Artificial Photosynthesis: From Nanosecond

Electron Transfer to Catalytic Water Oxidation

€ AS,
MARKUS D. KARK € ERIC V. JOHNSTON, OSCAR VERHO, AND
€
BJORN ÅKERMARK*
Department of Organic Chemistry, Arrhenius Laboratory, Stockholm University,
SE-106 91 Stockholm, Sweden
RECEIVED ON MARCH 18, 2013

CONSPECTUS

H uman society faces a fundamental challenge as energy consumption is

projected to increase due to population and economic growth as fossil
fuel resources decrease. Therefore the transition to alternative and sustainable
energy sources is of the utmost importance. The conversion of solar energy
into chemical energy, by splitting H2O to generate molecular O2 and H2, could
contribute to solving the global energy problem. Developing such a system
will require the combination of several complicated processes, such as light-
harvesting, charge separation, electron transfer, H2O oxidation, and reduction
of the generated protons. The primary processes of charge separation and
catalysis, which occur in the natural photosynthetic machinery, provide us with
an excellent blueprint for the design of such systems.
This Account describes our efforts to construct supramolecular assemblies
capable of carrying out photoinduced electron transfer and to develop artificial water oxidation catalysts (WOCs). Early work in our
group focused on linking a ruthenium chromophore to a manganese-based oxidation catalyst. When we incorporated a tyrosine
unit into these supramolecular assemblies, we could observe fast intramolecular electron transfer from the manganese centers, via
the tyrosine moiety, to the photooxidized ruthenium center, which clearly resembles the processes occurring in the natural system.
Although we demonstrated multi-electron transfer in our artificial systems, the bottleneck proved to be the stability of the WOCs.
Researchers have developed a number of WOCs, but the majority can only catalyze H2O oxidation in the presence of strong
oxidants such as CeIV, which is difficult to generate photochemically. By contrast, illumination of ruthenium(II) photosensitizers in
the presence of a sacrificial acceptor generates [Ru(bpy)3]3þ-type oxidants. Their oxidation potentials are significantly lower than
that of CeIV, but our group recently showed that incorporating negatively charged groups into the ligand backbone could decrease
the oxidation potential of the catalysts and, at the same time, decrease the potential for H2O oxidation. This permitted us to develop
both ruthenium- and manganese-based WOCs that can operate under neutral conditions, driven by the mild oxidant [Ru(bpy)3]3þ.
Many hurdles to the development of viable systems for the production of solar fuels remain. However, the combination of
important features from the natural photosynthetic machinery and novel artificial components adds insights into the complicated
catalytic processes that are involved in splitting H2O.

The supply and production of clean and sustainable carbon- Photosynthesis: Nature's Masterpiece
neutral energy will unquestionably be the 21st century's most About 2 billion years ago, Nature developed an extraordinary
demanding scientific challenge. One attractive option that process for storing solar energy, by converting H2O and CO2 into
holds sufficient potential to feed this process on a global scale carbohydrates and other valuable chemical feedstocks, such as
would be to use the energy derived from sunlight to split H2O ATP. To accomplish this demanding task, it is important to
into O2 and couple it with the production of solar fuels, such as efficiently combine several complex features: light-harvesting
H2. Here, Nature provides us with an excellent example of by a chromophore, charge separation, electron transfer (ET), oxi-
how this can be achieved, thus making it attractive to mimic dation of H2O, and finally reduction of the generated protons.5
the basic principles of natural photosynthesis for the sustain- Light-Induced Charge Separation. The first step in the
able production of renewable solar fuels.14 multistep process of photoinduced splitting of H2O is the
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absorption of a photon by chlorophyll and other light- man-made systems that mimicked the basic principles of the
absorbing pigments. They efficiently transfer the captured reaction center in PS II. It was decided to synthesize simple
energy to the reaction center of photosystem (PS) II, P680, model systems where a [Ru(bpy)3]2þ-type photosensitizer
resulting in an excited state (P680*). From the excited state of (bpy = 2,20 -bipyridine) was covalently coupled to a redox-
P680, ET occurs to a pheophytin molecule, whereby the active moiety containing manganese or tyrosine. It was
electron is passed along a transport chain to finally end up anticipated that upon illumination of the [Ru(bpy)3]2þ moi-
in PS I for the reduction of NADPþ and production of “H2” in ety, the excited state of ruthenium(II) would deliver an
the form of NADPH. However, the primary charge-separated electron to the external acceptor to yield ruthenium(III).
state that is created is short lived and would recombine The generated hole would subsequently be refilled by an
without this series of ET processes. The key to efficient intramolecular ET from the incorporated redox-active moi-
harnessing of the absorbed sunlight is to create a charge- ety. The [Ru(bpy)3]2þ-type complexes were chosen because
separated state where the electrons and electron holes are they have been studied for several decades as a result of
sufficiently separated from each other. The oxidized form of their long-lived excited state lifetimes, high chemical and
P680, P680•þ, is a strong oxidant with an oxidation potential thermal stability, and easy functionalization.7
of ca. þ1.2 V versus the normal hydrogen electrode (NHE). Our first attempts in achieving this focused on linking a
Regeneration of the P680 reaction center is accomplished by mononuclear manganese complex to a ruthenium photo-
the abstraction of an electron from the oxygen evolving sensitizer. Our approach resulted in the synthesis of the
complex (OEC) via a redox-active tyrosine moiety (Tyrz).15 heterobimetallic assemblies 18 (Figure 1).8,9 Flash photo-
The Oxygen Evolving Complex: The H2O Splitting Site. lysis experiments of complex 1 and the corresponding com-
The electrons that are used to convert CO2 into valuable plex without the manganese center, in the presence of an
building blocks are ultimately derived from H2O. At the heart external electron acceptor (methyl viologen, MV2þ), con-
of PS II, resides the so-called OEC, which is responsible for firmed that ET occurred from the excited ruthenium center to
catalyzing the four-electron oxidation of H2O. After four MV2þ to generate [Ru(bpy)3]3þ and MV•þ. Regeneration of
consecutive electron abstractions from the OEC, two mole- [Ru(bpy)3]2þ proved to be 1 order of magnitude faster for 1
cules of H2O are converted into one molecule of O2 and four than for the complex lacking the manganese, supporting
protons. The elaborate core of the OEC consists of a tetra- that intramolecular ET takes place to give a manganese(III)
nuclear manganese complex with a calcium atom in close species. The process displayed first-order kinetics with a rate
proximity (Mn4Ca).6 It is surrounded by amino acids, which constant of 1.8  105 s1.
are essential for stabilizing the OEC by charge neutralization Additional proof that the manganese(II) moiety in 1 is
and promoting proton-coupled electron transfer (PCET). able to reduce the photogenerated [Ru(bpy)3]3þ species was
afforded by electron paramagnetic resonance (EPR). Since
Artificial Photosynthesis both manganese(II), with S = 5/2, and [Ru(bpy)3]3þ are EPR
The photoinduced splitting of H2O requires interfacing sev- active, ET from the manganese(II) moiety should drastically
eral fundamental but challenging photophysical steps with alter the EPR spectra. Mixing equimolar amounts of
complicated chemical transformations. During the last four [Ru(bpy)3]3þ (chemically generated) and 1 resulted in the
decades great efforts have been devoted to develop sys- disappearance of the characteristic peaks for the starting
tems that are capable of mimicking the basic principles of compounds, highlighting that [Ru(bpy)3]3þ is capable of
Nature for conversion of solar energy into chemical energy. oxidizing manganese(II) to manganese(III). This work de-
The key components in an artificial system for H2O splitting monstrated for the first time that coupled ruthenium
are a light-absorbing photosensitizer, a water oxidation manganese systems can undergo intramolecular ET to the
catalyst (WOC), that is, a catalyst that refills the holes that photooxidized ruthenium(III) center in the presence of an
are created, and a reduction catalyst that converts the external electron acceptor, thereby mimicking the concept
generated electrons and protons to solar fuels. The essential of Nature.
feature in realizing artificial photosynthesis is the coupling of Additional work focused on investigating the different
the one-photonone-electron charge separation events to parameters that influenced the efficiency and rates of the
the four-electron oxidation of H2O.1 excited state quenching and the intramolecular ET between
Coupling Light Sensitization to Electron Transfer. In the the manganese moiety and the photogenerated ruthe-
late 1990s, we initiated a project dedicated to developing nium(III).10 The recovery of ruthenium(II) was found to be

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FIGURE 1. Molecular structures of the coupled rutheniummanganese complexes 18.

independent of the concentration of complexes 18, estab- The introduction of electron-withdrawing substituents on
lishing that the ET occurs intramolecularly. This work the bpy ligands made it possible to localize the excited state
showed that the quenching rate constant decreased expo- on these ligands and thus increase the distance to the
nentially with the metal-to-metal distance for complexes manganese moiety. This is clearly demonstrated by the
18. More importantly, it demonstrated that it is possible to dramatic differences in excited state lifetimes of 7 (23 ns)
increase the excited state lifetime with unchanged metal-to- and 8 (1200 ns). Furthermore, it was established that the ET
metal distance by tuning the ligand environment. Although rate was not only dependent on the metal-to-metal distance
complexes 4, 7, and 8 all have approximately the same and that variations in reorganization energy and electronic
metal-to-metal distance, the excited state lifetime of 7 is coupling were also important.
significantly shortened. This dramatic difference can be As observed from our initial work, having a too short
ascribed to the fact that the excited state in 7 is delocalized distance between the ruthenium- and manganese centers
over the phenyl ring that is linking the ruthenium and resulted in undesirable quenching of the excited photosen-
manganese moieties together, bringing the excited state sitizer. It was thought that introducing a spacer between the
closer to the manganese moiety and shortening the lifetime. ruthenium chromophore and the manganese moiety would

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FIGURE 2. Light-induced electron transfer in an artificial triad consisting of the rutheniumtyrosine assembly 9 and the Mn2III,III complex 10.

be favorable. This modification should preferably not to oxidize the external manganese complex in a controlled
quench the excited state of the photosensitizer and the fashion, to allow for efficient ET to occur. If successful, this
reorganization energy should be lower than for the manga- biomimetic approach would mimic several important as-
nese moiety, allowing for faster ET. In Nature, a redox-active pects in the natural photosynthetic machinery. The Mn2III,III
tyrosine unit (Tyrz) is involved in the ET between P680 and the complex 10 would be an excellent candidate, because the
OEC. We therefore prepared a supramolecular assembly one-electron oxidation product, the mixed-valence Mn2III,IV,
consisting of a tyrosine unit linked to a ruthenium(II) photo- is stable and EPR-active. Combined flash photolysis and EPR
sensitizer (Figure 2).11 measurements of a reaction mixture containing 9, manga-
When the tyrosine containing compound 9 was studied nese complex 10, and an electron acceptor (MV2þ or CoIII),
by time-resolved emission spectroscopy, in the absence of resulted in the 16-multiline signal characteristic of a mixed-
any electron acceptors, negligible quenching was observed valence Mn2III,IV species. Solutions lacking either 9 or
by the tyrosine unit. However, addition of one of the electron the manganese complex did not result in any observable
acceptors, MV2þ or pentaamminechlorocobalt(III) chloride 16-multiline signal, verifying that the Mn2III,IV is generated
([Co(NH3)5Cl]þ, CoIII), resulted in a decreased emission life- from light-dependent reactions. Transient EPR measure-
time. With transient absorption spectroscopy, the electron ments in the absence of 10 revealed that the photogener-
transfer was followed for compound 9 and a reference ated ruthenium(III) center was reduced via intramolecular ET
compound, lacking the tyrosine unit. The reference com- from the tyrosine moiety (vide supra). However, addition of
pound exhibited similar behavior as [Ru(bpy)3]2þ. A deviat- manganese complex 10 resulted in a faster decay of the
ing result was observed with the tyrosine containing tyrosyl radical, establishing that manganese complex 10
compound 9, which displayed an increased rate for the mediates ET to it. The promising findings with this system
ruthenium(II) recovery. This effect suggested that intramo- were significant steps toward realizing rutheniummanga-
lecular ET from tyrosine to photogenerated ruthenium(III) nese-based systems for artificial photosynthesis.
occurred in 9, regenerating ruthenium(II) and forming a Based on the collected data from our synthesized model
tyrosyl radical. Further support for this tyrosineruthenium systems, a dinuclear manganese(II,II) complex was con-
ET was afforded by EPR measurements, in which an EPR nected to a ruthenium photosensitizer through an amide
signal at g = 2.0045 was generated and ascribed to a tyrosyl link to generate the trinuclear supramolecular assembly 11
radical. To prove that ET indeed took place intramolecularly, (Figure 3).13,14 Emission lifetime measurements confirmed
the ET for the separate components (i.e., tyrosine and that the manganese centers in 11 had a profound influence
[Ru(bpy)3]2þ) was studied. This demonstrated that the tyro- on the quenching of the ruthenium excited state. From flash
sine enhanced the ruthenium(II) recovery but to a lower photolysis experiments of 11, it could be seen that the
extent compared with the coupled system 9. generated ruthenium(III) species was not reduced by recom-
The intriguing results derived with compound 9 led us to bination of ruthenium(III) and MV•þ. The recovery of the
test whether a suitable manganese complex could be photo- ruthenium(II) was essentially complete in less than 100 ns,
oxidized by 9.12 Our expectation was that the photogener- and instead intramolecular ET from the dinuclear manga-
ated tyrosyl radical would possess enough oxidizing power nese moiety had occurred. The ET events were found to be

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FIGURE 3. The coupled RuMn2 system 11, where the Mn2II,II unit is
capable of mediating three consecutive electron transfers to the
photogenerated RuIII to generate Mn2III,IV. FIGURE 4. Coupled RuRu2 systems for photoinduced electron transfer.

limited by the initial quenching of the MV2þ, indicating that and EPR measurements were combined. When 11 was
the rate constant for the intramolecular ET from the man- subjected to several flashes (in aqueous solutions), EPR
ganese moiety to the generated ruthenium(III) is greater showed that the manganese centers in 11 were oxidized
than 1  107 s1. This is an enhancement by 2 orders of mag- three steps to generate the Mn2III,IV species. Electrochemical
nitudes compared with other rutheniummanganese dyads measurements showed that the presence of H2O had a
with comparable rutheniummanganese distances (∼16 Å). profound effect on the redox chemistry of the dinuclear
In related studies, Wieghardt and co-workers presented a manganese moiety in 11. The addition of H2O alters the
trinuclear manganese complex coupled to an array of six cyclic voltammogram of 11 where the most significant
[Ru(bpy)3]2þ-type photosensitizers, where it was shown that alteration is lowering of the Mn2III,IV/Mn2III,III redox potential.
after excitation and transfer of an electron to an acceptor, It is assumed that when the Mn2III,III state is reached, ligand
the Mn3II cluster was oxidized to Mn2IIMnIII.15 exchange occurs in the presence of H2O. Replacement of the
Charge separation with single electronic transitions is acetate ligands by aqua ligands enables the complex to
relatively easy to accomplish, but additional hurdles appear access the Mn2III,IV state by allowing for PCET. This reduces
when carrying out multi-electron transfer. The excited the overall charge of the complex and allows for the gen-
ruthenium(II) is a strong reductant and has the possibility eration of the Mn2III,III state by the photochemically gener-
of being oxidatively quenched by any intermediate with a ated ruthenium(III), a key element for performing multi-
higher redox potential. Therefore, absorption of the next electron transfer and catalysis.
photon by the ruthenium chromophore increases the driv- Continued work addressed linking a dinuclear ruthenium
ing force for the oxidized manganese complex to become unit to a ruthenium chromophore, which resulted in assem-
reduced by ET from the excited state of the ruthenium(II) blies 12ac (Figure 4).16 Surprisingly, quenching of the
chromophore. This is a nonproductive and energy wasting [Ru(bpy)3]2þ chromophore excited state was very efficient.
reaction that obviously cannot be avoided by manipulating Even attachment of carboxyl groups to the chromophore,
the redox potentials. Instead, it has to be resolved by which had proven to be efficient with the corresponding
rendering the backward reaction slow compared with the manganese dyads, failed, and the lifetime remained short.
forward ET from the ruthenium(II) excited state. However, attaching dyads 12b and 12c to nanostructured
The question now was whether we could extract several TiO2 allowed for charge separation thanks to the extremely
electrons from the manganese moiety, allowing for multi- fast electron injection from the excited ruthenium(II)
step oxidations. To answer this question, flash photolysis state into the conduction band of TiO2. Recently, several

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FIGURE 5. Molecular structures of complexes 1315.

examples have appeared where a ruthenium photosensiti- group has previously shown that negatively charged groups
zer has been coupled to a ruthenium WOC and subsequently in the ligand backbones decreased the redox potentials of
attached to an electrode, which splits H2O photo(electro)- the corresponding metal complexes.20,21 Replacing the
chemically.17,18 benzylic amines in these complexes by more robust func-
tional groups, in combination with phenolic and carboxylic
Water Oxidation Catalysis groups, would hopefully favor proton-coupled events and
The four-electron oxidation of H2O manages to connect result in active WOCs with low redox potentials. This led to
single-electron chemistry with multi-electron catalysis. One the development of complexes 1315 (Figure 5),2225
way of facilitating this complicated task would be to involve which were all active WOCs and had significantly decreased
PCET. PCET is of fundamental importance in many biological redox potentials compared with earlier WOCs based upon
and chemical process, and involves the coupling of electron neutral polypyridyl ligands.
transfer to proton transfer, which has a profound effect in the Molecularly Defined Single-Site Ruthenium Water Oxi-
natural H2O oxidation. PCET permits the total charge of a dation Catalysts: Simple and Efficient. Based on the effi-
chemical species to remain unchanged, whereas just single- ciency of complex 15, it was envisioned that the two
electron transfers without the loss of a proton leads to molecularly defined single-site ruthenium complexes 16
charge build-up and high-energy intermediates. Coupling and 17 housing two benzimidazole-based meridionally co-
electron transfer to proton transfer may open a route for the ordinating ligands were promising ligand backbones and
accumulation of multiple redox equivalents at single metal could favor proton-coupled events (Figure 6).26 In order to
centers and influence reaction pathways and energetics of a assess the catalytic activity, real-time mass spectrometry
chemical reaction.19 (MS) measurements were used to detect the evolved gas-
Introducing Negatively Charged Groups into the Li- eous products during catalysis. To our delight both com-
gand Backbones of Water Oxidation Catalysts. Most of plexes were active WOCs, when either pregenerated or
the developed WOCs suffer from a serious drawback; in photogenerated [Ru(bpy)3]3þ-type complexes were used as
order for the oxidations to be thermodynamically favorable, oxidant. In the chemical oxidations, it was revealed that
they need to be driven by a strong oxidant, such as ceric complex 16 generated a high turnover number (TON) and a
ammonium nitrate (CeIV). Since CeIV cannot be photochemi- high turnover frequency (TOF).
cally regenerated from CeIII, its use in large scale applications Electrochemical measurements showed that the redox
is questionable. An appealing and more viable approach potentials of both complexes were significantly lowered
would be to drive H2O oxidation with [Ru(bpy)3]3þ that can compared with other ruthenium WOCs housing neutral ligands,
be photogenerated from the corresponding [Ru(bpy)3]2þ- together with an electrocatalytic wave for H2O oxidation start-
type complex. ing at 1.24 V vs NHE (at pH 7). Support for a ligand exchange
This could be accomplished by lowering the catalyst process in which a picoline is exchanged by a solvent H2O
redox potentials by the introduction of anionic functional- molecule, to generate the important rutheniumaqua species,
ities (i.e., substituents that have the possibility to be was obtained from UVvis spectrophotometric titration,
deprotonated) into the ligand frameworks of WOCs. Our along with high-resolution MS experiments. We could also

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FIGURE 6. Water oxidation catalysis by the single-site ruthenium complexes 16 and 17. L = 4-picoline.

amide) ligands are still relatively exotic. An important fea-

ture of N-amidato ligands is that they display strong σ-donor
ability from the coordinated nitrogen(s). This stabilizes the
metal center and allows access to high oxidation states. It
was envisioned that a tailored catalyst design based upon
the tetradentate ligand H2bpb (H2bpb = N,N0 -1,2-phenylene-
bis(2-pyridine-carboxamide) would afford active ruthenium
WOCs.28 This tetradentate ligand contains two sites with
dissociable protons, and the readily accessible ligand scaf-
fold offers an easily modified environment. This is an
important factor for the tuning of future WOCs and in the
FIGURE 7. Pourbaix diagram of complex 16 (where HRu(II) construction of integrated supramolecular assemblies for
corresponds to the ruthenium(II) complex with the protonated overall H2O splitting.
imidazole). Adapted with permission from ref 26. Copyright 2012 Complex 18 was found to be capable of driving H2O
WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
oxidation with [Ru(bpy)3]3þ as chemical oxidant. Under the
observe the high-valent RuVdO intermediate by MS, re- highly oxidizing conditions required to carry out the oxida-
garded as the key intermediate in H2O oxidation.27 Finally, tion of H2O, the WOCs decompose or deactivate after a
the Pourbaix diagram (potential/pH diagrams) for complex 16 certain period of time. This is a serious and general issue
was constructed since this type of diagram is a valuable tool encountered with WOCs and insight into the deactivation
and points out possible stable (oxidation) states of a system. pathways is necessary if more efficient WOCs are to be
The Nernst equation reveals that the potential for a one- developed. Examining the reaction mixtures after O2 evolu-
electronone-proton redox reaction will change by 59 mV tion had ceased showed the appearance of a peak at m/z
per pH unit and for a two-electronone-proton redox reac- 462.9985, corresponding to [Ru(bpb)(CO)(H2O) (19)  Hþ]
tion this change will be 29 mV per pH unit. This distin- (Figure 8). During H2O oxidation, CO and CO2 are usually
guishes redox processes that are proton-coupled from observed due to decomposition of the organic components,
nonproton-coupled, that is, only processes associated with arising either from the catalyst itself or from the [Ru(bpy)3]3þ
the loss of one or more protons will display a pH-dependent oxidant. This constitutes the source of CO and explains the
behavior. The Pourbaix diagram of complex 16 showed that conversion of complex 18 into 19. These results imply that
all three redox couples, RuIII/RuII, RuIV/RuIII, and RuV/RuIV, the generated complex 19 is not active in H2O oxidation and
were pH-dependent with slopes of 59 mV per pH unit to affirm this, 19 was synthesized separately. Several at-
(Figure 7). This suggests that the imidazole unit is involved in tempts were performed to utilize complex 19 for H2O
the redox processes and can participate as a proton mediator. oxidation, but none produced detectable amounts of O2.
The amide bond is one of the most, if not the most, To elucidate the fundamental difference in reactivity
essential bonds occurring in biological systems. It represents between complexes 18 and 19, the Pourbaix diagrams were
the fundamental backbone in peptides, enzymes, and a vast constructed (Figure 9). The Pourbaix diagram for 18 revealed
array of natural products. Although transition metal com- that H2O coordinates to the low-valent ruthenium(II) center
plexes containing amines (-NR3) or amides (-NR2) are well as a seventh ligand, due to the large bite angle (115°)
explored, complexes containing N-amidato (deprotonated offered by the ligand. A key feature observed from these

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FIGURE 8. Structures of the active ruthenium-based WOC 18 and the

inactive complex 19. FIGURE 9. Pourbaix diagrams of (a) complex 18 and (b) complex 19 in
the range 1.5 < pH < 8.0 (pKa values are denoted by the vertical dashed
lines). Reprinted with permission from ref 28. Copyright 2013
electrochemical measurements is that catalytic H2O oxida- WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
tion occurs after the RuIV f RuVI oxidation, suggesting that
the RuVI oxidation state initiates O2 evolution. This is Early work in our laboratories focused on systems based
exceptional and differs from a majority of reported sin- on corroles, which are naturally occurring macrocylic ligands
gle-site ruthenium-based WOCs, in which the catalysts and known to stabilize the coordinated metal centers
usually reach the ruthenium(V) state, which has enough in high-valent oxidation states. We therefore decided to
power to mediate H2O oxidation. Several attempts to synthesize the mono- and bis-manganese corroles 20 and
detect this high-valent RuVI species by MS were made 21 (Figure 10).34 In 21, the two corrole units are situated in a
without any success, probably due to the high reactivity face-to-face manner, which keeps the two metal centers in a
of this ruthenium species. The Pourbaix diagram for the CO- close and rigid environment that is beneficial in stabilizing
containing complex 19 shows that the complex only the metals in high-valent states. The xanthene moiety was
reaches the ruthenium(V) state. The observed diverse cat- employed as the bridge between the two corrole moieties
alytic activity toward H2O oxidation for the two ruthenium since it offered more flexibility compared with the often
complexes might be ascribed to the fact that it is essential employed aryl bridge. In the monocorrole complex 20, the
for the catalyst to reach the ruthenium(VI) state, in order to xanthene unit could participate by coordinating an aqua
enable H2O oxidation. ligand to the metal center through hydrogen bonding.
Manganese-Based Water Oxidation Catalysts. Special Electrochemical measurements of the two corrole com-
attention has been devoted to developing catalysts based plexes verified that high-valent oxidation states could be
upon earth-abundant metals, in particular manganese, due reached at relatively low potentials. The bis-corrole com-
to its low cost and biomimetic nature. Although a variety of plex 21 also showed that there existed an intramolecular
molecular manganese complexes have been prepared to interaction between the two manganese centers. These
mimic the structural motif of the natural system,29,30 only a intriguing properties encouraged us to examine the possibi-
handful of them have been reported to evolve O2.3133 lity of mediating H2O oxidation with the developed

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FIGURE 10. Molecular structures of manganese-based water oxidation catalysts.

SCHEME 1. Plausible Mechanistic Cycle for O2 Evolution by Manganese Corrole Complex 22

manganese corrole complexes. The catalytic activities of the mechanism, it was decided to prepare the related manga-
two complexes were studied by electrochemistry. Upon nese corrole complex 22 which had the possibility of form-
scanning to anodic potentials (E > 0.8 V vs. Ag/Agþ), a ing a stable MnVdO species.36 The addition of the oxidant
reduction peak appeared at 1.29 V for both complexes, t-BuOOH generated the MnVdO, and the subsequent addition
which could be assigned to the reduction of O2. This study of (n-Bu)4NOH triggered rapid O2 evolution, as verified by
proved that manganese complexes could be used for H2O real-time MS measurements. The catalytic intermediates
oxidation and that the formation of high-valent manganese responsible for the O2 formation could be observed by the
at low redox potentials could be the key feature in the combined use of electronic absorption spectra and high-
developed complexes. resolution MS. The assumed mechanism by which H2O is
Density functional theory (DFT) calculations suggested oxidized is depicted in Scheme 1 and begins with generation
that O2 formation from complexes 20 and 21 occurred via of the high-valent MnVdO species 23. This is subseq-
nucleophilic addition of H2O (or OH) to a MnVdO uently attacked by hydroxide to afford a manganese(III)-
intermediate.35 To obtain experimental evidence for this hydroperoxy intermediate (24). Further oxidation results in the

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FIGURE 11. Molecular structures of ligand 26 and the dinuclear Mn2II,III

complex 27.

MnIV-hydroperoxy, which after loss of a proton gave inter-

mediate 25. Intermediate 25 may disproportionate with
liberation of O2 or be further oxidized to the MnV state, from
which O2 is released to regenerate the starting complex 22. FIGURE 12. Crystal structure of the tetranuclear manganese complex
generated from complex 27, with ellipsoids displayed at 50%
This work proved that nucleophilic attack of hydroxide on a
probability level. Adapted with permission from ref 37. Copyright 2011
MnVdO intermediate is a viable mechanism for the genera- WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
tion of O2 from H2O.
As previously described, the manganese moiety in 11 acceptor. However, with [Ru(bpy)3](PF6)2 as photosensitizer
was capable of delivering three electrons to the photogen- only a single turnover could be achieved. Replacing
erated ruthenium(III) center. A fourth ET would certainly [Ru(bpy)3](PF6)2, with [Ru(bpy)2(deeb)](PF6)2, which generates
have produced a species with enough power to oxidize a higher oxidation potential and a higher thermodynamic
H2O to O2, but instead probably resulted in decomposition driving force, allowed for four catalytic turnovers.
of the dinuclear manganese moiety due to the labile With several of the previously reported manganese-
benzylic amines in the ligand. By replacing the benzylic based WOCs, inconclusive evidence exists regarding the
amines with more robust functional groups, we aimed to source of the oxygens in the generated O2. To ensure that
increase the stability of the ligand and the corresponding both oxygen atoms in the generated O2 originate from H2O,
manganese complex. It was projected that ligand 26 would experiments were conducted with 18O-labeled H2O (18OH2).
accommodate all the necessary features to generate a The ratio of 16,18O2/16,16O2 was found to be in agreement
proper environment for manganese that would result in with the theoretical value when both oxygen atoms are
an active WOC; replacing the benzylic amines with imida- derived from H2O, confirming that H2O is the source of the
zoles would generate a more oxidatively stable ligand and evolved O2. Although extensive effort has been dedicated
the inclusion of carboxylate functions would promote the into developing manganese-based complexes capable of
lowering of the redox potential of the complex. With ligand mediating the four-electron oxidation of H2O, this has gen-
26, the dinuclear manganese(II,III) complex 27 was obtained erally resulted in decomposition of the complexes or forma-
(Figure 11), which in the solid state shows a tetranuclear tion of heterogeneous manganese oxides as the active
manganese core (Figure 12), resembling the active site of catalysts (for in depth discussions, see refs 38 and 39). Our
the OEC.37 study revealed that the ligand environment afforded by
The catalytic activity was first assessed with the mild ligand 26 provided a stabilizing surrounding for the manga-
chemical oxidant [Ru(bpy)3]3þ (E° = 1.26 V vs. NHE). When nese centers to allow for catalytic H2O oxidation by use of
a deoxygenated buffered aqueous solution containing the the mild single-electron oxidant [Ru(bpy)3]3þ, both chemi-
dinuclear complex 27 was added to the single-electron cally and photochemically generated. This seems to be the
oxidant, O2 evolution was immediately detected. After ap- first example of a homogeneous manganese-based catalyst
proximately 1 h, the O2 evolution had ceased, giving a TON capable of promoting catalytic H2O oxidation with one-
of ∼25 and an initial TOF of ∼0.027 s1. It was also of electron oxidants, although the involvement of active metal
interest to test whether complex 27 displayed activity in nanoparticles cannot be ruled out.38,39
photodriven H2O oxidation under neutral conditions.
The photocatalytic setup consisted of [Ru(bpy)3](PF6)2 or Conclusions and Future Prospects
[Ru(bpy)2(deeb)](PF6)2 (deeb = diethyl 2,20 -bipyridine-4,40 - The conversion of H2O into solar fuels holds enormous
dicarboxylate) as photosensitizers and persulfate as electron potential, and here Nature provides us with an excellent

J ’ ACCOUNTS OF CHEMICAL RESEARCH ’ 000–000 ’ XXXX ’ Vol. XXX, No. XX

 €rka
Artificial Photosynthesis Ka €s et al.

example of how to achieve this. Mimicking the photosyn- 4 Alstrum-Acevedo, J. H.; Brennaman, M. K.; Meyer, T. J. Chemical Approaches to Artificial
Photosynthesis. Inorg. Chem. 2005, 44, 6802–6827.
thetic machinery constitutes a central scientific challenge in
5 Dau, H.; Zaharieva, I. Principles, Efficiency, and Blueprint Character of Solar-Energy
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resulted in several biomimetically inspired catalysts, both 9 Sun, L.; Hammarstr€om, L.; Norrby, T.; Berglund, H.; Davydov, R.; Andersson, M.; B€orje, A.;
Korall, P.; Philouze, C.; Almgren, M.; Styring, S.; Åkermark, B. Intramolecular Electron
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10 Abrahamsson, M. L. A.; Berglund Baudin, H.; Tran, A.; Philouze, C.; Berg, K. E.; Raymond-
There still exist several difficulties to be overcome before a Johansson, M. K.; Sun, L.; Åkermark, B.; Styring, S.; Hammarstr€om, L. Ruthenium-
viable artificial system for production of solar fuels can be Manganese Complexes for Artificial Photosynthesis: Factors Controlling Intramolecular Electron
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realized. But every small finding that is made brings us one 11 Magnuson, A.; Berglund, H.; Korall, P.; Hammarstr€om, L.; Åkermark, B.; Styring, S.; Sun, L.
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12 Magnuson, A.; Frapart, Y.; Abrahamsson, M.; Horner, O.; Åkermark, B.; Sun, L.; Girerd,
We would like to thank all present and past co-workers for their J.-J.; Hammarstr€om, L.; Styring, S. A Biomimetic Model System for the Water Oxidizing
contributions. Financial support from the Swedish Energy Agency Triad in Photosystem II. J. Am. Chem. Soc. 1999, 121, 89–96.
13 Sun, L.; Raymond, M. K.; Magnuson, A.; LeGourrierec, D.; Tamm, M.; Abrahamsson, M.;
and the Knut and Alice Wallenberg Foundation is gratefully Kenez, P. H.; Martensson, J.; Stenhagen, G.; Hammarstr€om, L.; Styring, S.; Åkermark, B.
acknowledged. Towards an Artificial Model for Photosystem II: A Manganese(II,II) Dimer Covalently Linked to
Ruthenium(II) Tris-Bipyridine via a Tyrosine Derivative. J. Inorg. Biochem. 2000, 78, 15–22.
14 Huang, P.; Magnuson, A.; Lomoth, R.; Abrahamsson, M.; Tamm, M.; Sun, L.; van
Rotterdam, B.; Park, J.; Hammarstr€om, L.; Å kermark, B.; Styring, S. Photo-Induced
BIOGRAPHICAL INFORMATION Oxidation of a Dinuclear Mn2II,II Complex to the Mn2III,IV State by Inter- and Intramolecular
Electron Transfer to Ru Tris-Bipyridine. J. Inorg. Biochem. 2002, 91, 159–172.
Markus D. Ka € rka
€ s received his Ph.D. degree in 2013 in organic
15 Burdinski, D.; Wieghardt, K.; Steenken, S. Intramolecular Electron Transfer from Mn or
chemistry at Stockholm University. As a graduate student, Markus Ligand Phenolate to Photochemically Generated RuIII in Multinuclear Ru/Mn Complexes.
€rn Åkermark on the develop-
carried out research with Professor Bjo Laser Flash Photolysis and EPR Studies on Photosystem II Models. J. Am. Chem. Soc.
1999, 121, 10781–10787.
ment and mechanistic insight of artificial water oxidation catalysts.
16 Xu, Y.; Eilers, G.; Borgstr€om, M.; Pan, J.; Abrahamsson, M.; Magnuson, A.; Lomoth, R.;
Eric V. Johnston received his Ph.D. degree in 2012 in organic Bergquist, J.; Polívka, T.; Sun, L.; Sundstr€om, V.; Styring, S.; Hammarstr€om, L.; Åkermark,
chemistry at Stockholm University under the supervision of Pro- B. Synthesis and Characterization of Dinuclear Ruthenium Complexes Covalently Linked to
RuII Tris-Bipyridine: An Approach to Mimics of the Donor Side of Photosystem II. Chem.;
€ckvall and Bjo
fessors Jan-Erling Ba €rn Åkermark. During his Ph.D., Eur. J. 2005, 11, 7305–7314.
he worked on several different projects, mainly in the area of 17 Conception, J. J.; Jurss, J. W.; Brennaman, M. K.; Hoertz, P. G.; Patrocinio, A. O. T.; Iha,
catalytic oxidations and artificial photosynthesis. N. Y. M.; Templeton, J. L.; Meyer, T. J . Making Oxygen with Ruthenium Complexes. Acc.
Chem. Res. 2009, 42, 1954–1965.
Oscar Verho is a graduate student in organic chemistry at 18 Li, L.; Duan, L.; Xu, Y.; Gorlov, M.; Hagfeldt, A.; Sun, L. A Photoelectrochemical Device for
Stockholm University working with transition metal catalysis under Visible Light Driven Water Splitting by a Molecular Ruthenium Catalyst Assembled on Dye-
Sensitized Nanostructured TiO2. Chem. Commun. 2010, 46, 7307–7309.
€ckvall.
the supervision of Professor Jan-Erling Ba
19 Weinberg, D. R.; Gagliardi, C. J.; Hull, J. F.; Fecenko Murphy, C.; Kent, C. A.; Westlake,
Bjo€ rn Åkermark is Professor at Stockholm University. During B. C.; Paul, A.; Ess, D. H.; Granville McCafferty, D.; Meyer, T. J. Proton-Coupled Electron
many years, his research has been focused on sustainable energy Transfer. Chem. Rev. 2012, 112, 4016–4093.
€ Zou,
20 Lee, B.-L.; K€ark€as, M. D.; Johnston, E. V.; Inge, A. K.; Tran, L.-H.; Xu, Y.; Hansson, O.;
conversion. He has been studying and developing supramolecular X.; Åkermark, B. Synthesis and Characterization of Oligonuclear Ru, Co and Cu Oxidation
assemblies for charge separation, iron hydrogenases for produc- Catalysts. Eur. J. Inorg. Chem. 2010, 5462–5470.
tion of hydrogen, and artificial water oxidation catalysts. 21 Norrby, T.; B€orje, A.; Hammarstr€om, L.; Alsins, J.; Lashgari, K.; Norrestam, R.; Martensson,
J.; Stenhagen, G.; Åkermark, B. Synthesis, Structure, and Photophysical Properties of Novel
Ruthenium(II) Carboxypyridine Type Complexes. Inorg. Chem. 1997, 36, 5850–5858.
FOOTNOTES 22 Xu, Y.; Åkermark, T.; Gyollai, V.; Zou, D.; Eriksson, L.; Duan, L.; Zhang, R.; Åkermark, B.;
*Corresponding Author. E-mail: [email protected]. Sun, L. A New Dinuclear Ruthenium Complex as an Efficient Water Oxidation Catalyst. Inorg.
The authors declare no competing financial interest. Chem. 2009, 48, 2717–2719.
23 Xu, Y.; Duan, L.; Tong, L.; Åkermark, B.; Sun, L. Visible Light-Driven Water Oxidation
Catalyzed by a Highly Efficient Dinuclear Ruthenium Complex. Chem. Commun. 2010, 46,
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