sr²⁺-containing photosystem II (PSII) has been synthesized and characterized, which provides a new synthetic model of the OEC.

Full text of DOI:10.1039/c4cc02349h

Showcasing work from the Laboratory of Hongxing Dong,
Polymer Materials Research Center, College of Materials
Science and Chemical Engineering, Harbin Engineering
University (Harbin) and Laboratory of Chunxi Zhang, Laboratory
of Photochemistry, Institute of Chemistry, Chinese Academy of
Sciences (Beijing).
As featured in:
A synthetic model for the oxygen-evolving complex
in Sr2+-containing photosystem II
It is of a great challenge for chemists to synthesize accurate
structural model for the oxygen-evolving complex (OEC) in
Photosystem II. Here, a novel artificial complex is synthesized
with remarkable structural similarities to the OEC, in respects of
the peripheral ligands, the Mn3SrO4 cuboidal moiety and three
different types of bridging oxido moieties, which may provide
new insights to understanding of the structure and properties of
the OEC in nature.
See Chunxi Zhang,
Hongxing Dong et al.,
Chem. Commun., 2014, 50, 9263.
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A synthetic model for the oxygen-evolving
complex in Sr2+-containing photosystem II†
Changhui Chen,a Chunxi Zhang,*b Hongxing Dong*a and Jingquan Zhaob
Cite this: Chem. Commun., 2014,
50, 9263
Received 30th March 2014,
Accepted 25th April 2014
DOI: 10.1039/c4cc02349h
www.rsc.org/chemcomm
A novel heterometallic MnSr complex containing the Mn3SrO4 cuboidal m2-O2À (e.g. O4), m3-O2À (e.g. O1, O2, O3) and m4-O2À (e.g. O5). The
moiety and all types of l-O2À moieties observed in the oxygen-evolving entire OEC is embedded in a large protein matrix through H-bond
complex (OEC) in Sr2+-containing photosystem II (PSII) has been interactions and direct ligations to six carboxylate and one imidazole
synthesized and characterized, which provides a new synthetic model group of the amino acid residues on the D1 and CP43 polypeptides in
of the OEC.
PSII. Ca2+ is known to be an essential component of the function of
OEC,6 which can be functionally replaced only by Sr2+ without
The oxygen-evolving complex (OEC) within photosystem II (PSII) significantly disturbing the structure of the OEC.5,7
of plants, algae and cyanobacteria serves as nature’s blueprint for
The water-splitting reaction involves five different S-states
a water splitting catalyst.1,2 The structure of OEC has been recently (Sn, n = 0 to 4) of the OEC. Spectroscopic studies have shown
revealed by the X-ray crystal structure of PSII (Fig. 1).3–5 There are that the oxidation states and the geometry of the OEC undergo
two unique characteristics of the structural motif of OEC. One is changes during these state transitions.8,9 However, the detailed
the incorporation of Ca2+ within the Mn3CaO4 cubane through catalytic mechanism of the OEC, including the role of Ca2+/Sr2+ in
three m-oxido moieties. The other is the simultaneous presence of PSII remains under extensive debate.10–17 Due to the structural
complexity of the OEC, it is a great challenge for chemists to
synthesize accurate structural and functional models for the OEC
in the laboratory.
To date, many multinuclear Mn complexes have been
synthesized as models of the OEC.1,18–23 However, only a few
synthetic MnCa and MnSr heterometallic complexes24–36 have
been reported. Moreover, no effort has been made to mimic the
three types of bridging oxido moieties (m2-O2À, m3-O2À and m4-O2À
)
at the same time. In terms of the functional properties, the redox
potentials of the two current complexes containing MnIV3CaO4 or
MnIV3SrO4 cuboidal moieties with a multinucleating ligand34,36
were very low, À0.5V vs. NHE, compared to the requirement of the
thermodynamic potential for water oxidation (+0.8 V vs. NHE).37,38
Therefore, it is highly desirable to synthesize more accurate
structural and functional models for the OEC.
Here, we report a novel MnSr complex containing the
Mn3SrO4 cuboidal moiety and all types of m-oxido moieties
observed in the OEC; in addition, the complex exhibits the
redox potential at +0.9 V vs. NHE, suggesting its potential as a
good synthetic model for the OEC.
Fig. 1 Scheme for the OEC in PSII.
a Polymer Materials Research Center, Key Laboratory of Superlight Materials &
Surface Technology of Ministry of Education, College of Materials Science and
Chemical Engineering, Harbin Engineering University, Harbin 150001, China.
E-mail: dhongxing@hrbeu.edu.cn; Tel: +86-451-82568191
b Laboratory of Photochemistry, Institute of Chemistry, Chinese Academy of
Sciences, Beijing 100190, China. E-mail: chunxizhang@iccas.ac.cn;
Fax: +86-10-82617315; Tel: +86-10-82617053
This complex was synthesized in a reaction of Bun4NMnO4,
Mn(CH3CO2)2(H2O)4 and Sr(CH3CO2)2(H2O)0.5 in a molar ratio
of 4 : 1 : 1 in boiling acetonitrile in the presence of an excess of
pivalic acid. Red-brown crystals were formed after cooling,
which were further recrystallized in ethyl acetate solution in
† Electronic supplementary information (ESI) available: Experimental section,
X-ray structure information, BVS calculations, UV-vis absorption spectrum, EPR
spectrum, Cyclic voltammogram (CV), Differential pulse voltammogram (DPV).
CCDC 994140. For ESI and crystallographic data in CIF or other electronic format
see DOI: 10.1039/c4cc02349h
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deprotonated state of all bridged oxygen atoms are confirmed
by bond-valence sum calculations (Table S4, ESI†). To our
knowledge, this is the first time that a MnSr complex containing
three types of m-O2À moieties simultaneously has been synthesized.
Therefore, complex 1 provides an artificial model to interrogate the
functionalities of these m-O2À moieties in the OEC of PSII.
The average distance of Mn–Sr in complex 1 is 3.58 Å, which
is longer than 3.40 Å observed in a previous Mn3SrO4 complex
containing a multinucleating ligand,34 but is close to the 3.55 Å
separation observed in OEC of Sr2+-containing PSII5 (Table S5,
ESI†). The average 2.77 Å distance of Mn–Mn in complex 1 is
slightly shorter than that observed previously in the Mn3SrO4
complex34 (2.82 Å), and also obviously shorter than 3.00 Å than
that in the OEC of Sr2+-containing PSII,5 which is likely because
of the higher oxidation states of the Mn ions in complex 1.
The average distance of m3-O–Mn in the complex 1 is 1.86 Å,
Fig. 2 The structure of complex 1. Mn, Sr, O, N, C and H are shown in
yellow, violet, red, blue, cyan and green, respectively. For clarity, all hydrogen
atoms except two active protons of pivalic acids are omitted. H-bonds are
shown with a dashed line, and values display the H-bond lengths.
which is slight shorter than 1.88 Å observed in the OEC of Sr2+
-
the presence of B2% pyridine (for details of preparation, see
ESI†). The final product of complex 1, [MnIV6Sr2O9(ButCO2)10
(ButCO2H)2(C5H5N)2] was obtained as black rod crystals with a
yield of 22% (on a strontium basis).‡
containing PSII,5 or 1.87 Å in the Mn3SrO4 complex reported.34
The average distance of m2-O–Mn in complex 1 is 1.76 Å, which
is shorter than 1.89 Å observed in OEC of Sr2+-containing PSII5
(Table S5, ESI†), which is likely because of the higher oxidation
state of the Mn ions in complex 1 as well.
Fig. 2 shows the crystal structure of complex 1. The peripheral
ligands of complex 1 include ten pivalate, two pivalic acid and two
pyridine groups. Each coordinated pivalic acid further interacts
with m3-O2À through a strong H-bond (Fig. S2, ESI†). All these
ligations and H-bond interactions in complex 1 are reminiscent of
the protein environment of the OEC in PSII.3–5
The lengths of the two m4-O–Mn in complex 1 are in the range
of 1.84 Å to 1.87 Å with an average of 1.86 Å, which is a common
distance for m4-O2À–Mn in most multinuclear Mn complexes and
heteronuclear MnSr or MnCa complexes.24,25,35,39 However, the
length of 1.86 Å is remarkably shorter (by 0.64 Å) than the average
value of 2.5 Å in the OEC of Ca2+ or Sr2+ containing PSII.4,5 It is
important to point out that the m4-O5 atom in the OEC has attracted
extensive attention in the studies of water oxidation in PSII
recently.14,16,17,39–43 Theoretical studies16,17 have suggested that the
m4-O5 atom may act as a source of oxygen atoms for the formation of
O–O bonds in the higher S-state (e.g. S3, S4) of the OEC, in which the
valences for all Mn ions are most likely to be +4,8,9 similar to that
in complex 1. It is important to mention that the assignment of
this m4-O5 atom was not unambiguous due to its much weaker
electron density than all other bridging oxido moieties in the X-ray
diffraction data of the OEC.4,5,39 The structural characteristics of
the m4-O2À in complex 1 and various MnSr–MnCa complexes24,25,35
could be considered as structural pieces of evidence to argue that
the binding and the function of the m4-O5 atom in the OEC is
worth being addressed in the future.
All six Mn ions are six-coordinate. The two Sr2+ ions are
eight- and nine-coordinate, respectively, resulting in the asymmetry
of the entire structure of complex 1 (Table S3, ESI†).
In the core of complex 1 (Fig. 3), two MnIV3SrO4 cuboidal
units are connected by one m2-O2À and two m4-O2À moieties.
Three types of m-O2À moieties (m2-O2À, m3-O2À, m4-O2À) are seen
in complex 1. The +4 valences of all six Mn ions and the doubly
The EPR measurements show that complex 1 displays similar
EPR signals as observed in the Mn3Ca2O4 complex reported by
Christou’s group.35 It was found that both solid and solution
samples of complex 1 give rise to similar EPR signals (Fig. S5,
ESI†), which suggests that the entire structure of complex 1 is
maintained not only in crystals but also in solution.
Cyclic voltammogram (CV) measurements (Fig. 4) of complex 1
display two irreversible redox processes at À0.5 V and +0.9 V vs.
NHE, assigned to the couples of [MnIIIMnIV2SrO4]/[MnIV3SrO4] and
[MnIV3SrO4]/[MnVMnIV2SrO4], respectively, according to a previous
report.34,44 The irreversibility of these two couples may reflect
some structural changes during the redox processes. It is noticed
that the +0.9 V redox process appears only after undertaking the
À0.5 V irreversible redox process (Fig. S6 and S7, ESI†), suggesting
Fig. 3 The core of complex 1 (bottom) and OEC in PSII (top). The fraction
of Mn4SrO5 of complex 1 similar to the OEC is emphasized with a red-
dashed circle. The values display the lengths of selected bonds (Å).
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Fundamental Research Funds for the Central Universities of
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Notes and references
‡ Elemental analysis (%) calcd for complex 1 (C70H120N2O33Mn6Sr2): C,
41.57; H, 5.98; N, 1.38; found: C, 41.57; H, 5.79; N, 1.63. Crystal
structure data for complex 1: C70H120N2O33Mn6Sr2, M = 2022.56, black
rod crystal, orthorhombic, P212121, a = 15.290(3) Å, b = 18.205(4) Å, c =
36.041(7) Å, a = 90.001, b = 90.001, g = 90.001, V = 10032(3) Å3, 32 066
reflections collected; 1083 parameters were refined in the final cycle of
refinement using 17 540 reflections (I 4 2s(I)); R1 = 0.0947, wR2 = 0.2202
(based on F2 and all data). Also see CCDC 994140 for complex 1.
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This journal is ©The Royal Society of Chemistry 2014
Chem. Commun., 2014, 50, 9263--9265 | 9265