Nucleophilic attack of hydroxide on a Mnv oxo complex: A model of the O-O bond formation in the oxygen evolving complex of photosystem II

Article abstract of DOI:10.1021/ja901139r

(Figure Presented) A manganese(III) corrole complex, 1, has been synthesized and used to study a potential mechanism for oxidation of water to molecular oxygen. Oxidation by t-BuOOH gave the Mn^V=O complex 2. Addition of hydroxide led to release

Full text of DOI:10.1021/ja901139r

Published on Web 06/04/2009
Nucleophilic Attack of Hydroxide on a MnV Oxo Complex: A Model of the
O-O Bond Formation in the Oxygen Evolving Complex of Photosystem II
Yan Gao,† Torbjo¨rn Åkermark,‡ Jianhui Liu,§ Licheng Sun,*,§,| and Bjo¨rn Åkermark*,†
Department of Organic Chemistry, Arrhenius Laboratory, Stockholm UniVersity, 10691 Stockholm, Sweden, DiVision
of Applied Electrochemistry, Department of Chemical Engineering and Technology, School of Chemical Science and
Engineering, Royal Institute of Technology (KTH), 10044 Stockholm, Sweden, State Key Laboratory of Fine
Chemicals, DUT-KTH Joint Education and Research Center on Molecular DeVices, Dalian UniVersity of
Technology (DUT), Zhongshan Road 158-40, 116012 Dalian, China, and DiVision of Organic Chemistry,
Department of Chemistry, School of Chemical Science and Engineering, Royal Institute of Technology (KTH),
10044 Stockholm, Sweden
Received February 13, 2009; E-mail: lichengs@kth.se; bjorn.akermark@organ.su.se
Scheme 1. Possible Mechanism of the Oxygen Evolution Cycle
In photosynthesis by green plants, water is the source of the
electrons that are finally used to convert carbon dioxide into
biomass. In this process, which takes place in the oxygen evolving
complex (OEC) of photosystem II, water is oxidized to molecular
oxygen. The catalytic center of the OEC consists of a tetranuclear
manganese cluster.1 Despite numerous experimental and theoretical
model studies, the actual mechanism for the formation of molecular
oxygen is not clear.2
In principle, three different mechanisms have been suggested
for the formation of the O-O bond: (a) nucleophilic attack of water
or hydroxide on a formally MnV species, (b) radical coupling of
two MnV oxo species, and (c) radical coupling of water (or
hydroxide) with a bridging oxygen in the manganese cluster.2
Many attempts have been made to prepare MnV oxo complexes
from species related to the OEC, but to date only circumstantial
evidence for their existence has been obtained. The groups of both
Crabtree and Brudvig2e and Pecoraro2c have provided evidence for
MnV oxo intermediates related to the OEC that were very short-
lived. However, both porphyrins3 and corroles and some related
complexes have been shown to give MnV oxo species with certain
stability.4 It therefore seemed interesting to prepare a reasonably
stable MnV corrole complex and react this with hydroxide ion in
order to see whether molecular oxygen could in fact be generated
by such a species. Here we report the successful outcome of a study
of this type using nitrophenylcorrole complex 1.
corrole complex 1 was therefore first prepared in high yield (91%)
by the reaction of 5,10,15-tris(4-nitrophenyl)corrole7 with
Mn(OAc)2 ·4H2O in refluxing DMF. This complex was dissolved
in acetonitrile and treated at room temperature with a slight excess
of t-BuOOH. A color change characteristic of conversion of a MnIII
to a MnV species occurred, as shown by the UV-vis spectra (Figure
1). Addition of an aqueous solution of (n-Bu)4NOH initiated rapid
evolution of oxygen, as shown by mass spectrometry.
In a previous study, we showed that both mononuclear and
dinuclear “Pacman” MnIV corrole complexes could act as catalysts
for electrochemical oxidation of water to molecular oxygen.5 The
dinuclear Mn complex was a more efficient catalyst than the
mononuclear one, but the difference was moderate. It thus seems
likely that a similar mechanism operates in both cases. This was
verified by density functional theory calculations, which suggested
that both complexes react via nucleophilic addition of water (or
hydroxide) to MnV oxo species (Scheme 1).6 In principle, a
dinuclear Mn complex could react via oxygen-oxygen coupling,
but this route was found to be energetically less favorable than
nucleophilic attack.
The electronic absorption spectrum of complex 1 shows major peaks
at 480 and 662 nm and a small peak at 418 nm (Figure 1a, solid line).
In the corresponding hydroxide complex, the peak at 418 nm does
not appear (Figure S1 in the Supporting Information). After addition
of a small excess of t-BuOOH, the absorption peaks at 480 and 662
nm were replaced by a new strong peak at 420 nm (Figure 1a, dashed
line). This spectrum is very similar to those previously reported for
MnVdO corrole complexes,4a,c,8 suggesting that the MnVdO complex
was formed in our system. Next, 2 equiv of (n-Bu)4NOH were added
to the mixture. Rapid oxygen evolution ensued, accompanied by the
disappearance of the peak at 420 nm and the appearance of new peaks
at 372, 455, and 605 nm (Figure 1a, dotted line). This spectrum
suggests that a MnIV complex was initially formed in our experiment.8,9
However, after a few minutes, the peaks at 372, 455, and 605 nm
decreased and were replaced by new peaks at 484 and 666 nm (Figure
In an attempt to get experimental evidence for a mechanism
involving nucleophilic addition, we decided to study the reaction
between a MnVdO corrole species and hydroxide ion. The MnIII
† Stockholm University.
‡ Department of Chemical Engineering and Technology, Royal Institute of
Technology.
§ Dalian University of Technology.
| Department of Chemistry, Royal Institute of Technology.
9
8726 J. AM. CHEM. SOC. 2009, 131, 8726–8727
10.1021/ja901139r CCC: $40.75  2009 American Chemical Society

C O M M U N I C A T I O N S
experiment and shows that the 16,18O2 was formed by addition of
18O hydroxide to the unlabeled MnVdO.
Figure 1. UV-vis spectral alterations for manganese corrole complexes
in CH3CN. (a) MnIII corrole complex (solid); after addition of oxidant
(dashed); after addition of base (dotted); (b) time-dependent UV-vis spectral
alteration for the MnIV species.
Figure 3. Oxygen isotope studies using online gas analysis by mass
spectrometry: (left) without 18O-labeled water; (right) with 18O-labeled water.
The solid lines are fits to the 16,18O2 data (O).
The mechanism of water oxidation can thus be summarized in
the following way: First, the MnIII corrole complex 1 is oxidized
to the MnV oxo complex 2. Second, nucleophilic attack of hydroxide
presumably gives initially the MnIII hydroperoxy complex 3. This
is oxidized (e.g., by unreacted MnV oxo complex) to give the MnIV
hydroperoxy complex, which after loss of a proton gives rise to
the observed peroxy complex 4. This either disproportionates with
loss of oxygen or is oxidized to the corresponding MnV complex,
which undergoes reductive elimination of oxygen to form the
starting complex 1. The main conclusion from this study is that
O-O bond formation via nucleophilic attack of hydroxide on a
1b). These spectral changes indicate that the MnIV species was
gradually transformed into a MnIII species.
MnV oxo oxygen has been experimentally demonstrated and is a
viable mechanism for conversion of water into molecular oxygen.
Acknowledgment. Financial support of this work by the
Swedish Energy Agency (STEM), the K & A Wallenberg Founda-
Figure 2. Oxygen isotope studies using HRMS.
tion, and the Swedish Research Council (VR) is gratefully ac-
knowledged.
The results could be confirmed by high-resolution mass spectrom-
etry (HRMS) of the Mn corrole intermediates in the reaction (Figure
2 and Figures S2, S3, and S4). The mass spectrum of the starting MnIII
corrole complex 1 (negative mode, m/z) showed a strong peak at
758.0851, corresponding to [M + HCOO]- (Figure S2; calcd for M
) C37H20MnN7O6, 758.0832). Upon oxidation with t-BuOOH, the
MnVdO complex 2 (M ) C37H20MnN7O7) was formed, as shown by
both the appearance of a peak at 802.1482 (Figure 2, left; calcd for
[M + t-BuO]-, 802.1458) and the UV-vis spectrum (Figure 1). On
addition of 2 equiv of alkali, a MnIV complex was rapidly formed, as
shown by both UV-vis spectrum and the peak at 745.0780 in the
mass spectrum attributable to MnIV complex 4 (Figure S3; calcd for
M ) C37H20MnN7O8, 745.0754 [M]-). After another few minutes,
the composition of the mixture changed, and the major observed peak
was found at 730.0903, corresponding to the MnIII complex [1 + OH]-
(Figure S4; calcd 730.0883).
Supporting Information Available: Experimental preparation of
1, UV-vis spectra of complex 1 upon reaction with hydroxyl, HRMS
data for complex 1 and intermediate 4, and the gas analysis setup. This
material is available free of charge via the Internet at http://pubs.acs.org.
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When these experiments were repeated using 18O-labeled water,
incorporation of 18O into the peroxy intermediate 4 was observed
by HRMS. There was thus a substantial increase of the peak at
747.0818 corresponding to 18O-labeled 4 (Figure 2, right; calcd
747.0796 [M]-).
The experiments were carried out using online gas analysis by
mass spectrometry to measure the amount of oxygen generated
(Figure 3). When hydroxide was added to oxo complex 2, rapid
oxygen evolution took place. The oxygen curves in Figure 3 show
that only a small amount of 16,18O2 was formed, corresponding to
the content of 18O in natural water (Figure 3, left). However, when
18O-labeled water (10% 18O) was used, ∼8% 16,18O2 was contained
in the generated oxygen (Figure 3, right). This is approximately
proportional to the 18O/16O ratio of the labeled water in the
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