Artificial Photosynthesis: Learning from NatureDong Ryeol Whang* and Dogukan Hazar Apaydin[a]

ChemPhotoChem 2018, 2, 148 – 160 T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim148

ReviewsDOI: 10.1002/cptc.201700163

1. Introduction

Photosynthetic autotrophs have been converting photon

energy to chemical energy for 3.4 billion years; some of the

converted energy was deposited on earth as forms of fossilfuels. Currently, human beings are consuming 13 TW of energy,

in which 81 % is based on combustion of fossil fuels.[1] Alongwith the fast depletion of fossil fuels, the use of carbon-based

fuels inevitably produces air pollution and greenhouse gases.To solve this conflict between energy demand and ecological

issues, sustainable and clean technologies for energy produc-

tion are required. Sun provides 171 000 TW energy on the sur-face of the earth, thus utilizing only 0.01 % of it will be just

enough to meet the whole need of energy by human beings.In this context, developing a system which can convert the

photon energy to chemical energy is of great importance forthe solar flux utilization.

Natural photosynthesis utilizes solar energy to convert water

and/or carbon dioxide into higher energy components such ascarbohydrates. Artificial photosynthesis replicates the photo-

chemical process of natural photosynthesis, however, it ismore dedicated to the production of useful fuels or valuable

chemicals such as molecular hydrogen (H2), methane, metha-nol, etc. The first idea of artificial photosynthesis dates back tothe beginning of 1900s when Giacomo Ciamician commented

in his paper that human should shift from consuming fossilfuels to generating sustainable energy from the sun.[2] The first

experimental demonstration of light-driven water splitting wasso called “Honda–Fujishima effect”.[3, 4] The photoelectrochemi-cal cell (PEC) was composed of TiO2 photoanode and platinumblack cathode. By illumination of the photoanode (l>400 nm),

O2 and H2 were generated at the photoanode and cathode, re-spectively. The same group reported a photocatalytic CO2 re-duction with aqueous suspension of various semiconductor

particles.[5] Since the pioneering works by Honda and Fujishi-ma, enormous efforts have been made in pursuit of efficient,

stable and cost-effective artificial photosystems for water split-

ting and CO2 reduction.[6–49]

Nature has developed several strategies to run the photo-

chemical processes of photosynthesis in an efficient and

robust way: i) accumulative charge transfer to run the multi-electron process of product production efficiently, ii) photopro-

tection to prevent the system from being damaged by excessphoton flux, and iii) self-healing to repair or replace damaged

proteins prolong the activity of whole system. Those strategieshave been developed to balance the maximum efficiency and

sustainability upon fluctuating environmental conditions. Thus,

closely mimicking these nature’s strategies is a challenging butpromising approach to realize the efficient and stable artificial

photosynthesis in real life application. This approach has re-ceived recent attention, and many research groups are current-

ly developing molecular components which mimic the naturalphotosystem for solar fuel production.

In this contribution, we would illustrate recent progresses

on molecular systems for artificial photosynthesis by mimickingthe nature’s strategies. There is another research area of biohy-

brid systems directly using the part of nature, i.e. , bacteria orenzymes, which will not be discussed in this paper.

2. Overview of Photosystem II (PSII)

Production of organic matter and maintenance of most formsof life on Earth is maintained by oxygenic photosynthesis pro-

cess. This process converts light energy from sun into chemicalenergy, which is stored as highly reduced organic compounds.Two main photosynthetic reaction centers (RC) namely, photo-system I (PSI) and PSII, are responsible for linear electron trans-

port in oxygenic photosynthesis. In early 20th century Emersonand Arnold reported that hundreds of chlorophyll (Chl) mole-cules operated together to produce one oxygen molecule.[50]

This network of Chl molecules, which supplied excitationenergy to photochemical catalytic center, was later on named

as “photosynthetic unit”. In 1960 Hill and Bendall proposedthat a two-pigment system worked in series in order to realize

oxygenic photosynthesis where short-wavelength reaction and

a long wavelength reaction take place.[51] This hypothesis ofHill and Bendall, called zigzag model or “Z-Scheme” was exper-

imentally proved by several studies in 1961 and the terms PSIand PSII were coined. PSII, which is a multi-subunit membrane

protein that has the unique ability to extract electrons fromwater to result in molecular oxygen (O2) upon reduction of

Artificial photosynthesis has been devised and investigated inpursuit of solving the 21st century’s energy problem. Despite

significant advances in recent decades, applying the technolo-gy in real life is still a challenging subject for scientists. As the

term “artificial photosynthesis” stems from mimicking naturalphotosynthesis, we can learn from nature’s strategies whichhave evolved over 3.4 billion years. This Review highlights im-

portant strategies of natural photosynthesis which can be bor-rowed for highly efficient and robust artificial photosystems for

solar fuel production. Starting with a brief description of pho-tosystem II in natural photosynthetic autotrophs, three relevant

bioinspired strategies are discussed in this article: i) accumula-tive charge transfer, ii) photoprotection, and iii) self-healing.

Next, development of artificial photosystems mimicking thosestrategies will be discussed. Finally, remaining challenges and

perspectives for future development of artificial photosynthesis

are described.

[a] Dr. D. R. Whang, D. H. ApaydinInstitute of Physical ChemistryJohannes Kepler University LinzAltenbergerstraße 69, 4040 Linz (Austria)E-mail : patrick.whang@jku.at

The ORCID identification number(s) for the author(s) of this article canbe found under: https://doi.org/10.1002/cptc.201700163.

An invited contribution to a Special Issue on Artificial Photosynthesis.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim149

Reviews

plastoquinone. PSII constitutes at least 25 different proteinsubunits many of which are bound to the thylakoid mem-

brane.[52, 53] However, minimal reaction center responsible forO2 evolution has fewer members.

The most important constituents of the minimal reactioncenter of PSII are proteins D1, D2, a and b subunits of Cyt b559

and PsbI subunit. This assembly of five is responsible for thecharge separation.[53] Among these D1 and D2 are of great im-portance. D1 and D2 are responsible for keeping all cofactors

in a specific position so that the reactions can proceed in theright order.[54] The process starts with capturing of light energyby pigments within the antenna system. Then the energy istransferred to the Cholorophylls (Chls) that involves the pri-

mary electron donor, P680, to generate an excited singletstate, P680*. Excited state relaxes back by reducing a nearby

Pheophytin (Pheo), a molecule similar to Chl in structure but

missing the central Mg ion, forming the primary radical pairP680+Pheo@ . Reduced Pheophytin, Pheo@ , then oxidized back

to Pheo by giving an electron to the primary plastoquinoneelectron acceptor, QA, attached to the D2 protein. The electron

is then transferred to the secondary plastoquinone electron ac-ceptor, QB, bound to D1. QB is then reduced once more and

gets protonated to yield the plastoquinol, QBH2. After leaving

the PSII system, this molecule is replaced by an oxidized plas-toquinone molecule from a pool of plastoquinone molecules

located in the lipid bilayer. P680+ , the oxidized primary donor,is reduced by a redox-active tyrosine residue, Tyr 161 of the D1

protein. Tyr 161 is afterwards reduced by the Mn4Ca cluster, co-

ordinated by aspartate, glutamate, and histidine residues inthe D1 protein, including the C-terminus of mature D1, and by

residual glutamate of CP43. The Mn4Ca cluster exists in five dis-tinct oxidation or S states termed S0-S4, where the subscript in-

dicates the number of accumulated oxidizing equivalents. Onemolecule of oxygen occurs from two moles of water after for-

mation of the S4 state, resetting the enzyme to the S0 state,and so occurs with a periodicity of four.

3. Accumulative Charge Transfer

Water splitting and CO2 reduction are multi-electron processes(Scheme 1), which implies that multiple electrons should be ac-

cumulated at the catalytic center to run the photochemical

cycles. Even for the simplest processes for H2 production or COformation, it requires two electrons accumulated to a catalyst.

It should be noted that in general, photon absorption is a

monoelectronic process, results in single charge separation. Inthis context, it is required to accumulate multiple electrons or

holes with several rounds of successive single photon absorp-tion before charge recombination occurs.

In PSII apparatus, multiple rounds of single electronic ab-sorption are successfully coupled with extraction of four elec-

trons from the Mn4Ca cluster to run water oxidation. The

mechanism of water oxidation by PSII has been extensively in-vestigated so far.[55–57] Schematic representation of the key co-

factors in PSII is shown in Figure 1 a. The photolytic cycle startswith light absorption of the chlorophyll pigment (P680) to

form a photoexcited state (P680*), followed by charge separa-

Dong Ryeol Whang received a PhD in

materials science and engineering

from Seoul National University in 2014.

Dr. Whang is currently an assistant pro-

fessor at Johannes Kepler University

Linz, Austria. His research expertise

and interests lie in the areas of artificial

photosynthesis for solar fuel produc-

tion. His research interests include cat-

alysis for energy (fuel and chemicals)

production combined with fine ligand

synthesis, organometallic synthesis,

density functional theory (DFT) based quantum chemical calcula-

tions, steady and time-resolved spectroscopy, and analytical

chemistry.

Dogukan H. Apaydin obtained his BSc.

degree in chemistry (2010) from Istan-

bul Technical University and his MSc.

degree in polymer science and tech-

nology (2012) from Middle East Techni-

cal University in Turkey. Currently he is

a PhD student/teaching assistant at

Johannes Kepler University Linz in Aus-

tria focusing on (photo)electrochemi-

cal catalysis and electrochemical

carbon capture.

Scheme 1. Electron equivalents for water splitting and CO2 reduction pro-cesses.

Figure 1. a) Arrangement of cofactors in PSII ; b) S-states for the formation ofO2 proposed by Kok and co-workers. Reproduced with permission fromRef. [55] . Copyright (2007) Elsevier B. V.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim150

Reviews

tion to generate radical cation (P680+). The hole can furtherbe transferred to multi-electron-donor of tetramanganese clus-

ter (CaMn4) through tyrosine (YZ) as a charge transfer mediator.It had been generally accepted that sequential extraction of

four electrons from CaMn4 is responsible for the catalytic cyclefor water oxidation (Figure 1 b).[58, 59] Five-step reaction ofCaMn4, denoted as S0 through S4, can be realized upon consec-utive charge transfer, where S0 is the ground state and S4 isthe four electron oxidized state. The S4 state of CaMn4 is quiteunstable and rapidly reacts with water to produce O2.

3.1. Accumulation of Electrons

Wasielewski and co-workers first reported an accumulation of

two electrons in a donor-acceptor-donor triad where two free-base porphyrin donors are attached to a two-electron acceptor

of N,N’-diphenyl-3,4,9,10-perylenebis(dicarboximide) (PBDCI)

unit (Figure 2 a).[60] Upon flash photolysis of the porphyrin units

with high laser intensities (up to 20 photons/molecule), the

PBDCI unit was doubly reduced to give PBDCI2@ and two holes

were stored in each porphyrin unites; only single charge sepa-ration was observed with low laser intensities (<50 photons/molecule). Imahori and co-workers reported a similar systemwhere tetracyanoanthraquinodimethane (TCAQ) and zinc por-

phyrin were employed as acceptor and units, respectively (Fig-ure 2 b).[61] Formation of doubly reduced TCAQ was successfully

demonstrated using double pulse technique i) first pulse of532 nm laser was used to photogenerate the single chargeseparated state and ii) second pulse was delayed by 233 ps

and set to 555 nm to selectively photoexcite the unexcitedporphyrin units. Due to the distinct optical properties of

singly- and doubly-reduced acceptor units, possible applicationof this molecular system as an optical switch was proposed in-

stead of artificial photosynthesis. However, pioneered by these

works, several examples of accumulative electron transfer inmolecular systems aiming on the multiple electrons utilization

in artificial photosynthesis.[62–66]

A first principle for the accumulative electron transfer in APS

is to store multiple electrons in one molecule to run the cata-lytic cycles. Molecular electron-reservoirs are compounds,

which can store and transfer multi-electrons stoichiometricallyor catalytically without decomposition or side reaction.[67–70]

However, the electron reservoir property in organometalliccompounds is restricted to some classes of compounds that

can withstand multiple redox changes without molecular dis-ruption. Especially for the transition metal complexes, it has

been noted that the population of d orbital upon photoexcita-tion or multiple reduction is a main reason of the degradation

of organometallic complexes. Electron reservoirs can be de-

signed with following strategies: i) the population of d orbitalcan be prevented if the orbitals affected by the electron addi-

tion are delocalized over an extended ligand framework, and ii)tethering multiple electron acceptors which can store and sta-

bilize excessive electrons in each electron reserving units.The Park group recently reported a PtII water reduction cata-

lyst (WRC) using the electron reservoir strategies.[71] Specially

designed tetraphenylsilane (TPS) substituent was introduced toa diimine ligand of a molecular PtII WRC (TPSPtCl2 in Figure 3).

TPS has a tetrahedral configuration where four phenyl ringsare attached to a central Si atom. The extended p-systems

enable delocalization of excess electrons over the ligands, thusimprove electron-reservoir character of the PtII WRC. Electro-

chemical study and density functional theory (DFT) based

quantum chemical approach revealed that TPS groups inTPSPtCl2 create electron-reservoir characteristics and dramati-

cally enhanced electrochemical stability upon two-electron re-duction. A turnover number of 510 000 was recorded for pho-

tocatalytic water reduction, which represents a large improve-ment over the control complexes that do not contain the TPS

substituents.

Sakai and co-workers reported a series of PtII WRCs whichcontains pyridinium or methyl viologen moieties as electron

storing moieties. A simple PtII terpyridyl complex with a methylpyridinium periphery, namely PV2+ , was synthesized and

tested for light-driven H2 production in combination with eth-ylenediaminetetraacetic acid (EDTA, YH2

2@) as a sacrificial elec-

tron donor (Figure 4 a).[72, 73] It was found that PV2 + formed a

doubly-reduced species PV0 by two consecutive photoinducedelectron transfer (PET) steps, namely: [PV2 + ···YH2

2@] + hn ![PV2 +*···YH2

2@] ! PV+ C + YH2@ , and [PV+ C···YH2

2@] + hn ![PV+ C*···YH2

2@] ! PV0 + YH2@ . This molecular system well

mimics the Z-Scheme, although the two reductive quenching

Figure 2. Chemical structures of a) PBDCI and b) TCAQ-Zn porphyrins.

Figure 3. Chemical structure of TPSPtCl2.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim151

Reviews

processes do not perfectly match with the oxidative ones innatural photosynthesis (Figure 4 b). As a result, PV2++ recorded

a TON of 4.1 after 12 h of photoirradiation, which is ca. 10times larger than that of [Pt(tpy)Cl]+ (TON = 0.4).

Another class of PtII polypyridine derivatives with viologen

units was reported by the same research group (Figure 5 a).The catalytic activity of the complex was enhanced by tether-

ing viologen units as electron acceptors, which can temporarilycollect the high-energy electrons generated during the photo-

induced steps. In the case of the viologen-containing com-plexes, the ground state of the photosensitizing site, i.e. ,

PtCl2(bpy) was immediately regenerated from its reduced form

after the first PET step, thus restoring the light absorption abili-ty (Figure 5 b).As a result, the PtII bipyridyl complex with four

viologen periphery, [PtCl2(5,5’-MV4)]8 ++ , recorded one order of

magnitude higher TON of 27 after 12 h of photolysis comparedto PV2 ++ .[74] Further series study was carried out and TONs of 35

and 25.2 were recorded with a PtII bipyridyl complex[75] and aPtII terpyridyl complex,[76] respectively. With the same strategy,

RuII-based photosensitizers with peripheral methyl viologenunits were designed to store and transfer multiple electrons to

colloidal Pt WRC. Storing up to 8 electrons in a single photo-sensitizer was achieved by tethering 12 methyl viologen unitsto a [RuII(bpy)3]2 + center.[77, 78]

The Brewer group reported a series of trinuclear complexeswith a molecular structure of [(TL2RuIIBL)2MIIIX2]5+ (TL = terminalligand, BL = bridging ligand, M = Ir or Rh, and X = halogenligand).[79–81] Two photosensitizing RuII units were bridged to

the central electron accepting units to direct the accumulationof electrons. While IrIII center can store two electrons in its li-

gands without affecting the oxidation state of the metal

center, RhIII-based complexes undergo metal-centered reduc-tion to form RhII species upon one electron reduction. Then

RhII intermediate disproportionates to form RhIII and RhI specieswith loss of the two chloride ligands. The free coordination

site of RhI then opens a possibility for substrates such asproton to anchor to form metal-hydride, followed by H2 pro-

duction. Several RhIII-based trinuclear complexes were subject-

ed to photocatalytic H2 production[82–85] and TON of 1300 wasrecorded with [((Ph2 phen)2Ru(dpp))2RhBr2]5 ++ (Ph2phen = 4,7-

diphenyl-1,10-phenanthroline and dpp = 2,3-bis(2-pyridyl)pyra-zine, Figure 6 a) in combination with N,N’-dimethylaniline

(DMA) as a sacrificial electron donor.[85] Recently, Collomb andco-workers developed a trinuclear complex Ru2Rh, where two

RuII photosensitizing units are linked to the RhIII center with a

bridging ligand of 1,2-bis[4-(4’-methyl-2,2’-bipyridinyl)]ethane(Figure 6 b).[86] Non-conjugated ligand was used to minimize

the electronic coupling between the photosensitizing and elec-tron accepting units thus maintain the original physical proper-

Figure 4. Chemical structure of a) PtII WRCs and b) Z-Scheme of PV2 ++ . Repro-duced with permission from Ref. [76] . Copyright (2016) The Royal Society ofChemistry.

Figure 5. Chemical structures of a) Pt-MVs and b) charge transfer scheme.Reproduced with permission from Ref. [76] . Copyright (2016) The Royal Soci-ety of Chemistry.

Figure 6. Chemical structures of a) non-bridged and b) bridged RuII–RhIII–RuII

supramolecular complexes.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim152

Reviews

ties of parent molecules, i.e. , [RuII(bpy)3]2 + and [RhIII(bpy)2Cl2]+ .The authors highlighted a high TON of 430 in pure aqueous

system, however, it has been noted that the photocatalytic ac-tivities of the polynuclear systems have been rather low com-

pared to those of multi-component systems.[87]

3.2. Accumulation of Holes

Tetramanganese cluster is responsible for the accumulation of

four holes for O2 evolution from water in PSII, vide supra. Withthis in mind, several photosensitizer/donor or photosensitizer-donor systems have been made to mimic the charge accumu-lation, where the donors are based on mono- or polynuclear

manganese complexes. Styring and co-workers reported eitherinter- and intra-molecular accumulation of holes in dinuclearMn2

II,II unit in combination with RuII polypyridine moiety as a

photosensitizer (Figure 7 a).[88–90] In the presence of pentaammi-nechlorocobaltIII chloride as an electron acceptor, photoexcita-

tion of RuII center resulted in a stepwise extraction of two elec-trons from the Mn2

II,II. EPR spectroscopy revealed continuous

formation of CoII species and Mn2III,IV species, indicating that

three holes were accumulated in the dinuclear manganesemoiety (Figure 7 b).[88] Collomb and Deronzier et al. reported

similar systems where three RuII tris(bipyridine) complexes aretethered to a MnII tris(bipyridine) center.[91, 92] It was proposed

in these studies that upon one electron reduction of the MnII

center, the manganese complex were decomposed and irrever-

sibly transformed into corresponding di-m-oxo bridged Mn2III,IV

dimeric species (Figure 7 c). Despite the presence of MnII-basedunits, those systems did not show any catalytic activity of O2

production from water.Recently, dye-sensitized inorganic/organic hybrid systems

have been proposed to be an alternative approach for facilitat-ing accumulative charge transfer in molecular systems. Inor-

ganic nanocrystals such as TiO2 nanocrystals can utilized as anelectron/hole reservoir. Therefore, hybridizing them with or-

ganic/organometallic dyes offers multiple charge separationafter several rounds of single photon excitation. The Hammer-

strçm group reported a series of inorganic/organometallichybrid systems where RuII-polypyridine photosensitizers with

oligotriarylamine (OTA) donors are linked to TiO2 nanoparticlesas an acceptor.[93, 94] Careful and intensive study in combinationwith double pulse experiments showed efficient accumulative

electron transfer resulting in the formation of two-electron oxi-dized state of the OTA unit upon successive excitation by twophotons. Among the systems studied, one with OTARu dyeanchored onto nanocrystalline TiO2 (Figure 8) showed efficient

accumulative electron transfer upon successive photoexciationwith double pulse experiments. Once the RuII photosensitizer

was photoexcited by first excitation pulse, the exciton was in-

Figure 8. Chemical structure of OTARu. Reproduced with permission fromRef. [93] . Copyright (2010) American Chemical Society.

Figure 7. a) Schematic of chemical reaction sensitized by RuII(bpy). b) Decrease of Mn2II,II and increase of Mn2

III,IV signal amplitude as a function of number offlashes. c) Process of formation of di-m-oxo dimeric species. Reproduced with permission from Refs. [88] and [92] . Copyright (2002) Elsevier for Figure 7aand 7b; copyright (2006) The Royal Society of Chemistry for Figure 7c.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim153

Reviews

jected rapidly into the TiO2 nanocrystal within 1 ps to form RuIII

species. Then the ground state of RuII center was recovered by

oxidizing OTA within 1 ns regime, resulting in TiO2(@)-RuII-OTA+

state. With second photoexcitation, one more round of charge

separation occurred to yield doubly charge separated state ofTiO2

(2@)-RuII-OTA2 + . The overall yield of accumulative chargetransfer was reported as high as 100 %.

4. Photoprotection

The intensity of the solar radiation fluctuates and wheneverthe light intensity is greater than that needed to saturate thephotosynthesis, the plant or algae faces a danger of being

damaged by the excess of incoming photons. For example,when light absorption exceeds the capacity of photosystem inPSII, triplet excited state of chlorophyll (3Chl) is generated

either by intersystem crossing from its singlet excited state(1Chl) or by charge recombination of the primary radical pairs

between PSII primary donor and pheophytin (P680+/Phe@).The 3Chl is a potent sensitizer for molecular oxygen forming

singlet oxygen (1O2) which can cause oxidative damage to thepigments, lipids and proteins of the photosynthetic system. To

cope with fluctuating irradiance and prevent the cell or protein

from getting damaged, photosynthetic organisms haveevolved several photoprotective mechanisms: i) adjustment of

light-harvesting antenna size, ii) thermal dissipation of excessabsorbed light energy, and iii) scavenging reactive oxygen spe-

cies.[95–110] The regulation of excess photons thus can prolongthe lifetime of the photosynthetic apparatus. Achieving self-

regulating behavior in molecular system is a critical challenge

to prolong the artificial photosynthesis.

4.1. Adjustment of Light-Harvesting Antenna Size

One implication is that the light harvesting antennas in Chlscan rearrange in their protein matrix upon either a long term

or a short term fluctuation of light intensity.[111, 112] During long-

term acclimation to fluctuating light intensities, changes in an-tenna size are due to changes in light-harvesting chlorophyllprotein complex (LHCs gene expression[113–115] and/or LHCs

degradation.[116] In short term modulation of the antenna sizes,overexcitation of PSII results in detachment of LHCs from PSII,

thus decreases the effective size of LHCs.[117] In both cases, theoverall light absorption of photosystem can be reversibly

modulated with different light intensity.Molecular logic gate strategy can be borrowed to realize the

light-intensity dependent regulation of photochemical process-es. A molecular logic gate is a molecule that performs a logical

operation based on physical or chemical inputs. Once the logic

gate is operated by means of photons, that is, photochromicmolecule, we can modulate the photophysical properties of

the molecule thus give ways to form a photon regulator. Eitherphotoinduced intramolecular energy or electron transfer pro-

cesses have been successfully controlled by using the photo-chromic units. Effenberger and co-workers developed a D-B-Asystem with ON/OFF photoswitchable intramolecular energy

transfer by incorporation of a photochromic fulgimide be-tween anthracene and coumarin (Figure 9 a).[118] Tsuchiya re-

ported an optical control of photo-induced electron transferby incorporating two porphyrin units with a photoisomerizable

azobenzene linker (Figure 9 b).[119] Inspired by those works, sig-nificant efforts have been made on the development of artifi-

cial photoregulation systems on catalysts for chemical reac-

tions, however, most of the works have been focusing on thelight-induced activation of the catalytic processes and downre-

gulation of the catalytic activities are still scarce.[120] Althoughactual photoregulation has not been shown in those papers,

they provided a good photochemical background for usingthose systems for photoregulation in artificial photosynthesis.

The molecular logic gate concept was successfully adapted

to molecular photoregulatory system. Gust and co-workers re-ported a series of supramolecular systems which can downre-

gulate the high intensity light by activation of by using ther-mally-reversible photochromic units which can reverse the

photochemical process by thermal energy (Figure 10).[121] Inthe ground state, the dye exists in the dihydroindolazine (DHI)form (1c) which can absorb only blue lights. When 1c absorbs

light, it photoisomerizes into an open form of colored betaine(BT), depicted as 1o. Molecule 1o thermally converts back to1c with a time constant of 37 s at 25 8C. Based on this, the

Figure 9. a) Chemical structure of coumarin isomers and concept for switching intramolecular energy transfer in a molecular system.[118] b) Chemical structuresof electron-rich and electron-deficient porphyrins (upper) and process of photoswitching (lower). Reproduced with permission from Refs. [118] and [119].Copyright (1993) Elsevier B. V. for Figure 9a; copyright (1999) American Chemical Society for Figure 9b.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim154

Reviews

photoregulatory system of natural photosynthesis was success-

fully demonstrated by adjusting the absorption cross-sectionof the dye. Under low light intensity conditions, the molecule

mainly exists in a closed form (1c), and undergoes photoin-duced electron transfer from porphyrin to fullerene with a

quantum yield of 0.82; as the light intensity increases, forma-

tion of BT leads to quenching of the porphyrin excited state,reducing the quantum yield to as low as 0.27.

4.2. Carotenoids

Carotenoids are important pigments in photoregulatory

system of photosynthetic bacteria. They can either prevent the

formation of highly destructive singlet oxygen by thermal dissi-pation of 1Chl[122–129] or quenching the already produced singletoxygen to its triplet ground state.[130] In higher plants, there

are three carotenoid pigments that are active in the xantho-phyll cycle: violaxanthin, antheraxanthin, and zeaxanthin

(Figure 11). During light stress, violaxanthin is converted tozeaxanthin via the intermediate antheraxanthin, which plays a

direct photoprotective role acting as a lipid-protective anti-oxi-dant and by stimulating non-photochemical quenching within

light-harvesting proteins. Another role of carotenoids for pho-

toprotective reaction is that they can directly quench alreadygenerated singlet oxygens. Due to the low-lying triplet excited

state of the carotenoids, triplet carotene is formed as the sin-glet oxygen returns to its ground state.

The carotenoid photoprotection was successfully mimickedwith a molecular system where a carotenoid moiety was cova-

lently bonded to a porphyrin (Figure 12 a).[131] Bleaching of di-

phenylisobenzofuran (DPBF), which is vulnerable to singleoxygen, upon irradiating the aerated solution of the dyes were

investigated. If the solution contains only a tetra-arylporphyrinsensitizer in addition to DPBF, singlet oxygen is produced

under illumination and rapidly reacts with DPBF, resulting inthe fast bleaching of the dye. In the presence of the dyes I or

II, a significant decrease in the rate of photodestruction of

DPBF was observed because of the fast quenching of the trip-let excited state of the porphyrin unit by the carotenoids, thus

prevents the O2 sensitization (Figure 12 b).

Figure 10. Chemical structure of light intensity regulating pentad. Repro-duced with permission from Ref. [121] . Copyright (2008) Nature PublishingGroup.

Figure 11. Change in chemical structure of carotenoid pigments uponchange in light intensity.

Figure 12. a) Chemical structures of carotenoporphyrin complexes. b) Bleaching of DPBF at 390 nm by singlet oxygen. Filled squares and circles are with I andII, respectively. Unfilled shapes represents multicomponent mixture of tetraarylporphyrin and b-carotene. Reproduced with permission from Ref. [131] . Copy-right (1981) Nature Publishing Group.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim155

Reviews

5. Self-Healing

5.1. D1 Protein Repair Cycle in PSII

Despite the existence of photoprotective mechanisms in PSII,photodegradation occurs even at a very low irradiance.[132–134]

Several different mechanisms have been proposed for the PSIIphotodegradation; regardless of the mechanism, it is generallyaccepted that the irreversible photodamage of D1 protein is

responsible for the photoinhibition of PSII.[98, 100, 135] Once theD1 protein in PSII is irreversibly damaged by photons, a mech-anism is activated where the damaged part of the PSII com-plex are replaced by a fresh one to restore the photochemical

activity. Such a self-healing mechanism is termed as “PSII repaircycle”. Understanding the full cycles of self-healing is still un-

derway, however, it has been assumed to consist of a number

of distinct steps shown in Figure 13.

In 2008, the Nocera group reported a preparation of CoII-

based electrocatalyst, namely Co-Pi, which is capable of per-forming water oxidation.[137] They observed deposition of thecatalyst upon the oxidative polarization of an inert indium tin

oxide (ITO) electrode in CoII ion containing phosphate buffer.The catalyst was formed in situ and operated at low overpo-tential of 280 mV. Indeed, a plausible self-healing pathway wasproposed in the paper. The catalytic system was further stud-

ied by the same group and the self-healing capability was con-firmed.[138] Leaching of cobalt was observed during the water

electrolysis, while by applying potential in the presence of aphosphate counter ion resulted in a redeposition of the cata-lyst. It was noteworthy that the phosphate electrolyte ensures

then the stability of the catalytic film, by promoting redeposi-tion of CoIII, generated from electrochemical oxidation of CoII

ions leached in solution (Figure 14). A very similar strategywith Co-Pi, MnO2 water oxidation catalyst was reported by Na-

jafpour et al.[139] Self-healing of a MnO2 electrocatalytic film in

the presence of CeIV was demonstrated.As an important step forward to artificial photosynthesis,

Nocera’s self-healing WOC was further applied for a photoa-node visible-light driven water splitting photoelectrochemical

cells (PECs). Gamelin and co-workers reported a PEC where thephotoanode was prepared by electrodepositing Co-Pi on the

surface of photo-active hematite (a-Fe2O3) instead of using ITO

as a substrate.[141–143] Under AM 1.5 solar irradiation, the PEC

showed reduction of the bias voltage (>350 mV) for watersplitting. Steinmiller and Choi reported another photoelectro-

chemical approach by photochemically depositing Co-Pi onZnO rods.[144] By irradiating UV light instead of applying exter-

nal bias, photogenerated holes in the ZnO rods were used tooxidize CoII ions to CoIII ions to precipitate the Co-based cata-

lyst onto the surface. The photodeposition method ensures

the deposition of the catalyst where the photogenerated holesare most readily available, thus provides optimal catalytic site

for catalysis. In the presence of Co-Pi, the ZnO photoelectrodeshowed reduction of onset potential by 0.23 V with enhance-

ment of anodic photocurrent observed in a wide potentialrange. In both systems by Gamelin and Choi, the leaching of

the catalytic species was ruled out due to the self-healing abili-

ty of the Co-Pi catalyst, thus prolonged the catalytic activity.Since the reports, Co-Pi has been coupled with various light-

active semiconductors to enhance the catalytic activity of aphotoanode for O2 evolution, implying the importance of self-

healing for prolonged and efficient catalysis.[145–153]

By incorporating Co-Pi with a triple junction amorphous sili-con (3jn-a-Si) photovoltaic cell and H2-evolving NiMoZn ternary

alloy, a very high efficient solar-water-splitting device, namely“artificial leaf” was constructed with a device configuration ofCo-Pi/3jn-a-Si/NiMoZn (Figure 15).[154, 155] Overall solar-to-fuelsefficiencies (SFE) of 4.7 % was recorded with the artificial leaf,

corresponds to the overall water splitting efficiency of 60 %.The Bocarsly group reported a photoelectrochemical split-

ting of water in an ambient condition using polycrystallineCuRhO2 as a photocathode.[156] It was proposed that the pres-ence of O2 in the electrolyte solution either prevents the for-

mation of metallic Cu or rapidly reacts with trace quantities ofCu to regenerate CuRhO2.

One implication on the organometallic catalysts is that theyare prone to undergo ligand dissociation in the photolysis con-

ditions. Eisenberg and co-workers showed regeneration of the

ligand-dissociated catalysts by adding free ligand that reconsti-tuted the catalyst.[157, 158] Photocatalytic H2 evolution kinetics of

a cobalt catalyst, CoIII(dmgH)2pyCl (where dmgH = dimethyl-glyoximate and py = pyridine) were compared with various

concentrations of free dmgH2 (Figure 16 a). In the absence ofthe free ligand, the H2 evolution ceased in 5 h with a turnover

Figure 13. Schematic representation of PSII repair cycle. Reproduced withpermission from Ref. [136] . Copyright (2011) The Royal Society of Chemistry.

Figure 14. Schematic representation of self-healing process in oxygen-evolv-ing CoIII catalyst. Reproduced with permission from Ref. [140]. Copyright(2009) The Royal Society of Chemistry.[140]

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim156

Reviews

number of 360, while in the presence of 12 equiv of dmgH2,the catalytic activity prolonged 12 h recording a turnovernumber of 900 (Figure 16 b). On the other hand, the addition

of free ligand sometimes deteriorates catalytic activity when ametallic catalyst was used. The Bernhard group reported aphotocatalytic H2 production using IrIII (ppy)2(bpy) (whereppy = 2-phenylpyridine and bpy = 2,2’-bipyridine) photosensi-

tizers and colloidal Pt catalyst.[159] Addition of 50 equiv free bpyligand to the system lowered the H2 production activity to40 % of its original activity instead of regenerating the IrIII pho-tosensitizer, which was attributed to poisoning of the Pt cata-lyst.

Metal-organic frameworks (MOFs) have been studied as ascaffold for incorporating photosensitizers and catalysts for

solar fuel production due to their high ordered structure, highporosity, and facile functionalization.[160–167] Park and co-workers

suggested using the MOF as a self-healing platform.[168] Aseries of UiO-67-based MOFs, namely Ptn_Ir_BuiO, comprising

2,2’-bipyridine-5,5’-dicarboxylate (L) as a self-healing site,

PtII(L)Cl2 as a H2-evolving catalyst, and IrIII(ppy)2(L) as a photo-sensitizer were synthesized and tested for photocatalytic H2

production (Figure 17). Once the Pt-diimine bond was cleavedduring HER, abundant L ligand promoted re-coordination of Pt

to its diimine site and recovered the molecular catalytic activi-ty. As a result, the catalysis prolonged more than 6.5 days,

while the control MOF system without a free diimine ligand

showed leaching of Pt to form colloids.

6. Summary and Outlook

The purpose of this Review has been to understand andbenchmark the natural photosynthetic system and describe

their incorporation into artificial photosynthesis. Towards this

end, three important and unique strategies in PS II werestated: i) accumulative charge transfer, ii) photoprotection, and

iii) self-healing. The natural photosynthetic system has beenevolved to fulfill the strategies that the active units have opti-

mal spatial positions in a protein matrix for the balance be-tween efficient charge accumulation and photoprotective op-

eration. Additionally, the damaged proteins can be replaced

through a self-healing mechanism to further prolong the pho-tosynthetic activity. Many challenges have been made as ana-

logues for each strategy for artificial photosynthesis. Successful

Figure 16. a) Chemical structure of CoIII(dmgH)2pyCl and b) turnover for H2

evolution versus irradiation time. Reproduced with permission fromRefs. [157] and [158]. Copyright (2011) American Chemical Society for Fig-ure 16a; copyright (2009) American Chemical Society for Figure 16b.

Figure 15. Device structure of “artificial leaf”. Reproduced with permissionfrom Ref. [155] . Copyright (2012) American Chemical Society.

Figure 17. a) Schematic illustration for the self-healing of Ptn_Ir_BUiO b) H2 evolution kinetic curve for Ptn_Ir_BUiO. Inset: SEM image after 6.5 days of photol-ysis. Reproduced with permission from Ref. [168]. Copyright (2016) American Chemical Society.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim157

Reviews

achievements have been made using either supramolecularchemistry or an organic–inorganic hybrid approach. It was

shown also in inorganic systems, that is, Nocera’s Co-Pi cata-lyst, that the microscopic approach on the molecular or atomic

scale was very useful to control the catalytic activity.The promising results reported so far provide a good blue-

print for artificial photosynthesis; this research field requiresfurther development for real life application. The current status

in artificial photosynthesis is that each component responsible

for light harvesting, charge transfer and accumulation, and cat-alysis can be optimized in different working conditions, howev-

er, combining them in a single device as a complete module isstill a challenging task. Careful orchestration of the three strat-

egies mentioned in this article in one system is required. In theintegrated system we have to take account of critical factors:

1) Balancing between charge accumulation and the regulatorymechanism to aim to “kill two birds with one stone”, that

is, keeping optimal solar fuel production efficiency whilethe stability is guaranteed under fluctuating solar irradia-tion;

2) Self-healing should work while the catalytic system is under

operation;

3) The self-healing mechanism itself should be self consistent,not by stoichiometrically consuming other reagents or ad-

ditives.

Supramolecular chemistry can take a part to mimic the roleof protein matrix in natural photosystem. Controlling charge

separation, -transfer, and accumulation along with self-healing

can be accomplished with a supramolecular approach. Com-bining the benefits of homogeneous and heterogeneous

system can also provide a solution. The molecular system hasmerits of synthetic variety, ease of physical and chemical prop-

erty tuning, high catalytic site accessibility, while the disadvan-tages of low stability and low conductivity can be solved by

complementary inorganic systems. The multidisciplinary ap-

proach is still challenging, but we can learn from the 3.4 billionyears of evolution in nature.

Acknowledgements

This work was supported by the Austrian Science Foundation

(FWF) within the Wittgenstein Prize of Prof. N. S. Sariciftci (Z222-

N19). The authors acknowledged Prof. Soo Young Park and Prof.Niyazi Serdar Sariciftci for their supports and helpful discussions.

Conflict of interest

The authors declare no conflict of interest.

Keywords: artificial photosynthesis · carbon dioxide

reduction · photocatalysis · solar fuels · water splitting

[1] Key World Energy Statistics 2016, International Energy Agency, https://www.iea.org.

[2] G. Ciamician, Science 1912, 36, 385.[3] A. Fujishima, K. Honda, Nature 1972, 238, 37.[4] F. Akira, H. Kenichi, Bull. Chem. Soc. Jpn. 1971, 44, 1148.[5] T. Inoue, A. Fujishima, S. Konishi, K. Honda, Nature 1979, 277, 637.[6] R. Abe, J. Photochem. Photobiol. C 2010, 11, 179.[7] A. J. Bard, M. A. Fox, Acc. Chem. Res. 1995, 28, 141.[8] D. Chen, X. Zhang, A. F. Lee, J. Mater. Chem. A 2015, 3, 14487.[9] X. Chen, S. Shen, L. Guo, S. S. Mao, Chem. Rev. 2010, 110, 6503.

[10] R. J. Detz, K. Sakai, L. Spiccia, G. W. Brudvig, L. C. Sun, J. N. H. Reek,ChemPlusChem 2016, 81, 1024.

[11] W. Fan, Q. Zhang, Y. Wang, Phys. Chem. Chem. Phys. 2013, 15, 2632.[12] F. Fresno, R. Portela, S. Suarez, J. M. Coronado, J. Mater. Chem. A 2014,

2, 2863.[13] D. Gust, Faraday Discuss. 2015, 185, 9.[14] S. N. Habisreutinger, L. Schmidt-Mende, J. K. Stolarczyk, Angew. Chem.

Int. Ed. 2013, 52, 7372; Angew. Chem. 2013, 125, 7516.[15] V. P. Indrakanti, J. D. Kubicki, H. H. Schobert, Energy Environ. Sci. 2009,

2, 745.[16] M. Kapilashrami, Y. Zhang, Y.-S. Liu, A. Hagfeldt, J. Guo, Chem. Rev.

2014, 114, 9662.[17] M. G. Kibria, Z. Mi, J. Mater. Chem. A 2016, 4, 2801.[18] M. Kitano, M. Hara, J. Mater. Chem. 2010, 20, 627.[19] A. Kubacka, M. Fern#ndez-Garc&a, G. Coljn, Chem. Rev. 2012, 112, 1555.[20] A. Kudo, Y. Miseki, Chem. Soc. Rev. 2009, 38, 253.[21] Y. Lan, Y. Lu, Z. Ren, Nano Energy 2013, 2, 1031.[22] H. Li, Y. Zhou, W. Tu, J. Ye, Z. Zou, Adv. Funct. Mater. 2015, 25, 998.[23] J. Low, B. Cheng, J. Yu, M. Jaroniec, Energy Storage Mater. 2016, 3, 24.[24] J. Low, J. Yu, W. Ho, J. Phys. Chem. Lett. 2015, 6, 4244.[25] Q. Lu, Y. Yu, Q. Ma, B. Chen, H. Zhang, Adv. Mater. 2016, 28, 1917.[26] K. Maeda, K. Domen, J. Phys. Chem. Lett. 2010, 1, 2655.[27] J. Mao, K. Li, T. Peng, Catal. Sci. Technol. 2013, 3, 2481.[28] M. Marszewski, S. Cao, J. Yu, M. Jaroniec, Mater. Horiz. 2015, 2, 261.[29] K. Meyer, M. Ranocchiari, J. A. van Bokhoven, Energy Environ. Sci. 2015,

8, 1923.[30] S. J. A. Moniz, S. A. Shevlin, D. J. Martin, Z.-X. Guo, J. Tang, Energy Envi-

ron. Sci. 2015, 8, 731.[31] A. J. Morris, G. J. Meyer, E. Fujita, Acc. Chem. Res. 2009, 42, 1983.[32] J. Ran, J. Zhang, J. Yu, M. Jaroniec, S. Z. Qiao, Chem. Soc. Rev. 2014, 43,

7787.[33] M. Reza Gholipour, C.-T. Dinh, F. Beland, T.-O. Do, Nanoscale 2015, 7,

8187.[34] M. Rudolf, S. V. Kirner, D. M. Guldi, Chem. Soc. Rev. 2016, 45, 612.[35] J. Z. Su, L. Vayssieres, Acs Energy Lett. 2016, 1, 121.[36] W. Tu, Y. Zhou, Z. Zou, Adv. Funct. Mater. 2013, 23, 4996.[37] W. Tu, Y. Zhou, Z. Zou, Adv. Mater. 2014, 26, 4607.[38] M. G. Walter, E. L. Warren, J. R. McKone, S. W. Boettcher, Q. Mi, E. A.

Santori, N. S. Lewis, Chem. Rev. 2010, 110, 6446.[39] S. Wang, X. Wang, Angew. Chem. Int. Ed. 2016, 55, 2308; Angew. Chem.

2016, 128, 2352.[40] F. Y. Wen, C. Li, Acc. Chem. Res. 2013, 46, 2355.[41] J. L. White, M. F. Baruch, J. E. Pander, Y. Hu, I. C. Fortmeyer, J. E. Park, T.

Zhang, K. Liao, J. Gu, Y. Yan, T. W. Shaw, E. Abelev, A. B. Bocarsly, Chem.Rev. 2015, 115, 12888.

[42] J. Willkomm, K. L. Orchard, A. Reynal, E. Pastor, J. R. Durrant, E. Reisner,Chem. Soc. Rev. 2016, 45, 9.

[43] L. Wondraczek, E. Tyystj-rvi, J. M8ndez-Ramos, F. A. Meller, Q. Zhang,Adv. Sci. 2015, 2, 1500218.

[44] S. Xie, Q. Zhang, G. Liu, Y. Wang, Chem. Commun. 2016, 52, 35.[45] M. Yamamoto, K. Tanaka, ChemPlusChem 2016, 81, 1028.[46] J. Yang, D. Wang, H. Han, C. Li, Acc. Chem. Res. 2013, 46, 1900.[47] Y.-J. Yuan, H.-W. Lu, Z.-T. Yu, Z.-G. Zou, ChemSusChem 2015, 8, 4113.[48] H. Zhang, G. Liu, L. Shi, H. Liu, T. Wang, J. Ye, Nano Energy 2016, 22,

149.[49] N. Zhang, M.-Q. Yang, S. Liu, Y. Sun, Y.-J. Xu, Chem. Rev. 2015, 115,

10307.[50] T. J. Wydrzynski, K. Satoh, Photosystem II, : the light-driven water : plas-

toquinone oxidoreductase, Springer, Dordrecht, 2005.[51] R. Hill, F. Bendall, Nature 1960, 186, 136.[52] E. J. Boekema, H. van Roon, F. Calkoen, R. Bassi, J. P. Dekker, Biochem-

istry 1999, 38, 2233.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim158

Reviews

[53] S. J-rvi, M. Suorsa, E. M. Aro, Biochim. Biophys. Acta Bioenergetics 2015,1847, 900.

[54] J. J. S. van Rensen, V. B. Curwiel, Indian J. Biochem. Biophys. 2000, 37,377.

[55] H. Dau, M. Haumann, Coord. Chem. Rev. 2008, 252, 273.[56] M. Haumann, P. Liebisch, C. Meller, M. Barra, M. Grabolle, H. Dau, Sci-

ence 2005, 310, 1019.[57] J. P. McEvoy, G. W. Brudvig, Chem. Rev. 2006, 106, 4455.[58] H. Dau, M. Haumann, Biochim. Biophys. Acta Bioenergetics 2007, 1767,

472.[59] B. Kok, B. Forbush, M. McGloin, Photochem. Photobiol. 1970, 11, 457.[60] M. P. O’Neil, M. P. Niemczyk, W. A. Svec, D. Gosztola, G. L. Gaines, M. R.

Wasielewski, Science 1992, 257, 63.[61] H. Imahori, M. Hasegawa, S. Taniguchi, M. Aoki, T. Okada, Y. Sakata,

Chem. Lett. 1998, 27, 721.[62] A. F. Heyduk, D. G. Nocera, Science 2001, 293, 1639.[63] R. Konduri, H. Ye, F. M. MacDonnel, S. Serroni, S. Campagna, K. Rajesh-

war, Angew. Chem. Int. Ed. 2002, 41, 3185; Angew. Chem. 2002, 114,3317.

[64] Y. Pellegrinm, F. Odobel, Coord. Chem. Rev. 2011, 255, 2578.[65] L. Hammarstrçm, Acc. Chem. Res. 2015, 48, 840.[66] A. G. Bonn, O. S. Wenger, Chimia 2015, 69, 17.[67] D. Astruc, Comments Inorg. Chem. 1987, 6, 61.[68] D. Astruc, Bull. Chem. Soc. Jpn. 2007, 80, 1658.[69] D. Astruc, in Electron Transfer in Chemistry, Wiley-VCH, Weinheim 2008,

p. 714.[70] D. Astruc, New J. Chem. 2009, 33, 1191.[71] D. R. Whang, S. Y. Park, ChemSusChem 2015, 8, 3204.[72] M. Kobayashi, S. Masaoka, K. Sakai, Dalton Trans. 2012, 41, 4903.[73] M. Kobayashi, S. Masaoka, K. Sakai, Angew. Chem. Int. Ed. 2012, 51,

7431; Angew. Chem. 2012, 124, 7549.[74] K. Kitamoto, K. Sakai, Angew. Chem. Int. Ed. 2014, 53, 4618; Angew.

Chem. 2014, 126, 4706.[75] K. Kitamoto, K. Sakai, Chem. Commun. 2016, 52, 1385.[76] S. Lin, K. Kitamoto, H. Ozawa, K. Sakai, Dalton Trans. 2016, 45, 10643.[77] K. Kitamoto, M. Ogawa, G. Ajayakumar, S. Masaoka, H.-B. Kraatz, K.

Sakai, Inorg. Chem. Front. 2016, 3, 671.[78] K. Kitamoto, K. Sakai, Chem. Eur. J. 2016, 22, 12381.[79] S. M. Molnar, G. Nallas, J. S. Bridgewater, K. J. Brewer, J. Am. Chem. Soc.

1994, 116, 5206.[80] M. Elvington, K. J. Brewer, Inorg. Chem. 2006, 45, 5242.[81] D. F. Zigler, J. Wang, K. J. Brewer, Inorg. Chem. 2008, 47, 11342.[82] S. M. Arachchige, J. R. Brown, E. Chang, A. Jain, D. F. Zigler, K. Rangan,

K. J. Brewer, Inorg. Chem. 2009, 48, 1989.[83] K. Rangan, S. M. Arachchige, J. R. Brown, K. J. Brewer, Energy Environ.

Sci. 2009, 2, 410.[84] T. A. White, K. Rangan, K. J. Brewer, J. Photochem. Photobiol. A 2010,

209, 203.[85] T. A. White, S. L. H. Higgins, S. M. Arachchige, K. J. Brewer, Angew.

Chem. Int. Ed. 2011, 50, 12209; Angew. Chem. 2011, 123, 12417.[86] T. Stoll, M. Gennari, J. Fortage, C. E. Castillo, M. Rebarz, M. Sliwa, O.

Poizat, F. Odobel, A. Deronzier, M. N. Collomb, Angew. Chem. Int. Ed.2014, 53, 1654; Angew. Chem. 2014, 126, 1680.

[87] T. Stoll, M. Gennari, I. Serrano, J. Fortage, J. Chauvin, F. Odobel, M.Rebarz, O. Poizat, M. Sliwa, A. Deronzier, M. N. Collomb, Chem. Eur. J.2013, 19, 782.

[88] P. Huang, A. Magnuson, R. Lomoth, M. Abrahamsson, M. Tamm, L. Sun,B. van Rotterdam, J. Park, L. Hammarstrom, B. Akermark, S. Styring, J.Inorg. Biochem. 2002, 91, 159.

[89] A. Johansson, M. Abrahamsson, A. Magnuson, P. Huang, J. M,rtensson,S. Styring, L. Hammarstrçm, L. Sun, B. akermark, Inorg. Chem. 2003, 42,7502.

[90] L. Sun, M. K. Raymond, A. Magnuson, D. LeGourri8rec, M. Tamm, M.Abrahamsson, P. Huang Ken8z, J. M,rtensson, G. Stenhagen, L. Ham-marstrçm, S. Styring, B. akermark, J. Inorg. Biochem. 2000, 78, 15.

[91] M. N. Collomb, A. Deronzier, Eur. J. Inorg. Chem. 2009, 2025.[92] S. Romain, C. Baffert, S. Dumas, J. Chauvin, J. C. Lepretre, D. Daveloose,

A. Deronzier, M. N. Collomb, Dalton Trans. 2006, 5691.[93] S. Karlsson, J. Boixel, Y. Pellegrin, E. Blart, H.-C. Becker, F. Odobel, L.

Hammarstrçm, J. Am. Chem. Soc. 2010, 132, 17977.

[94] S. Karlsson, J. Boixel, Y. Pellegrin, E. Blart, H. C. Becker, F. Odobel, L.Hammarstrçm, Faraday Discuss. 2012, 155, 233.

[95] K. K. Niyogi, Annu. Rev. Plant Physiol. Plant Mol. Biol. 1999, 50, 333.[96] B. Demmig-Adams, Biochim. Biophys. Acta Bioenerg. 1990, 1020, 1.[97] a) G. H. Krause, E. Weis, Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991,

42, 313.[98] J. Barber, B. Andersson, Trends Biochem. Sci. 1992, 17, 61.[99] B. Demmig-Adams, W. W. Adams, Annu. Rev. Plant Physiol. Plant Mol.

Biol. 1992, 43, 599.[100] E. M. Aro, I. Virgin, B. Andersson, Biochim. Biophys. Acta Bioenerg. 1993,

1143, 113.[101] C. H. Foyer, P. Descourvieres, K. J. Kunert, Plant Cell Environ. 1994, 17,

507.[102] P. Horton, A. V. Ruban, R. G. Walters, Plant Physiol. 1994, 106, 415.[103] S. P. Long, S. Humphries, P. G. Falkowski, Annu. Rev. Plant Physiol. Plant

Mol. Biol. 1994, 45, 633.[104] O. Bjçrkman, B. Demmig-Adams, in Ecophysiology of Photosynthesis,

Springer, Berlin, Heidelberg, 1995, p. 17.[105] B. Demmig-Adams, W. W. Adams, Trends Plant Sci. 1996, 1, 21.[106] B. DemmigAdams, A. M. Gilmore, W. W. Adams, FASEB J. 1996, 10, 403.[107] P. Horton, A. V. Ruban, R. G. Walters, Annu. Rev. Plant Physiol. Plant Mol.

Biol. 1996, 47, 655.[108] J. M. Anderson, Y. I. Park, W. S. Chow, Physiol. Plant. 1997, 100, 214.[109] A. M. Gilmore, Physiol. Plant. 1997, 99, 197.[110] G. Noctor, C. H. Foyer, Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49,

249.[111] J. M. Anderson, Annu. Rev. Plant Physiol. Plant Mol. Biol. 1986, 37, 93.[112] A. Melis, Biochim. Biophys. Acta 1991, 1058, 87.[113] J. M. Escoubas, M. Lomas, J. Laroche, P. G. Falkowski, Proc. Natl. Acad.

Sci. USA 1995, 92, 10237.[114] D. P. Maxwell, D. E. Laudenbach, N. P. A. Huner, Plant Physiol. 1995, 109,

787.[115] R. G. Walters, P. Horton, Planta 1994, 195, 248.[116] M. Lindahl, D. H. Yang, B. Andersson, Eur. J. Biochem. 1995, 231, 503.[117] J. F. Allen, Physiol. Plant. 1995, 93, 196.[118] J. Walz, K. Ulrich, H. Port, H. C. Wolf, J. Wonner, F. Effenberger, Chem.

Phys. Lett. 1993, 213, 321.[119] S. Tsuchiya, J. Am. Chem. Soc. 1999, 121, 48.[120] R. S. Stoll, S. Hecht, Angew. Chem. Int. Ed. 2010, 49, 5054; Angew.

Chem. 2010, 122, 5176.[121] S. D. Straight, G. Kodis, Y. Terazono, M. Hambourger, T. A. Moore, A. L.

Moore, D. Gust, Nat. Nanotechnol. 2008, 3, 280.[122] F. Boucher, M. Van der Rest, G. Gingras, Biochim. Biophys. Acta Bioener-

getics 1977, 461, 339.[123] G. Cohen-Bazire, R. Y. Stanier, Nature 1958, 181, 250.[124] T. W. Goodwin, The biochemistry of the carotenoids, Chapman and Hall,

London, New York, 1980.[125] M. Griffiths, W. R. Sistrom, G. Cohenbazire, R. Y. Stanier, Nature 1955,

176, 1211.[126] P. Mathis, W. L. Butler, K. Satoh, Photochem. Photobiol. 1979, 30, 603.[127] T. G. Monger, R. J. Cogdell, W. W. Parson, Biochim. Biophys. Acta Bioen-

erg. 1976, 449, 136.[128] G. Renger, C. Wolff, Biochim. Biophys. Acta Bioenerg. 1977, 460, 47.[129] C. Wolff, H. T. Witt, Z Naturforsch B 1969, 24, 1031.[130] C. S. Foote, Y. C. Chang, R. W. Denny, J. Am. Chem. Soc. 1970, 92, 5216.[131] R. V. Bensasson, E. J. Land, A. L. Moore, R. L. Crouch, G. Dirks, T. A.

Moore, D. Gust, Nature 1981, 290, 329.[132] E. Tyystjarvi, E. M. Aro, Proc. Natl. Acad. Sci. USA 1996, 93, 2213.[133] J. Komenda, J. Barber, Biochemistry 1995, 34, 9625.[134] A. K. Mattoo, H. Hoffmanfalk, J. B. Marder, M. Edelman, P. Natl. Acad.

Sci. Biol. 1984, 81, 1380.[135] N. Adir, H. Zer, S. Shochat, I. Ohad, Photosynth. Res. 2003, 76, 343.[136] A. A. Boghossian, M. H. Ham, J. H. Choi, M. S. Strano, Energy Environ.

Sci. 2011, 4, 3834.[137] M. W. Kanan, D. G. Nocera, Science 2008, 321, 1072.[138] D. A. Lutterman, Y. Surendranath, D. G. Nocera, J. Am. Chem. Soc. 2009,

131, 3838.[139] M. M. Najafpour, M. Kompany-Zareh, A. Zahraei, D. J. Sedigh, H. Jac-

card, M. Khoshkam, R. D. Britt, W. H. Casey, Dalton Trans. 2013, 42,14603.

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim159

Reviews

[140] M. W. Kanan, Y. Surendranath, D. G. Nocera, Chem. Soc. Rev. 2009, 38,109.

[141] D. K. Zhong, D. R. Gamelin, J. Am. Chem. Soc. 2010, 132, 4202.[142] D. K. Zhong, J. Sun, H. Inumaru, D. R. Gamelin, J. Am. Chem. Soc. 2009,

131, 6086.[143] D. K. Zhong, M. Cornuz, K. Sivula, M. Gratzel, D. R. Gamelin, Energy En-

viron. Sci. 2011, 4, 1759.[144] E. M. P. Steinmiller, K.-S. Choi, Proc. Natl. Acad. Sci. USA 2009, 106,

20633.[145] F. F. Abdi, R. van de Krol, J. Phys. Chem. C 2012, 116, 9398.[146] J. Kamimura, P. Bogdanoff, F. F. Abdi, J. Lahnemann, R. van de Krol, H.

Riechert, L. Geelhaar, J. Phys. Chem. C 2017, 121, 12540.[147] R. S. Khnayzer, M. W. Mara, J. Huang, M. L. Shelby, L. X. Chen, F. N. Cas-

tellano, ACS Catal. 2012, 2, 2150.[148] J. J. H. Pijpers, M. T. Winkler, Y. Surendranath, T. Buonassisi, D. G.

Nocera, Proc. Natl. Acad. Sci. USA 2011, 108, 10056.[149] E. R. Young, R. Costi, S. Paydavosi, D. G. Nocera, V. Bulovic, Energy Envi-

ron. Sci. 2011, 4, 2058.[150] L. Ge, C. Han, X. Xiao, L. Guo, Appl. Catal. B 2013, 142, 414.[151] R.-L. Lee, P. D. Tran, S. S. Pramana, S. Y. Chiam, Y. Ren, S. Meng, L. H.

Wong, J. Barber, Catal. Sci. Technol. 2013, 3, 1694.[152] Y. Li, L. Zhang, A. Torres-Pardo, J. M. Gonzalez-Calbet, Y. Ma, P. Oleyni-

kov, O. Terasaki, S. Asahina, M. Shima, D. Cha, L. Zhao, K. Takanabe, J.Kubota, K. Domen, Nat. Commun. 2013, 4, 2566.

[153] S. K. Pilli, T. E. Furtak, L. D. Brown, T. G. Deutsch, J. A. Turner, A. M. Her-ring, Energy Environ. Sci. 2011, 4, 5028.

[154] S. Y. Reece, J. A. Hamel, K. Sung, T. D. Jarvi, A. J. Esswein, J. J. H. Pijpers,D. G. Nocera, Science 2011, 334, 645.

[155] D. G. Nocera, Acc. Chem. Res. 2012, 45, 767.[156] J. Gu, Y. Yan, J. W. Krizan, Q. D. Gibson, Z. M. Detweiler, R. J. Cava, A. B.

Bocarsly, J. Am. Chem. Soc. 2014, 136, 830.[157] T. Lazarides, T. McCormick, P. W. Du, G. G. Luo, B. Lindley, R. Eisenberg,

J. Am. Chem. Soc. 2009, 131, 9192.[158] T. M. McCormick, Z. Han, D. J. Weinberg, W. W. Brennessel, P. L. Holland,

R. Eisenberg, Inorg. Chem. 2011, 50, 10660.[159] L. L. Tinker, N. D. McDaniel, P. N. Curtin, C. K. Smith, M. J. Ireland, S.

Bernhard, Chem. Eur. J. 2007, 13, 8726.[160] A. Dhakshinamoorthy, A. M. Asiri, H. Garc&a, Angew. Chem. Int. Ed.

2016, 55, 5414; Angew. Chem. 2016, 128, 5504.[161] C. Gao, J. Wang, H. Xu, Y. Xiong, Chem. Soc. Rev. 2017, 46, 2799.[162] Y. Li, H. Xu, S. Ouyang, J. Ye, Phys. Chem. Chem. Phys. 2016, 18, 7563.[163] M. C. So, G. P. Wiederrecht, J. E. Mondloch, J. T. Hupp, O. K. Farha,

Chem. Commun. 2015, 51, 3501.[164] S. Wang, X. Wang, Small 2015, 11, 3097.[165] L. Zeng, X. Guo, C. He, C. Duan, Acs Catal. 2016, 6, 7935.[166] T. Zhang, W. Lin, Chem. Soc. Rev. 2014, 43, 5982.[167] T. Zhou, Y. Du, a. Borgna, J. Hong, Y. Wang, J. Han, W. Zhang, R. Xu,

Energy Environ. Sci. 2013, 6, 3229.[168] D. Kim, D. R. Whang, S. Y. Park, J. Am. Chem. Soc. 2016, 138, 8698.

Manuscript received: September 15, 2017

Revised manuscript received: November 23, 2017

Accepted manuscript online: November 28, 2017Version of record online: January 9, 2018

ChemPhotoChem 2018, 2, 148 – 160 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim160

Reviews