Artificial Photosynthesis for Production of ATP, NAD(P)H,and Hydrogen PeroxideShunichi Fukuzumi,*[a, b] Yong-Min Lee,*[a] and Wonwoo Nam*[a]

ChemPhotoChem 2018, 2, 121 – 135 T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim121

MinireviewsDOI: 10.1002/cptc.201700146

1. Introduction

Photosynthesis consists of reactions that require light and

others that occur in the dark. The light-dependent reactionproceeds on thylakoid membranes, which contain some inte-

grated membrane protein complexes that act as photocata-

lysts.[1–3] Photosystem II (PSII), cytochrome b6f complex, photo-system I (PSI) and ATP synthase are found in the thykaloid

membranes, which work cooperatively to produce finally ATPand NADPH.[1–3] The electrons and protons released from PSI

via PSII by water oxidation enables the two-electron/one-proton regioselective reduction of NADP+ to produce the 1,4-

dihydro form (NADPH), with which CO2 is reduced in the

Calvin–Benson cycle, where carbohydrates are produced.[4–17]

Alternatively, the electrons and protons can be employed in

the reduction of molecular dioxygen (O2) in the Mehler reac-tion producing, through dismutation of the superoxide anion,

the hydrogen peroxide species (H2O2).[18–20] The flow of elec-trons from the electron transport chain to O2 in the Mehler re-action can dissipate the excess light energy to prevent the

electron transport chain from photoinhibition.[21–27] Undernormal light intensity conditions, the reduction of O2 to H2O2

represents around 5–10 % of the total photosynthetic electronflow in C3 plants.[28] However, under stressed conditions suchas strong light intensity, the electron flow used for the O2 re-duction to H2O2 increases up to 30 % and even higher.[28] The

light-independent (dark) reactions use ATP and NADPH pro-

duced by the light-dependent reactions to fix CO2 and convert

the energy into the chemical bond energy in carbohydratessuch as glucose.[4–17]

There have been extensive studies to model the light-har-vesting (energy transfer) and charge-separation (electron-trans-

fer) processes in PSI and PSII.[29–33] A variety of electron donor–

acceptor compounds linked by covalent and noncovalentbonds have been designed and synthesized to mimic the

light-harvesting and charge-separation functions in photosyn-thetic reaction centers of PSI and PSII.[34–51] Extensive efforts

have also been devoted to develop the photocatalytic systemsfor the reduction of water to evolve hydrogen as well as the

oxidation of water to evolve O2.[52–68] The thermal and photoca-

talytic reduction of CO2 has also been extensively investigatedand reviewed.[69–82] However, artificial photosynthesis to pro-

duce the same products as those in natural photosynthesis(ATP, NAD(P)H, and H2O2) has yet to be reviewed and discussed

together.This Minireview focuses on artificial photosynthesis for solar-

driven production of ATP, NAD(P)H and H2O2, which are the

same products as those in natural photosynthesis. There aremany excellent reviews available on solar-driven water splittingto produce hydrogen,[83–97] which can reduce a variety of sub-strates including CO2, NAD(P)+ and O2. The standard oxidationpotential of H2 at pH 7 (E0’) is @0.41 V vs. SHE [Eq. (1)] , whereasthe standard reduction potential of NAD(P)+ is @0.32 V vs. SHE

[Eq. (2)] .[98, 99] The reduction of NAD(P)+ by H2 to produceNADPH [Eq. (3)] is thermodynamically favorable (exergonic) atpH 7, because the E0’ value of H2 is more negative than that of

NADP+ :[100]

H2 ! 2 Hþ þ 2 e@ E0 0 ¼ @0:41 V vs: SHE ð1Þ

NADPþ þ 2 e@ þ Hþ ! NADPH E0 0 ¼ @0:32 V vs: SHE ð2Þ

H2 þ NADðPÞþ ! Hþ þ NADPH ð3Þ

Thus, once H2 is produced by solar-driven water splitting[Eq. (4)]:

The initial product of photosynthesis is NADPH (dihydronicoti-namide adenine dinucleotide phosphate), which is produced

from the oxidized form (NADP+) by reduction with two elec-trons and one proton released from Photosystem I (PSI) via fer-redoxin. The proton gradient generated across the thylakoidmembrane produces a proton-motive force, which is utilizedto synthesize ATP by the use of ATP synthase. NADPH is used

as a hydride source in the Calvin–Benson cycle to producesugars by photosynthesis. In addition to NADP+ , PSI can

reduce O2 by two electrons with two protons to produce hy-drogen peroxide (H2O2), which can be used as a fuel in H2O2

fuel cells. This Minireview focuses on artificial photosyntheticsystems to produce the products of natural photosynthesis,

such as ATP, NAD(P)H and H2O2 from NAD+ and O2 with water

using solar energy, respectively. ATP was produced by use ofan artificial photosynthetic membrane, composed of a photo-synthetic reaction center mimic that pumps protons into theinterior of the liposome, where F-type ATP synthase was incor-porated. Solar-driven catalytic water splitting produces hydro-gen, which can reduce NAD+ to NADH with an iridium com-

plex catalyst in a slightly alkaline solution at room tempera-ture. H2O2 has been produced by the combination of four-elec-tron oxidation of H2O with four protons to evolve O2 and two-

electron/two-proton reduction of O2 under sun-light irradia-tion. H2O2 can also be produced by direct reaction of H2 and

O2 by the combination of an iridium complex catalyst andflavin coenzyme.

[a] Prof. Dr. S. Fukuzumi, Prof. Dr. Y.-M. Lee, Prof. Dr. W. NamDepartment of Chemistry and Nano ScienceEwha Womans UniversitySeoul 03760 (Korea)E-mail : fukuzumi@chem.eng.osaka-u.ac.jp

yomlee@ewha.ac.krwwnam@ewha.ac.kr

[b] Prof. Dr. S. FukuzumiGraduate School of Science and EngineeringMeijo University, NagoyaAichi 468-8502 (Japan)

The ORCID identification number(s) for the author(s) of this article canbe found under: https://doi.org/10.1002/cptc.201700146.

An invited contribution to a Special Issue on Artificial Photosynthesis

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim122

Minireviews

2 H2O hnK!2 H2 þ O2 ð4Þ

NAD(P)+ can be reduced by H2 to produce NAD(P)H [Eq. (3)] atpH 7. This Minireview discusses not only the direct solar-driven

reduction of NAD(P)+ to NAD(P)H but also the production ofNAD(P)H by the catalytic reduction of NAD(P)+ by H2 that canbe produced by solar-driven water splitting. By the sametoken, the production of H2O2 by the two-electron/two-proton

reduction of molecular O2 by H2 [Eq. (5)] that can be producedby solar-driven water splitting is also discussed together with

the direct production of H2O2 from H2O and O2 [Eq. (6)] . Pro-duction of ATP accompanied by oxidation of H2 [Eq. (7)] is also

discussed as well as direct solar-driven ATP production fromADP and inorganic phosphate (Pi) using the proton gradient

across the membrane [Eq. (8)] .

H2 þ O2 ! H2O2 ð5Þ2 H2Oþ O2

hnK!2 H2O2 ð6Þ

H2 þ ADPþ Pi ! 2 Hþ þ 2 e@ þ ATP ð7Þ

ADPþ PihnK!ATP ð8Þ

2. Production of ATP

2.1. Solar-Driven Production of ATP

Photoinduced charge separation in the photosynthetic reac-

tion centers results in proton transfer from the stroma into thethylakoid lumen, which generates a proton motive force (pmf)

across the thylakoid membrane.[101–103] The pmf drives ATP syn-thesis by the function of the ATP synthase using DpH, which is

the proton concentration gradient and the membrane poten-tial (DY), which results from the charge difference across the

thylakoid membrane.[104–110] A pmf was generated by using a

photosynthetic reaction center mimic triad (C-P-Q in Figure 1)

composed of a carotenoid polyene (C), a tetraarylporphyrin (P)and a naphthoquinone moiety fused to a norbornene unitwith a carboxylic acid (Q), which was incorporated into the bi-

layer of a liposome.[111] Photoexcitation of C-P-Q resulted inelectron transfer from the excited state of P to Q to produce

the initial charge-separated (CS) state (C-P· +-QC@), followed bysubsequent electron transfer (charge shift) from C to PC+ to

afford the final CS state (C· +-P-QC@), which exhibited a long life-time of the ms timescale with a quantum yield of up to 15 %

(Scheme 1).[112, 113] A lipid-soluble 2,5-diphenylbenzoquinone (Qs

in Scheme 1) acts as the proton shuttle. Qs near the externalaqueous phase is reduced by electron transfer from the QC@

moiety of the CS state (CC+-P-QC@) to produce QsC@ , which ac-cepts a proton from the nearby external aqueous phase to

produce neutral (nonpolar) semiquinone radical (QsHC).[111] Thenonpolar QsHC is diffused across the bilayer to the region near

Shunichi Fukuzumi received a BS

degree and Ph.D. degree at Tokyo

Institute of Technology in 1973 and

1978, respectively. After a three-year

postdoctoral experience at Indiana

University in the USA, he moved to

Osaka University (Japan) as an Assis-

tant Professor in 1981 and was pro-

moted to a Full Professor in 1994 and

to a Distinguished Professor in 2013.

His research has focused on electron

transfer chemistry, in particular, artifi-

cial photosynthesis. He is currently a Distinguished Professor at

Ewha Womans University (Korea), a Designated Professor at Meijo

University (Japan) and a Professor Emeritus at Osaka University

(Japan).

Yong-Min Lee earned his Ph.D. degree

in Inorganic Chemistry under the di-

rection of Professor Sung-Nak Choi at

Pusan National University (Korea) in

1999. Then, he moved to the Magnetic

Resonance Center (CERM) at University

of Florence (Italy) as a Postdoctoral

Fellow and Researcher under the direc-

tion of Professors Ivano Bertini and

Claudio Luchinat (from 1999 to 2005).

He has been a Special Appointment

Professor at Ewha Womans University

(Korea) since 2009.

Wonwoo Nam earned his BS (Honors)

degree in Chemistry from California

State University, Los Angeles, and his

Ph.D. degree in Inorganic Chemistry

under the direction of Professor Joan

S. Valentine in 1990 at University Cali-

fornia, Los Angeles (UCLA). After a

one-year postdoctoral experience at

UCLA (USA), he became an Assistant

Professor at Hongik University (Korea)

in 1991. He moved to Ewha Womans

University in 1994, where he is current-

ly a Distinguished Professor at Ewha Womans University (Korea)

since 2005. His current research focuses on dioxygen activation,

water oxidation, and sensors for metal ions in bioinorganic

chemistry.

Figure 1. A photosynthetic reaction center mimic triad (C-P-Q) composed ofa carotenoid polyene (C), a tetraarylporphyrin (P) and a naphthoquinone(Q).[111]

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim123

Minireviews

the interior aqueous phase, where proton-coupled electron

transfer from QsHC to CC+-P-Q occurs to release H+ to the interi-

or aqueous phase to generate the pH gradient, accompaniedby regeneration of Qs and C-P-Q.[111] Photoirradiation of C-P-Q

in the liposome with Qs for 10 min resulted in an average often protons imported per liposome to increase the external

pH value from 6.91 to 6.94.[111] The artificial photosyntheticmembrane in Scheme 1 converts photon energy into the vec-

torial intramembrane redox potential and then into pmf.[111]

When F0F1-ATP synthase was incorporated into the artificialphotosynthetic membrane (Scheme 1), visible-light illumination

of this artificial membrane resulted in production of ATPagainst a chemical potential of ATP (12 kcal mol@1) to achieve a

quantum yield of higher than 7 %.[114] F0F1-ATP synthase con-sists of two mechanically coupled regions by a common cen-tral stalk that is called “rotor”, F0 and F1.[106] The membrane em-

bedded F0 unit converts pmf into mechanical rotation of the“rotor’’, which causes cyclic conformational change in F1 todrive ATP synthesis.[106] Under the optimized conditions, ATPwas synthesized with a rate of 3.5 V 10@8 mol h@1, which corre-

sponds to the turnover number (TON = 7:1) of ATP per CF0F1

per second, because there are 9 V 1011 liposomes in the irradiat-

ed volume and there is one enzyme molecule per liposome.[114]

Thus, the artificial photosynthetic membrane in Scheme 1mimics well the energy-conversion process of photosynthetic

bacteria from light energy into a chemical potential of ATP.A liposome-based, light-driven transmembrane Ca2 + pump

was also reported using the C-P-Q triad in Figure 1 as a photo-synthetic reaction center mimic and a lipid-soluble hydroqui-

none as a shuttle molecule as shown in Figure 2.[115] The hydro-

quinone anion that chelates Ca2 + at the external interface dif-fuses across the membrane, and it is oxidized to the quinone

by the carotenoid radical cation (CC+) moiety of the CS state(CC+-P-QC@) that is formed by photoinduced electron transfer in

Scheme 1.[115] After Ca2+ is released to the internal aqueousvolume, the oxidized quinone diffuses back across the mem-

brane, where the quinone is reduced by the QC@ moiety of C-P-QC@ to regenerate the hydroquinone anion and C-P-Q.[115] Pho-

toirradiation of the assembly in Figure 2 with visible light ab-sorbed by the P moiety of C-P-Q resulted in transmembrane

Ca2 + transport, leading to an increase in the internal Ca2+ con-

centration, which was monitored by the use of the fluorescentdye (Fluo-3)[116] located only inside the liposomes.[115] It was

confirmed that no Ca2+ transport was detected in the absenceof C-P-Q or the hydroquinone shuttle molecule.[115] Photoirra-

diation of the membrane in Figure 2 under the experimentalconditions for Ca2+ pumping resulted in generation of a mem-brane potential (DY&120 mV) on the interior of the lipo-

somes.[115] No DY was produced without photoirradiation, orin the absence of C-P-Q or the shuttle molecule.[115]

Formation of a membrane potential was also achieved byusing electron donor–photosensitizer–acceptor triads such as

ferrocene–porphyrin–C60 (Fc-P-C60) linked triad molecules asphotosynthetic reaction center mimics, in which a hydrophilic

tetramethylammonium cation group is tethered to the Fcmoiety (Figure 3). Fc-P-C60 was incorporated into an intracellu-lar drug delivery carrier (cpHDL)[117] that was prepared by

mixing, in a 300:1 molar ratio, palmitoyloleoyl-phosphatidyl-choline (POPC) with a human apoA-I mutant fused to a TAT se-

quence (YGRKKRRQRRR).[118] Visible-light photoirradiation (l=

400–450 nm) of PC12 cells that were treated with the Fc-H2P-

C60-loaded cpHDL resulted in changes in the membrane poten-

tial to reach a constant value (depolarization = 13 mV) in 1 min(Figure 4 a).[117] In contrast, visible-light irradiation of PC12 cells

themselves and those treated with cpHDL loaded with H2P-refexhibited no change in membrane potential as shown in Fig-

ure 4 b and Figure 4 c, respectively.[117] Laser photoexcitation ofthe Fc-H2P-C60 triad in deaerated DMSO results in electron

Scheme 1. ATP synthesis by use of a liposome-based artificial photosyntheticmembrane, with which protons are pumped into the interior of the lipo-some and the CFOF1-ATP synthase by means of photoinduced charge separa-tion of the C-P-Q triad.[111]

Figure 2. A liposome-based, light-driven transmembrane Ca2 + pump usingC-P-Q in Figure 1 as a photosynthetic reaction center mimic and a lipid-solu-ble hydroquinone as a shuttle molecule. Reprinted with permission fromRef. [115]. Copyright 2002, Nature Publishing Group.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim124

Minireviews

transfer from the singlet excited state of the porphyrin moiety(1H2P*) to the C60 moiety of the triad, followed by subsequentelectron transfer (charge shift) from the Fc moiety to the H2PC+

moiety to afford the final CS state (Fc+-H2P-C60C@) in deaeratedDMSO with a lifetime of 5.5 ms.[117] Such long CS lifetimes have

also been reported for triads, tetrads, and pentad moleculescomposed of Fc, porphyrins and C60.[119–124] The final CS state

(Fc+-H2P-C60C@) was also observed in a deaerated aqueous solu-

tion of the PC12 cell treated with Fc-H2P-C60-loaded cpHDLwith a lifetime of 3.0 ms.[117] Thus, photoinduced long-lived

charge separation of the Fc-H2P-C60 triad is responsible for thegeneration of a membrane potential in the PC12 cells, which

were treated with the Fc-ZnP-C60-loaded cpHDL.[117] Photoin-duced electron-transfer reactions of photosynthetic reaction

center mimics other than C-P-Q in Figure 1 were also utilizedfor generation of a proton potential across a lipid mem-branes.[125–128] However, ATP synthesis by such visible-light-driven generation of the proton membrane potential has yet

to be achieved.A visible light-driven ATP synthesis has been performed by

using a F0F1-ATPase proteoliposome-coated PSII-based micro-sphere with a core@shell structure by molecular assembly asshown in Figure 5, where hydrogel-like PSII-based micro-

spheres are prepared through coprecipitation of bovine serumalbumin (BSA), PSII, and calcium carbonate (CaCO3), followed

by glutaric dialdehyde (GA) cross-linking and subsequent re-moval of the CaCO3 core.[129] F0F1-ATPase proteoliposomes are

coated on the surface of hydrogel-like PSII-based microspheresto construct a chloroplast-like light-driven artificial photophos-

phorylation system, where the visible-light-to-ATP synthesis

occurs in the thylakoid membrane (Figure 6).[129]

Under red-light illumination, PSII entrapped in the hydrogel-

like solid microsphere splits water into four protons, which se-quentially prompt the rotational catalysis of F0F1-ATPase pro-

teoliposomes on the shell, and four electrons that reduce fourequivalents of ferricyanide complex ([FeIII(CN)6]3@) to ferrocya-

nide complex ([FeII(CN)6]4@).[129] The activity of the ATPase–PSII

microsphere system was measured by means of an increase in

Figure 3. Ferrocene–porphyrin–C60 (Fc-P-C60) triads as photosynthetic reac-tion center models in which a hydrophilic cationic moiety (a tetramethyl-ammonium group) is tethered to the Fc moiety (e.g. , Fc-H2P-C60 and Fc-ZnP-C60) and reference compounds (e.g. , H2P-ref and ZnP-ref). Reprinted withpermission from Ref. [117]. Copyright 2012, American Chemical Society.

Figure 4. Time profiles of changes in the membrane potential under visible-light irradiation (l= 400–450 nm, input power: 5 mW cm@2) of PC12 cellstreated for 3 min with a) Fc-H2P-C60-loaded cpHDL, b) H2P-ref-loaded cpHDL,and c) medium only and then they were washed with phosphate-bufferedsaline. Reprinted with permission from Ref. [117] . Copyright 2012, AmericanChemical Society.

Figure 5. A red-light-driven ATP synthetic system composed of F0F1-ATPaseproteoliposome-coated PSII-based microsphere with a core@shell structure,constructed by molecular assembly. Reprinted with permission fromRef. [129] . Copyright 2016, American Chemical Society.

Figure 6. Time profiles of ATP synthesis in the thylakoid membrane usingthe membrane potential generated under visible-light irradiation (l= 400–450 nm with input power of 5 mW cm@2) and in darkness. Reprinted withpermission from Ref. [129]. Copyright 2016, American Chemical Society.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim125

Minireviews

the concentration of produced ATP by use of the luciferin andluciferase assay.[130] When luciferase catalyzes the luciferin oxi-

dation by consuming ATP, a photon is released and the ob-served luminescence intensity increases proportionally with in-

creasing the amount of ATP present in the system. As shownin Figure 6, the production of ATP increases with increasing du-

ration of red-light irradiation to reach around 1100 nmol ATP(mg Chl)@1 (red squares), whereas it is nearly unchanged in thedark (blue squares).[129]

ATP has also been synthesized by combining bacteriorho-dopsin (BR), which is a light-driven transmembrane protonpump, with F0F1-ATP synthase that is reconstituted in polymer-somes (Figure 7).[131] BR is composed of opsin apoproteins and

a covalently linked retinal that changes its conformation via

the photoexcited state to induce a conformational change ofthe surrounding protein, which starts the proton pumping

action.[132, 133] Visible-light illumination of BR results in genera-tion of a proton gradient across the cell membrane via a light-

induced BR photocycle,[132, 133] driving the ATP synthesis fromADP and inorganic phosphate (Pi) by use of ATP synthase

(Figure 7). The maximum rate of ATP synthesis was 116 nmolmin@1 per mg of ATP synthase at the first 5 min under greenLED light (l= 570 nm) irradiation.[131] Because ATP synthesis by

use of ATP synthase is activated by the pH gradient across themembrane, the rapid acidification during the initial illumina-

tion leads to a faster initial rate of ATP synthesis.[131] Proteogelsthat contain proteoliposomes with both BR and F0F1-ATP syn-

thase were also reported to couple the generation of the

photoinduced proton gradient and the ATP synthesis.[134]

2.2. H2-Fueled Production of ATP

Hydrogen (H2) is used as a fuel to generate a proton gradientby using a modified electrode surface integrating a mem-

brane-bound NiFeSe hydrogenase from Desulfovibrio vulgarisHildenborough (Dv-SeHase) and a F0F1-ATPase in a phospholip-

id bilayer (PhBL),[135, 136] which can couple the electrocatalyticoxidation of H2 to the ATP synthesis from ADP and inorganic

phosphate (Pi ; Figure 8).[137] The NiFeSe hydrogenase exhibits ahigh reactivity with marginal inhibition by H2 and tolerance to

O2.[138–140] Protons produced in the electrocatalytic H2 oxidationare used for the ATP synthesis from ADP and Pi by use of F0F1-ATPase.[137]

Cyclic voltammograms of the activated Hase/PhBL/ATPase-modified electrode in an anaerobic chamber under one atmos-pheric pressure of H2 in a phosphate buffer solution are shownin Figure 9 A, where the anodic current increases with an in-

crease in the potential to reach a plateau value of @0.20 V vs.SCE due to the two-electron oxidation of H2 to produce pro-tons.[137] At the PhBL/electrode interface of the biomimeticstructure protons were produced by applying a continuous po-

tential of + 0.150 V vs. SCE for 130 min in the presence of ADP(500 mm) under one atmospheric pressure of H2, when ATPwas synthesized from ADP and Pi as monitored by a spectro-

photometric method (Figure 9 B).[137] Control measurementswith PhBL-modified electrodes in the absence of either Dv-

SeHase or FOF1-ATPase confirmed that no ATP was produced inthe bulk solution during H2 oxidation with the immobilized hy-

drogenase in the absence of any component of F0F1-ATPase,

ADP and Pi.[137]

As mentioned in the Introduction, there have been many

studies on photodriven H2O splitting to produce H2

[Eq. (4)] .[83–97] However, the photodriven H2O splitting to pro-

duce H2 has yet to be coupled with ATP synthesis using H2 asa fuel.

Figure 7. Schematic drawing of proteopolymersomes, which are reconstitut-ed by BR and F0F1-ATP synthase that utilize an electrochemical proton gradi-ent generated by photoexcitation of BR for ATP synthesis from ADP and in-organic phosphate (Pi). Reprinted with permission from Ref. [131]. Copyright2005, American Chemical Society.

Figure 8. Schematic drawing of a supramolecular catalytic system for thesynthesis of ATP coupled with the electrocatalytic oxidation of H2 by NiFeSehydrogenase, which is immobilized on an Au electrode modified with a SAMof 4-aminothiophenol and anchored to a PhBL through its lipid tail. ThePhBL embeds F0F1-ATPases. Reprinted with permission from Ref. [137].Copyright 2016, WILEY-VCH Verlag GmbH.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim126

Minireviews

3. Production of NAD(P)H

3.1. Solar-Driven Production of NAD(P)H

NAD(P)H, which is a product of natural photosynthesis, is pro-

duced by photocatalytic reduction of NAD(P)+ using water asan electron and proton source, [Co4(H2O)2(PW9O34)2]10@

[Co4(POM)] as a water oxidation catalyst,[141–143] [RuII(bpy)3]2+ asa photocatalyst, and [Cp*RhIII(L)(H2O)]2 + (Cp* =h5-pentamethyl-

cyclopentadienyl ; L: bpy = 2,2’-bipyridine, 4-dmbpy = 4,4’-di-methyl-2,2’-bipyridine, 5-dmbpy = 5,5’-dimethyl-2,2’-bipyridine,

and 4-dcbpy = 4,4’-dicarboxy-2,2’-bipyridine) as an NAD(P)+ re-

duction catalyst[144–147] (Scheme 2).[148] Weinkamp and Streckhanreported earlier selective generation of NADH from NAD+ in

the presence of the photochemically generated [RhI(bpy)2]+

complex as a catalyst and [RuII(bpy)3]2 + as a photocatalyst and

triethanolamine (TEOA) as a sacrificial electron donor undervisible-light irradiation.[149] Knçr and co-workers reported that

[RuII(bpy)3]2 + was replaced by a water-soluble tin(IV) complex

of meso-tetrakis(N-methylpyridinium)chlorin in the photocata-lytic selective generation of NADH from NAD+ with

[Cp*RhIII(bpy)H]+ .[150] The regioselective reduction of NAD+ tothe 1,4-dihydro form (NADH) by [Cp*RhIII(bpy)H]+ was pro-

posed to be made possible by the coordination of the amide

group to the Cp*RhIII metal center, which results in generationof the transition state with a kinetically favorable six-mem-

bered ring structure for plausible concerted hydride transfer/insertion to C4 for the regioselective production of NADH.[151]

Photoinduced electron transfer form the excited state of[RuII(bpy)3]2 + ([RuII(bpy)3]2+*, where * denotes the excited

state) to [Cp*RhIII(4-dcbpy)(H2O)]2 + occurs efficiently with a

rate constant of (1.1–2.78) V 109 m@1 s@1, which is comparable tothat of Co4POM, whereas other catalysts [Cp*RhIII(L)(H2O)]2 +

afford much smaller rate constants.[148] [Cp*RhII(4-dcbpy)(H2O)]+

is further reduced by electron transfer with [RuII(bpy)3]2+* to

produce [Cp*RhI(4-dcbpy)(H2O)], which reacts with a proton toafford the Rh–hydride complex [Cp*RhIII(4-dcbpy)(H)]+ . The re-

gioselective 1,4-reduction of NAD(P)+ by [Cp*RhIII(4-

dcbpy)(H)]+ occurs to yield NAD(P)H,[144–147, 149–151] accompaniedby regeneration of [Cp*RhIII(4-dcbpy)(H2O)]2 + (Scheme 2).[148] As

indicated by the highest reactivity of [Cp*RhIII(4-dcbpy)(H2O)]2 +

for the oxidative quenching of [RuII(bpy)3]2 +* (see above), theyield of NADH is the highest among the Rh complexes(Figure 10).[148] The yield of NADH (10.7 %) obtained with

Co4POM increased to 70.7 % when TEOA was used as a sacrifi-cial electron donor.

Nicotinamide cofactor photogeneration was combined with

redox enzymatic synthesis of l-glutamate with NAD(P)H asshown in Scheme 3, where [Cp*RhIII(4-dcbpy)](H2O)]2 + exhibit-

ed the highest activity for the production of l-glutamate.[148]

Willner et al. pioneered this type of reaction, reporting the

photodriven NAD(P)H regeneration, which was coupled to a

number of secondary enzyme-catalyzed reactions (for example:reduction of butan-2-one to form butan-2-ol, reduction of ace-

toacetic acid to produce b-hydroxybutyric acid, formation ofalanine through reductive amination of pyruvic acid, and re-

ductive amination of a-oxoglutaric acid to glutamic acid).[152, 153]

The products were found to demonstrate high optical purity

Figure 9. A) Cyclic voltammograms of the Hase/PhBL/ATPase-modified elec-trode in a phosphate buffer solution (0.10 m, pH 8.0), which was activated byH2 incubation (solid line) and under N2 gas prior to activation (dashed line).The star corresponds to the applied redox potential (0.15 V vs. SCE) requiredfor the ATP synthesis at a scan rate of 10 mV s@1 at 308C. B) Time course ofthe ATP synthesis from ADP and Pi in a phosphate buffer solution (0.10 m,pH 8.0) at the applied potential of 0.15 V vs. SCE and under one atmosphericpressure of H2 by use of Hase/PhBL/ATPase-modified electrode (black solidcircles), PhBL/ATPase-modified electrode (gray filled circles), and Hase/PhBL-modified electrode (gray open circles) electrodes. Reprinted with permissionfrom Ref. [137]. Copyright 2016, WILEY-VCH Verlag GmbH.

Scheme 2. Photocatalytic cycle for the regeneration of NAD(P)H cofactorsusing water as an electron source, Co4POM as a water oxidation catalyst,[RuII(bpy)3]2 + as a photocatalyst, and a Rh complex as a NAD(P) + reductioncatalyst. Reprinted with permission from Ref. [148]. Copyright 2014, WILEY-VCH Verlag GmbH.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim127

Minireviews

and the enzymes and the coenzymes showed high turnovernumbers and stability.[152, 153] A P450-catalyzed O-dealkylation

reaction was also coupled to photodriven NAD(P)H regenera-tion using TEOA as a sacrificial electron donor, Eosin Y as an or-ganic photocatalyst, and [Cp*RhIII(bpy)(H2O)]2 + as an NADP+

reduction catalyst.[154]

A photoelectrochemical (PEC) cell was constructed for NADH

regeneration using water as an electron source as shown inFigure 11, where a cobalt phosphate (Co-Pi)-deposited hema-tite (a-Fe2O3) is used as a photoanode for photocatalytic wateroxidation and [Cp*RhII(bpy)(H2O)]+ is used as a cathode for re-

gioselective NADH regeneration from NAD+ , and formate de-hydrogenase (FDH) is used as a CO2 reduction enzyme.[155]

Under visible-light irradiation, the a-Fe2O3 photoelectrode ab-

sorbs solar energy to drive water oxidation catalyzed by cobaltphosphate (Co-Pi).

[155]

Electrons produced by photodriven water oxidation aretransferred to the [Cp*RhII(bpy)H2O]+-modified cathode for the

regioselective 1,4-reduction of NAD+ to produce NADH,

whereas NADH is oxidized as a redox counterpart for FDH-cat-alyzed reduction of CO2 to form formate.[155] The NADH yield

increased up to 68 % with an increase in the external bias from0.80 to 1.20 V. This indicates that the PEC cell platform still re-

quires additional driving force such as the external bias for re-generation of NADH using water as an electron source.[155] The

PEC cell system in Figure 11 performed better than the majori-ty of homogeneous colloidal systems that typically require or-

ganic sacrificial electron donors such as TEOA.[156–161] Further-more, the rate of NADH regeneration in the PEC system was

7.5 times faster than the rate in the [RuII(bpy)3]2+-photocata-lyzed homogeneous colloidal system in which water is used as

an electron source (Scheme 2 and Figure 10).[155]

A silicon-based PEC cell composed of cobalt phosphate (Co-Pi)-deposited triple junction silicon on ITO (3-jn-Si/ITO/Co-Pi) as

a photoanode with a formate dehydrogenase from Thiobacillussp. (TsFDH) was also reported for visible-light-driven electro-

chemical CO2 reduction to formate through NADH regenera-tion with a Faradaic efficiency of 16.2 % at an applied biaspotential of 1.80 V.[162]

3.2. Production of NAD(P)H with H2

Regioselective hydrogenation of NAD+ to NADH has success-fully been achieved using H2 as a reductant, which can be ob-tained by solar-driven water splitting [Eq. (4)] ,[83–97] a cyclome-

talated organoiridium complex [IrIII(Cp*)(4-(1H-pyrazol-1-yl-kN2)benzoic acid-kC3)(H2O)]2·SO4 ([1]2·SO4) as a catalyst fro re-gioselective reduction of NAD+ to NADH under one atmos-

pheric pressure of H2 at 298 K in a neutral or weakly basicaqueous solution (Scheme 4).[163] At pH>7, the benzoic acid

moiety in 1 is deprotonated to afford the benzoate form(2).[163] 2 reacts with H2 to produce the IrIII–hydride complex (3)

that reduces NAD+ regioselectively to produce NADH, accom-

panied by regeneration of 2 with H2O (Scheme 4).[164] The rate-determining step in the catalytic cycle is the formation of the

IrIII–hydride complex (3) in the reaction of 2 with H2.[164] Therate constant (kobs) of formation of 3 under one atmospheric

pressure of H2 at pH 7.0 was determined to be 6.3 V 10@2 s@1 at298 K.[164] The same catalyst (2) was also effective for the reduc-

Figure 10. Time profiles of production of NADH in the photocatalytic reduc-tion of NAD+ coupled by water oxidation with [Cp*RhIII(L)(H2O)]2+ (L = bpy,4-dmbpy, 5-dmbpy and 4-dcbpy). Reprinted with permission from Ref. [148].Copyright 2014, WILEY-VCH Verlag GmbH.

Scheme 3. Photocatalytic cycle for the regeneration of NAD(P)H cofactorsusing water as an electron source, Co4POM as a water oxidation catalyst,[Ru(bpy)3]2 + as a photocatalyst, and a Rh complex as a NAD(P)+ . Reprintedwith permission from Ref. [148]. Copyright 2014, WILEY-VCH Verlag GmbH.

Figure 11. Photoelectrocatalytic production of formate by CO2 reduction viageneration of NADH under visible-light illumination using hematite as aphotoanode for water oxidation with cobalt phosphate (Co-Pi) and[Cp*RhII(bpy)(H2O)]+ as a cathode catalyst for regioselective reduction ofNAD+ to NADH and formate dehydrogenase from Thiobacillus sp. KNK65MA(TsFDH) as an enzyme for formation of formate by CO2 reduction withNADH. Reprinted with permission from Ref. [155]. Copyright 2016, RoyalSociety of Chemistry.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim128

Minireviews

tion of CO2 by H2 to produce formate through formation ofspecies 3.[165]

Carbon black particles modified with a hydrogenase from E.coli and NAD+ reductase (SHI64A protein from R. eutropha

HF210 (pGE749)) were reported to catalyze the regioselectivereduction of NAD+ by H2 to generate NADH as shown in

Figure 12.[165] A high turnover frequency of 24 s@1 was obtained

for generation of NADH per second per NAD+ reductase witha TON = 53 100.[165] A key advantage of the immobilization of

NAD+ recycling enzymes in the carbon black particles is thatthey can be easily recovered from a batch reaction and repeat-

edly reused.[165] The reaction of NAD+ (1 mm) with H2 in thepresence of NAD+-reductase-immobilized carbon black parti-

cles initially yielded 25 % NADH. The carbon black catalyst par-

ticles were then separated from the reaction mixture by meansof centrifugation and were re-suspended in a fresh H2-saturat-

ed NAD+ solution (1 mm) three times. The reused particlesshowed 76, 64, and 46 % of the original activity in the 2nd, 3rd

and 4th cycles, respectively.[165]

The NADH recycling system was then utilized to provideNADH to an NADH-dependent enzyme such as an alcohol de-

hydrogenase (ADH) for the hydrogenation of acetophenone to

produce phenylethanol.[165] The initial activity (mol s@1 per molof NAD+ reductase) of the co-immobilized catalyst with all

three enzymes was 1.41 s@1, which is doubled as comparedwith 0.74 s@1 for the alcohol dehydrogenase (ADH) enzyme

employed in solution.[165] The total TON was over 130 000,demonstrating that the H2-driven cofactor recycling catalytic

system is quite robust over many catalytic cycles.[165]

A hydrogenase and NAD+ reductase were also co-immobi-lized on a carbon-nanotube-lined quartz column (CNC) in elec-

tronic contact, allowing for the electrons produced by H2 oxi-dation by the hydrogenase to be efficiently provided for regio-selective reduction of NAD+ with H2 to produce NADH with aTON of 18000.[166] An (S)-selective ADH (ADH 105 enzyme) was

further co-immobilized on a CNC modified with hydrogenaseand NAD+ reductase for enantioselective ketone reduction. A

H2-saturated reaction mixture that contained NAD+ (1 mm)

and acetophenone (8.7 mm) was continuously recycled byusing a CNC that was modified with hydrogenase, NAD+ re-

ductase and ADH 105 for 24 h to yield 1-phenylethanol with-out any by-products.[166]

A catalytic NADH regeneration with H2 was also reportedusing a heterogeneous catalyst (Pt/Al2O3), which was combined

with an ADH at ambient pressure. Employing this system, it

was found that NADH yield and turnover frequency (TOF) in-creased with increasing temperature (from 20 to 37 8C) and

pH value (from 4.0 to 9.9).[167] The NADH regeneration by heter-ogeneous catalysis has provided a cleaner and more conven-

ient alternative to currently used enzymatic and homogeneousphotocatalytic and electrocatalytic techniques with the added

benefit of straightforward separation of the catalyst.[165–171] The

viability of coupling NADH regeneration with enzymatic reac-tions has been established in the reduction of aldehyde to al-

cohol such as propanal to propanol with H2, where the alcoholyield reached 100 %.[167] Although H2 can be produced by solar-

driven water splitting [Eq. (4)] ,[83–97] NADH regeneration has yetto be combined with solar-driven water splitting.

4. Production of H2O2

4.1. Production of H2O2 from H2 and O2

Hydrogen peroxide (H2O2) is a highly active and environmen-tally friendly oxidant that is frequently used in the manufacture

of numerous organic and inorganic compounds in chemical in-dustry.[172–177] It should be noted that H2O2 is also a product innatural photosynthesis.[18–28] The current industrial process for

H2O2 production consists of the Pd-catalyzed hydrogenation ofalkylanthraquinone with H2 and oxidation of the resulting alky-

lanthrahydroquinone with O2, which are not environmentallybenign because of many disadvantages, such as requiring

toxic solvents, large consumption of energy, and multiple

steps.[178–181] Thus, extensive efforts have been devoted to ach-ieve the direct synthesis of H2O2 from H2 and O2 as an alterna-

tive to current indirect methods using precious heterogeneousmetal catalysts (mainly Pd, Au, or Au–Pd).[180–185]

Direct synthesis of H2O2 from H2 and O2 in water has beenmade possible using the [C,N]-cyclometalated organoiridium

Scheme 4. Catalytic cycle for the regioselective reduction of NAD+ by H2

with a cyclometalated organoiridium complex (2) at pH 7. Reprinted withpermission from Ref. [163]. Copyright 2012, American Chemical Society.

Figure 12. The enzyme-modified particle system composed of a hydroge-nase (green) for oxidation of H2 and transfer of the electrons into theenzyme-modified particle through a chain of FeS clusters (spheres shown inelemental colors) with the co-immobilized NAD+ reductase (blue) for the re-gioselective reduction of NAD+ to produce NADH. Reprinted with permis-sion from Ref. [165]. Copyright 2015, WILEY-VCH Verlag GmbH.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim129

Minireviews

complex (2) in Scheme 4 combined with flavin mononucleo-

tide (FMN) at room temperature as shown in Scheme 5.[186] TheIrIII–hydride complex (3) reduces FMN to FMNH2, followed by

the reduction of O2 to produce H2O2,[187, 188] accompanied by re-generation of FMN. Without FMN, the four-electron/four

proton reduction of O2 by 3, which was generated by reacting2 with H2, would afford H2O instead of H2O2.[186] The stoichio-

metric amount of H2O2 was produced when the concentration

of FMN was changed for the stepwise reduction of FMN by H2

with 2 to generate FMNH2, followed by the oxidation of

FMNH2 by O2 to produce H2O2 as shown in Figure 13, wherethe concentration of produced H2O2 was the same as that of

FMN loaded at the beginning of the reaction irrespective ofthe concentration of FMN.[186] When Sc(NO3)3 (100 mm) was

added to an aqueous phosphate buffer solution (pH 6.0) for

the direct synthesis of H2O2 from H2 and O2 with 2 and FMN,the amount of H2O2 was dramatically increased to attain a TON

of 847 with respect to 2 in 4 h.[186] The rate of catalytic forma-tion of H2O2 increased with increasing [Sc3 +] to reach TOF =

50 h@1.[186]

As shown in Scheme 4, NADH is produced by the catalytic

reduction of NAD+ by H2.[163] In such a case H2O2 is producedfrom NADH and O2 as shown in Scheme 6, where a water-solu-

ble IrIII complex (2) reacts with NADH to produce the IrIII–hy-dride complex (3), which reduces a ubiquinone coenzyme ana-

logue (Q0) to the hydroquinone (Q0H2) followed by reductionof O2 with Q0H2 to produce H2O2, accompanied by regenera-

tion of 2 and Q0 in water at pH 8.[189] Thus, the overall catalytic

reduction of O2 by NADH proceeds to generate H2O2 in thepresence of 2 and a ubiquinone coenzyme analogue (Q0) that

acts as a cocatalyst.[189]

4.2. Solar-Driven Production of H2O2

H2O2 is produced directly from H2O and O2 without any elec-tron source such as H2 and NADH under visible-light irradiation

by using [RuII(Me2phen)3]2 + (Me2phen = 4,7-dimethyl-1,10-phe-

nanthroline) as a photocatalyst, water as an electron source,and [(Cp*)CoIII(bpy)(H2O)]2 + as an efficient water oxidation cat-

alyst in the presence of Sc(NO3)3 as shown in Scheme 7.[190, 191]

Photoinduced electron transfer from the excited state of[RuII(Me2phen)3]2+ ([RuII(Me2phen)3]2 +*) to O2 occurs to produce[RuII(Me2phen)3]3+ and O2C@ to which Sc3 + is bound to produce

the O2C@–Sc3 + complex, which was detected by EPR spectrosco-py with superhyperfine coupling resulting from the scandiumnuclear spin (I = 7/2) in solution (pathway b in Scheme 7).[192, 193]

The strong binding of Sc3 + to O2C@ resulted in prohibition ofback electron transfer from O2C@ to [RuIII(Me2phen)3]3+ and gen-

eration of [RuII(Me2phen)3]2 + .[190] The O2C@–Sc3 + complex dispro-portionates with protons to yield H2O2 (pathway c in

Scheme 7).[190, 191]

Time courses of visible-light-driven generation of[RuIII(Me2phen)3]3 + and H2O2 in pathways b and c in Scheme 7

are shown in Figure 14 to establish the stoichiometry of thetwo-electron/two-proton reduction of O2 by [RuII(Me2phen)3]2 +

[Eq. (9)]:[191]

Scheme 5. Catalytic cycles for direct synthesis of H2O2 from H2 and O2 with acyclometalated organoiridium complex (2) and FMN in water. Reprinted withpermission from Ref. [186]. Copyright 2013, WILEY-VCH Verlag GmbH.

Figure 13. Plot of concentration of H2O2 produced by the catalytic two-elec-tron/two-proton reduction of O2 by FMNH2 that was generated by the two-electron/two-proton reduction of FMN by 3, which was produced by thetwo-electron-two proton reduction of 2 (25 mm) with H2 in an aqueous phos-phate buffer solution (pH 6.0) vs. concentration of FMN (25 mm @1.0 mm)loaded at the beginning of the reaction at 298 K. Reprinted with permissionfrom Ref. [186]. Copyright 2013, WILEY-VCH Verlag GmbH.

Scheme 6. Overall catalytic cycle for selective H2O2 generation from NADHand O2 with a cyclometalated organoiridium complex (2) and a ubiquinonecoenzyme analogue, 2,3-dimethoxy-5-methyl-1,4-benzoquinone (Q0), whichacts as a cocatalyst in water. Reprinted with permission from Ref. [189].Copyright 2016, American Chemical Society.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim130

Minireviews

The rate constants (ket) of photoinduced electron transfer from[RuII(Me2phen)3]2+* to O2 in the absence and presence of

Sc(NO3)3 are close to the diffusion-limited value, indicating that

the binding of Sc(NO3)3 to O2C@ is much faster than the photo-induced electron transfer from [RuII(Me2phen)3]2 +* to O2.[190]

The catalytic water oxidation by [RuIII(Me2phen)3]3 + with[(Cp*)CoIII(bpy)(H2O)]2 + to evolve O2 (reaction pathway a in

Scheme 7) was confirmed as shown in Figure 15, where the O2

yield increased with increasing concentration of

[(Cp*)CoIII(bpy)(H2O)]2 + to approach 100 % (one quarter of theinitial concentration of [RuIII(Me2phen)3]3 +).[191] The combination

of photochemical reduction of O2 with [RuII(Me2phen)3]2 + in

the presence of Sc(NO3)3 and the catalytic oxidation of water

by [RuIII(Me2phen)3]3 + resulted in photocatalytic production ofH2O2 from H2O and O2 [Eq. (10)]:[190]

The TON of photocatalytic production of H2O2 based on[RuII(Me2phen)3]2+ was determined to be 612 after 9 h photoir-

radiation.[190] The TON based on [(Cp*)CoIII(bpy)(H2O)]2 + was

also determined to be 61 after 9 h photoirradiation.[190] Thequantum yield (F) of the photocatalytic H2O2 production

under visible-light irradiation at l= 450 nm was determined byuse of a ferrioxalate actinometer to be 37 %, and the solar

energy conversion efficiency from solar energy to chemicalenergy was also determined using a solar simulator (1 sun) to

be 0.25 %,[190] which is higher than the solar energy conversionefficiency of switchgrass (0.2 %) that is a promising biofuel.[194]

Ever since the first report on the photocatalytic production

of H2O2 from H2O and O2 in Scheme 7,[190] there have been anumber of papers reported on the photodriven production ofH2O2 from H2O and O2 in one-compartment cells.[195–208] Howev-

er, a concentration of H2O2 higher than 10 mm has yet to beattained in a one-compartment cell. The highest concentration

of H2O2 was reported by use of a two-compartment cell(Figure 16), which consists of a narrow-band-gap semiconduc-

tor photocatalyst for oxidation of H2O (surface-modified BiVO4

with FeO(OH))[209] and a cobalt chlorin complex [CoII(Ch)] as aselective electrocatalyst for the two-electron/two-proton re-

duction of O2,[210, 211] separated by a Nafion membrane under si-mulated solar light irradiation.[212] Time courses of H2O2 produc-

tion with the FeO(OH)/BiVO4/FTO photoanode and theCoII(Ch)/carbon paper cathode in pure water at pH 1.3 are

Scheme 7. Photodriven production of H2O2 by the combination of oxidativequenching of [Ru(Me2phen)3]2 + * with O2 (pathway b) and water oxidation by[Ru(Me2phen)3]3 + with [(Cp*)CoIII(bpy)(H2O)]2 + (pathway a) in the presence ofSc(NO3)3.[190, 191] The disproportionation of HO2C affords H2O2 (pathway c). Re-printed with permission from Ref. [191]. Copyright 2017, Royal Society ofChemistry.

Figure 14. Time courses of production of [RuIII(Me2phen)3]3 + (red circles) andH2O2 (blue circles) in the photocatalytic oxidation of [RuII(Me2phen)3]2+ by O2

under photoirradiation (white light) of an air-saturated solvent mixture ofMeCN and H2O (v/v = 23:2) containing [RuII(Me2phen)3]2 + (100 mm) in thepresence of Sc(NO3)3 (100 mm) at 298 K. Reprinted with permission fromRef. [191] . Copyright 2017, Royal Society of Chemistry.

Figure 15. Time courses of O2 evolution observed in the catalytic water oxi-dation by [RuIII(Me2phen)3]3 + (1.0 mm) with [(Cp*)CoIII(bpy)(H2O)]2 + [10 mm(red), 50 mm (orange), 100 mm (green), and 200 mm (blue)] in the presence ofSc(NO3)3 (100 mm) in a deaerated solvent mixture of MeCN and H2O (v/v = 9:1, 1.0 mL) at 298 K. Reprinted with permission from Ref. [191].Copyright 2017, Royal Society of Chemistry.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim131

Minireviews

shown in Figure 17 (red circles), where the maximum concen-

tration of H2O2 reached 60 mm.[212] The highest solar energyconversion efficiency of H2O2 production in pure water was ob-

tained as 6.6 % under simulated solar irradiation adjusted to0.05 sun after a photocatalytic reaction for 1 h (0.89 % under 1

sun irradiation).[212]

In contrast to the case when BiVO4 and FeO(OH) were re-

placed by WO3 that is activated by seawater to afford more

H2O2,[213] in the case of FeO(OH)/BiVO4/FTO photoanodesystem, seawater or an NaCl aqueous solution deactivated the

photocatalyst due to the instability of BiVO4 in the presence ofCl@ under solar irradiation (blue circles and squares in

Figure 17).[212] The conversion of chemical energy into electricenergy has been achieved using H2O2, which is produced by

the photocatalytic oxidation of H2O with O2 as a fuel in H2O2

fuel cells,[213–217] where an open-circuit potential of 0.79 V and amaximum power density of 2.0 mW cm@2, respectively, were re-

corded.[212] The energy conversion efficiency of the H2O2 fuelcell was evaluated to be about 50 % by the measurements of

output energy as electrical energy versus consumed chemical

energy of H2O2, which is comparable to the efficiency of a H2

fuel cell.[213]

5. Conclusion

Products of natural photosynthesis, such as ATP, NAD(P)H andH2O2, can be obtained by artificial photosynthesis. ATP is pro-

duced by using an artificial photosynthetic membrane, com-posed of a photosynthetic reaction center mimic that pumps

protons into the interior of the liposome and the F-type ATPsynthase enzyme that was incorporated into the membrane.

ATP can also be synthesized using H2 as a fuel using a mem-

brane-bound NiFeSe hydrogenase and an F0F1-ATPase, whichare co-immobilized on a flat gold electrode surface with a lipid

membrane. NAD(P)H is produced by photocatalytic reductionof NAD(P)+ using water as an electron source,

[Co4(H2O)2(PW9O34)2]10@ [Co4(POM)] as a water oxidation cata-lyst, [Ru(bpy)3]2 + as a photocatalyst, and [Cp*Rh(4-dmbpy)-

(H2O)]2 + as a NAD(P)+ reduction catalyst. The photoelectro-

chemical cell is also applied for NADH regeneration usingwater as an electron source, consisting of a cobalt phosphate(Co-Pi)-deposited hematite (a-Fe2O3) photoelectrode for photo-catalytic water oxidation and a cathode catalyst for the regio-

selective reduction of NAD+ to NADH. Regioselective 1,4-hy-drogenation of NAD+ to NADH has also been achieved using

H2 as a reductant, which can be obtained by solar-driven watersplitting [Eq. (4)] in the presence of a catalytic amount of a cy-clometalated organoiridium complex under one atmospheric

pressure of H2 at room temperature in a neutral or weaklybasic aqueous solution. Direct synthesis of H2O2 from H2 and

O2 has been made possible by combining the cyclometalatedorganoiridium complex catalyst with flavin mononucleotide.

H2O2 can be produced directly from H2O and O2 in the air bycombining the photocatalytic two-electron/two-proton reduc-

tion of O2 to H2O2 and the catalytic four-electron/four-proton

oxidation of H2O under solar light irradiation. The energy con-version efficiency has reached 6.6 % under 0.05 sun irradiation.

Further combination of solar-light-driven water splitting withproduction of ATP, NAD(P)H and H2O2 would provide promising

ways of producing the same products as those of naturalphotosynthesis with higher efficiency and simplicity.

Acknowledgements

The authors acknowledge very much the contributions of their

collaborators and co-workers cited in the listed references, andsupport by a SENTAN project (to S.F.) from Japan Science and

Technology Agency (JST), JSPS KAKENHI (No. 16H02268 to S.F.),the NRF of Korea through CRI (NRF-2012R1A3A2048842 to W.N.),GRL (NRF-2010-00353 to W.N.), and Basic Science ResearchProgram (2017R1D1A1B03029982 to Y.-M.L. and2017R1D1A1B03032615 to S.F.).

Conflict of interest

The authors declare no conflict of interest.

Figure 16. A schematic reaction diagram of a two-compartment photoelec-trochemical cell for H2O2 production from H2O and O2. Reprinted with per-mission from Ref. [212]. Copyright 2016, American Chemical Society.

Figure 17. Time courses of H2O2 production with the FeO(OH)/BiVO4/FTOphotoanode and the CoII(Ch)/carbon paper cathode in pure water at pH 1.3(red circles), in seawater at pH 1.3 (blue circles) and in an NaCl aqueous solu-tion at pH 1.3 (blue squares) under simulated 1 sun (AM 1.5G, 100 mW cm@2)illumination. Time course of H2O2 production in the absence of CoII(Ch) oncarbon paper under simulated 1 sun (AM 1.5G, 100 mW cm@2) illumination inpure water at pH 1.3 is shown as black circles. Reprinted with permissionfrom Ref. [212]. Copyright 2016, American Chemical Society.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim132

Minireviews

Keywords: artificial photosynthesis · ATP · hydrogen

peroxide · NAD(P)H · water oxidation

[1] D. S. Gray, N. Yeerxiati, In Green Photo-active Nanomaterials: SustainableEnergy and Environmental Remediation, N. Nuraje, R. Asmatulu, G. Mul,Eds. ; RSC Green Chem. Ser. , 2016, Chap. 4, p. 64 – 91, RSC Publishing.

[2] N. Sekar, R. P. Ramasamy, J. Photochem. Photobiol. C 2015, 22, 19 – 33.[3] M. E. El-Khouly, E. El-Mohsnawy, S. Fukuzumi, J. Photochem. Photobiol.

C 2017, 31, 36 – 83.[4] K. Hasan, R. D. Milton, M. Grattieri, T. Wang, M. Stephanz, S. D. Minteer,

ACS Catal. 2017, 7, 2257 – 2265.[5] S. K. Ravi, S. C. Tan, Energy Environ. Sci. 2015, 8, 2551 – 2573.[6] A. A. Boghossian, M.-H. Ham, J. H. Choi, M. S. Strano, Energy Environ.

Sci. 2011, 4, 3834 – 3843.[7] G. Renger, Curr. Sci. 2010, 98, 1305 – 1310.[8] Y. Mazor, A. Borovikova, I. Caspy, N. Nelson, Nat. Plants 2017, 3, 17014.[9] T. Shikanai, Photosynth. Res. 2016, 129, 253 – 260.

[10] X. Qin, M. Suga, T. Kuang, J.-R. Shen, Science 2015, 348, 989 – 995.[11] M. Suga, X. Qin, T. Kuang, J.-R. Shen, Curr. Opin. Struct. Biol. 2016, 39,

46 – 53.[12] J. Yano, V. Yachandra, Chem. Rev. 2014, 114, 4175 – 4205.[13] M. M. Najafpour, G. Renger, M. Hołynska, A. N. Moghaddam, E.-M. Aro,

R. Carpentier, H. Nishihara, J. J. Eaton-Rye, J.-R. Shen, S. I. Allakhverdiev,Chem. Rev. 2016, 116, 2886 – 2936.

[14] M. M. Najafpour, S. Heidari, S. E. Balaghi, M. Hołynska, M. H. Sadr, B.Soltani, M. Khatamian, A. W. Larkum, S. I. Allakhverdiev, Biochim. Bio-phys. Acta 2017, 1858, 156 – 174.

[15] J.-R. Shen, Annu. Rev. Plant Biol. 2015, 66, 23 – 48.[16] S. Paul, F. Neese, D. A. Pantazis, Green Chem. 2017, 19, 2309 – 2325.[17] M. Suga, F. Akita, M. Sugahara, M. Kubo, Y. Nakajima, T. Nakane, K. Ya-

mashita, Y. Umena, M. Nakabayashi, T. Yamane, T. Nakano, M. Suzuki, T.Masuda, S. Inoue, T. Kimura, T. Nomura, S. Yonekura, L.-J. Yu, T. Saka-moto, T. Motomura, J.-H. Chen, Y. Kato, T. Noguchi, K. Tono, Y. Joti, T.Kameshima, T. Hatsui, E. Nango, R. Tanaka, H. Naitow, Y. Matsuura, A.Yamashita, M. Yamamoto, O. Nureki, M. Yabashi, T. Ishikawa, S. Iwata,J.-R. Shen, Nature 2017, 543, 131 – 135.

[18] A. H. Mehler, Arch. Biochem. Biophys. 1951, 33, 65 – 77.[19] A. Mehler, Arch. Biochem. Biophys. 1951, 34, 339 – 351.[20] A. Mehler, A. H. Brown, Arch. Biochem. Biophys. 1952, 38, 365 – 370.[21] M. R. Badger, S. von Caemmerer, S. Ruuska, H. Nakano, Phil. Trans. R.

Soc. Lond. B 2000, 355, 1433 – 1446.[22] K. Asada, Phil. Trans. R. Soc. Lond. B 2000, 355, 1419 – 1431.[23] P. Posp&sil, Biochim. Biophys. Acta 2009, 1787, 1151 – 1160.[24] C. Miyake, Plant Cell Physiol. 2010, 51, 1951 – 1963.[25] P. Posp&sil, Biochim. Biophys. Acta Bioenerg. 2012, 1817, 218 – 231.[26] M. M. Borisova, M. A. Kozuleva, N. N. Rudenko, I. A. Naydov, I. B. Kleni-

na, B. N. Ivanov, Biochim. Biophys. Acta Bioenerg. 2012, 1817, 1314 –1321.

[27] S. Fukuzumi, Biochim. Biophys. Acta Bioenerg. 2016, 1857, 604 – 611.[28] T. Roach, C. S. Na, A. Krieger-Liszkay, Plant J. 2015, 81, 759 – 766.[29] D. Gust, T. A. Moore, A. L. Moore, Acc. Chem. Res. 2009, 42, 1890 – 1898.[30] M. Wang, W. Zhan, Acc. Chem. Res. 2016, 49, 2551 – 2559.[31] K. L. Mulfort, L. M. Utschig, Acc. Chem. Res. 2016, 49, 835 – 843.[32] D. L. Ashford, M. K. Gish, A. K. Vannucci, M. K. Brennaman, J. L. Temple-

ton, J. M. Papanikolas, T. J. Meyer, Chem. Rev. 2015, 115, 13006 – 13049.[33] L. Hammarstrçm, Acc. Chem. Res. 2015, 48, 840 – 850.[34] D. M. Guldi, Chem. Soc. Rev. 2002, 31, 22 – 36.[35] S. Fukuzumi, Org. Biomol. Chem. 2003, 1, 609 – 620.[36] S. Fukuzumi, Bull. Chem. Soc. Jpn. 2006, 79, 177 – 195.[37] F. D’Souza, O. Ito, Chem. Commun. 2009, 4913 – 4928.[38] S. Fukuzumi, T. Kojima, J. Mater. Chem. 2008, 18, 1427 – 1439.[39] S. Fukuzumi, Phys. Chem. Chem. Phys. 2008, 10, 2283 – 2297.[40] F. D’Souza, O. Ito, Chem. Soc. Rev. 2012, 41, 86 – 96.[41] S. Fukuzumi, T. Honda, K. Ohkubo, T. Kojima, Dalton Trans. 2009,

3880 – 3889.[42] S. Fukuzumi, K. Ohkubo, J. Mater. Chem. 2012, 22, 4575 – 4587.[43] M. J. Llansola-Portoles, D. Gust, T. A. Moore, A. L. Moore, C. R. Chimie

2017, 20, 296 – 313.[44] M. Rudolf, S. V. Kirner, D. M. Guldi, Chem. Soc. Rev. 2016, 45, 612 – 630.

[45] S. Fukuzumi, K. Ohkubo, T. Suenobu, Acc. Chem. Res. 2014, 47, 1455 –1464.

[46] M. E. El-Khouly, S. Fukuzumi, F. D’Souza, ChemPhysChem 2014, 15, 30 –47.

[47] C. B. KC, F. D’Souza, Coord. Chem. Rev. 2016, 322, 104 – 141.[48] S. Fukuzumi, K. Ohkubo, F. D’Souza, J. L. Sessler, Chem. Commun. 2012,

48, 9801 – 9815.[49] V. Strauss, A. Roth, M. Sekita, D. M. Guldi, Chemistry 2016, 1, 531 – 556.[50] S. Fukuzumi, ECS J. Solid State Sci. Technol. 2017, 6, M3055 – M3061.[51] K. Ladomenou, V. Nikolaou, G. Charalambidis, A. Charisiadis, A. G. Cout-

solelos, C. R. Chim. 2017, 20, 314 – 322.[52] Y.-J. Yuan, Z.-T. Yu, D.-Q. Chen, Z.-G. Zou, Chem. Soc. Rev. 2017, 46,

603 – 631.[53] J. Willkomm, K. L. Orchard, A. Reynal, E. Pastor, J. R. Durrant, E. Reisner,

Chem. Soc. Rev. 2016, 45, 9 – 23.[54] S. Fukuzumi, Curr. Opin. Chem. Biol. 2015, 25, 18 – 26.[55] Z. Yu, F. Li, L. Sun, Energy Environ. Sci. 2015, 8, 760 – 775.[56] S. Fukuzumi, Y. Yamada, T. Suenobu, K. Ohkubo, H. Kotani, Energy Envi-

ron. Sci. 2011, 4, 2754 – 2766.[57] J. Su, L. Vayssieres, ACS Energy Lett. 2016, 1, 121 – 135.[58] S. Fukuzumi, D. Hong, Y. Yamada, J. Phys. Chem. Lett. 2013, 4, 3458 –

3467.[59] S. Fukuzumi, Y. Yamada, J. Mater. Chem. 2012, 22, 24284 – 24296.[60] W. Zhang, W. Lai, R. Cao, Chem. Rev. 2017, 117, 3717 – 3797.[61] T. K. Michaelos, D. Y. Shopov, S. B. Sinha, L. S. Sharninghausen, K. J.

Fisher, H. M. C. Lant, R. H. Crabtree, G. W. Brudvig, Acc. Chem. Res.2017, 50, 952 – 959.

[62] B. M. Hunter, H. B. Gray, A. M. Meller, Chem. Rev. 2016, 116, 14120 –14136.

[63] S. Fukuzumi, J. Jung, Y. Yamada, T. Kojima, W. Nam, Chem. Asian J.2016, 11, 1138 – 1150.

[64] M. D. K-rk-s, B. akermark, Dalton Trans. 2016, 45, 14421 – 14461.[65] J. D. Blakemore, R. H. Crabtree, G. W. Brudvig, Chem. Rev. 2015, 115,

12974 – 13005.[66] X. Sala, S. Maji, R. Bofill, J. Carc&a-Antjn, J. Escriche, A. Lloget, Acc.

Chem. Res. 2014, 47, 504 – 516.[67] S. Fukuzumi, D. Hong, Eur. J. Inorg. Chem. 2014, 645 – 659.[68] M. D. K-rk-s, O. Verho, E. V. Johnston, B. akermark, Chem. Rev. 2014,

114, 11863 – 12001.[69] S. R. Lingampalli, M. M. Ayyub, C. N. R. Rao, ACS Omega 2017, 2, 2740 –

2748.[70] Y. Sohn, W. Huang, F. Taghipour, Appl. Surf. Sci. 2017, 396, 1696 – 1711.[71] D. Bae, B. Seger, P. C. K. Vesborg, O. Hansen, I. Chorkendorff, Chem.

Soc. Rev. 2017, 46, 1933 – 1954.[72] N. Serpone, A. V. Emeline, V. K. Ryabchuk, V. N. Kuznetsov, Y. M. Arte-

m’ev, S. Horikoshi, ACS Energy Lett. 2016, 1, 931 – 948.[73] W. Kim, B. A. McClure, E. Edri, H. Frei, Chem. Soc. Rev. 2016, 45, 3221 –

3243.[74] X. Chang, T. Wang, J. Gong, Energy Environ. Sci. 2016, 9, 2177 – 2196.[75] S. Xie, Q. Zhang, G. Liu, Y. Wang, Chem. Commun. 2016, 52, 35 – 59.[76] S. Aoi, K. Mase, K. Ohkubo, T. Suenobu, S. Fukuzumi, ACS Energy Lett.

2017, 2, 532 – 536.[77] J. L. White, M. F. Baruch, J. E. Pander III, 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 – 12935.

[78] Y. Yamazaki, H. Takeda, O. Ishitani, J. Photochem. Photobiol. C 2015, 25,106 – 137.

[79] D. Chen, X. Zhang, A. F. Lee, J. Mater. Chem. A 2015, 3, 14487 – 14516.[80] Y. Ma, X. Wang, Y. Jia, X. Chen, H. Han, C. Li, Chem. Rev. 2014, 114,

9987 – 10043.[81] S. Berardi, S. Drouet, L. Franc/s, C. Gimbert-SuriÇach, M. Guttentag, C.

Richmond, T. Stoll, A. Llobet, Chem. Soc. Rev. 2014, 43, 7501 – 7519.[82] W. Tu, Y. Zhou, Z. Zou, Adv. Mater. 2014, 26, 4607 – 4626.[83] Q. Wang, T. Hisatomi, Q. Jia, H. Tokudome, M. Zhong, C. Wang, Z. Pan,

T. Takata, M. Nakabayashi, N. Shibata, Y. Li, I. D. Sharp, A. Kudo, T.Yamada, K. Domen, Nat. Mater. 2016, 15, 611 – 615.

[84] Q. Wang, T. Hisatomi, Y. Suzuki, Z. Pan, J. Seo, M. Katayama, T. Mine-gishi, H. Nishiyama, T. Takata, K. Seki, A. Kudo, T. Yamada, K. Domen, J.Am. Chem. Soc. 2017, 139, 1675 – 1683.

[85] L. G. Bloor, R. Solarska, K. Bienkowski, P. J. Kulesza, J. Augustynski, M. D.Symes, L. Cronin, J. Am. Chem. Soc. 2016, 138, 6707 – 6710.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim133

Minireviews

[86] Y. Peng, G. V. Govindaraju, D. K. Lee, K.-S. Choi, T. L. Andrew, ACS Appl.Mater. Interfaces 2017, 9, 22449 – 22455.

[87] M. R. Shaner, H. A. Atwater, N. S. Lewis, E. W. McFarland, Energy Environ.Sci. 2016, 9, 2354 – 2371.

[88] C. Ding, J. Shi, Z. Wang, C. Li, ACS Catal. 2017, 7, 675 – 688.[89] B. D. Sherman, M. V. Sheridan, K.-R. Wee, S. L. Marquard, D. Wang, L.

Alibabaei, D. L. Ashford, T. J. Meyer, J. Am. Chem. Soc. 2016, 138,16745 – 16753.

[90] M. V. Sheridan, D. J. Hill, B. D. Sherman, D. Wang, S. L. Marquard, K.-R.Wee, J. F. Cahoon, T. J. Meyer, Nano Lett. 2017, 17, 2440 – 2446.

[91] J. Jia, L. C. Seitz, J. D. Benck, Y. Huo, Y. Chen, J. W. D. Ng, T. Bilir, J. S.Harris, T. F. Jaramillo, Nat. Commun. 2016, 7, 13237.

[92] E. Verlage, S. Hu, R. Liu, R. J. R. Jones, K. Sun, C. Xiang, N. S. Lewis, H. A.Atwater, Energy Environ. Sci. 2015, 8, 3166 – 3172.

[93] J. Liu, Y. Liu, N. Liu, Y. Han, X. Zhang, H. Huang, Y. Lifshitz, S.-T. Lee, J.Zhong, Z. Kang, Science 2015, 347, 970 – 974.

[94] J. Luo, J.-H. Im, M. T. Mayer, M. Schreier, M. K. Nazeeruddin, N.-G. Park,S. D. Tilley, H. J. Fan, M. Gr-tzel, Science 2014, 345, 1593 – 1596.

[95] T. Hisatomi, J. Kubota, K. Domen, Chem. Soc. Rev. 2014, 43, 7520 –7535.

[96] K. Maeda, ACS Catal. 2013, 3, 1486 – 1503.[97] A. Kudo, Y. Miseki, Chem. Soc. Rev. 2009, 38, 253 – 278.[98] Y. Zu, R. J. Shannon, J. Hirst, J. Am. Chem. Soc. 2003, 125, 6020 – 6021.[99] W. Buckel, R. K. Thauer, Biochim. Biophys. Acta Bioenerg. 2013, 1827,

94 – 113.[100] R. A. Alberty, Arch. Biochem. Biophys. 2001, 389, 94 – 109.[101] M. P. Johnson, Essays Biochem. 2016, 60, 255 – 273.[102] M. A. Schçttler, S. Z. Tjth, A. Boulouis, S. Kahlau, J. Exp. Botany 2015,

66, 2373 – 2400.[103] E. Altamura, F. Milano, R. R. Tangorra, M. Trotta, O. H. Omar, P. Stano, F.

Mavelli, Proc. Natl. Acad. Sci. USA 2017, 114, 3837 – 3842.[104] U. Armbruster, V. C. Galvis, H.-H. Kunz, D. D. Strand, Curr. Opin. Plant

Biol. 2017, 37, 56 – 62.[105] W. Junge, N. Nelson, Annu. Rev. Biochem. 2015, 84, 631 – 657.[106] Y.-G. Shu, J.-C. Yue, Z.-C. Ou-Yang, Nanoscale 2010, 2, 1284 – 1293.[107] C. von Ballmoos, A. Wiedenmann, P. Dimroth, Annu. Rev. Biochem.

2009, 78, 649 – 672.[108] W. Junge, H. Sielaff, S. Engelbrecht, Nature 2009, 459, 364 – 370.[109] M. Wikstrçm, V. Sharma, V. R. I. Kaila, J. P. Hosler, G. Hummer, Chem.

Rev. 2015, 115, 2196 – 2221.[110] S. Mukherjee, A. Warshel, Photosynth. Res. 2017, 134, 1 – 15.[111] G. Steinberg-Yfrach, P. A. Liddell, S.-C. Hung, A. L. Moore, D. Gust, T. A.

Moore, Nature 1997, 385, 239 – 241.[112] D. Gust, T. A. Moore, A. L. Moore, A. N. Macpherson, A. Lopez, J. M. De-

Graziano, I. Gouni, E. Bittersmann, G. R. Seely, F. Gao, R. A. Nieman,X. C. Ma, L. J. Demanche, S.-C. Hung, D. K. Luttrull, S.-J. Lee, P. K. Kerri-gan, J. Am. Chem. Soc. 1993, 115, 11141 – 11152.

[113] D. Gust, T. A. Moore, A. L. Moore, Acc. Chem. Res. 1993, 26, 198 – 205.[114] G. Steinberg-Yfrach, J.-L. Rigaud, E. N. Durantini, A. L. Moore, D. Gust,

T. A. Moore, Nature 1998, 392, 479 – 482.[115] I. M. Bennett, H. M. V. Farfano, F. Bogani, A. Primak, P. A. Liddell, L.

Otero, L. Sereno, J. J. Silber, A. L. Moore, T. A. Moore, D. Gust, Nature2002, 420, 398 – 401.

[116] A. Minta, J. P. Y. Kao, R. Y. Tsien, J. Biol. Chem. 1989, 264, 8171 – 8178.[117] T. Numata, T. Murakami, F. Kawashima, N. Morone, J. E. Heuser, Y.

Takano, K. Ohkubo, S. Fukuzumi, Y. Mori, H. Imahori, J. Am. Chem. Soc.2012, 134, 6092 – 6095.

[118] T. Murakami, W. Wijagkanalan, M. Hashida, K. Tsuchida, Nanomedicine2010, 5, 867 – 879.

[119] H. Imahori, K. Tamaki, D. M. Guldi, C. Luo, M. Fujitsuka, O. Ito, Y. Sakata,S. Fukuzumi, J. Am. Chem. Soc. 2001, 123, 2607 – 2617.

[120] H. Imahori, D. M. Guldi, K. Tamaki, Y. Yoshida, C. Luo, Y. Sakata, S. Fuku-zumi, J. Am. Chem. Soc. 2001, 123, 6617 – 6628.

[121] H. Imahori, Y. Sekiguchi, Y. Kashiwagi, T. Sato, Y. Araki, O. Ito, H.Yamada, S. Fukuzumi, Chem. Eur. J. 2004, 10, 3184 – 3196.

[122] D. M. Guldi, H. Imahori, K. Tamaki, Y. Kashiwagi, H. Yamada, Y. Sakata, S.Fukuzumi, J. Phys. Chem. A 2004, 108, 541 – 548.

[123] D. Curiel, K. Ohkubo, J. R. Reimers, S. Fukuzumi, M. J. Crossley, Phys.Chem. Chem. Phys. 2007, 9, 5260 – 5266.

[124] S. H. Lee, A. G. Larsen, K. Ohkubo, J. R. Reimers, S. Fukuzumi, M. J.Crossley, Chem. Sci. 2012, 3, 257 – 269.

[125] S. Bhosale, A. L. Sisson, P. Talukdar, A. Ferstenberg, N. Banerji, E. Vau-they, G. Bollot, J. Mareda, C. Rçger, F. Werthner, N. Sakai, S. Matile, Sci-ence 2006, 313, 84 – 86.

[126] D. Hvasanov, J. R. Peterson, P. Thordarson, Chem. Sci. 2013, 4, 3833 –3838.

[127] X. Xie, E. Bakker, Phys. Chem. Chem. Phys. 2014, 16, 19781 – 19789.[128] M. M. A. Kelson, R. S. Bhosale, K. Ohkubo, L. A. Jones, S. V. Bhosale, A.

Gupta, S. Fukuzumi, S. V. Bhosale, Dyes Pigm. 2015, 120, 340 – 346.[129] X. Feng, Y. Jia, P. Cai, J. Fei, J. Li, ACS Nano 2016, 10, 556 – 561.[130] W. Qi, L. Duan, K. W. Wang, X. H. Yan, Y. Cui, Q. He, J. B. Li, Adv. Mater.

2008, 20, 601 – 605.[131] H.-J. Choi, C. D. Montemagno, Nano Lett. 2005, 5, 2538 – 2542.[132] O. P. Ernst, D. T. Lodowski, M. Elstner, P. Hegemann, L. S. Brown, H. Kan-

dori, Chem. Rev. 2014, 114, 126 – 163.[133] K. Inoue, Y. Kato, H. Kandori, Trends Microbiol. 2015, 23, 91 – 98.[134] T.-J. M. Luo, R. Soong, E. Lan, B. Dunn, C. Montemagno, Nat. Mater.

2005, 4, 220 – 224.[135] C. Guti8rrez-S#nchez, D. Olea, M. Marques, V. M. Fern#ndez, I. A. C. Per-

eira, M. V8lez, A. L. De Lacey, Langmuir 2011, 27, 6449 – 6457.[136] =. Guti8rrez-Sanz, C. Tapia, M. C. Marques, S. Zacarias, M. V8lez, I. A. C.

Pereira, A. L. De Lacey, Angew. Chem. Int. Ed. 2015, 54, 2684 – 2687;Angew. Chem. 2015, 127, 2722 – 2725.

[137] =. Guti8rrez-Sanz, P. Natale, I. M#rquez, M. C. Marques, S. Zacarias, M.Pita, I. A. C. Pereira, I. Llpez-Montero, A. L. De Lacey, M. V8lez, Angew.Chem. Int. Ed. 2016, 55, 6216 – 6220.

[138] C. Wombwell, C. A. Caputo, E. Reisner, Acc. Chem. Res. 2015, 48, 2858 –2865.

[139] A. Ruff, J. Szczesny, S. Zacarias, I. A. C. Pereira, N. Plumer8, W. Schuh-mann, ACS Energy Lett. 2017, 2, 964 – 968.

[140] C. Guti8rrez-S#nchez, O. Rediger, V. M. Fern#ndez, A. L. De Lacey, M.Marques, I. A. C. Pereira, J. Biol. Inorg. Chem. 2010, 15, 1285 – 1292.

[141] Q. Yin, J. M. Tan, C. Besson, Y. V. Geletii, D. G. Musaev, A. E. Kuznetsov,Z. Luo, K. I. Hardcastle, C. L. Hill, Science 2010, 328, 342 – 345.

[142] Z. Huang, Z. Luo, Y. V. Geletii, J. W. Vickers, Q. Yin, D. Wu, Y. Hou, Y.Ding, J. Song, D. G. Musaev, C. L. Hill, T. Lian, J. Am. Chem. Soc. 2011,133, 2068 – 2071.

[143] H. Lv, J. Song, Y. V. Geletii, J. W. Vickers, J. M. Sumliner, D. G. Musaev, P.Kçgerler, P. F. Zhuk, J. Bacsa, G. Zhu, C. L. Hill, J. Am. Chem. Soc. 2014,136, 9268 – 9271.

[144] F. Hildebrand, C. Kohlmann, A. Franz, S. Letz, Adv. Synth. Catal. 2008,350, 909 – 918.

[145] H. C. Lo, O. Buriez, J. B. Kerr, R. H. Fish, Angew. Chem. Int. Ed. 1999, 38,1429 – 1432; Angew. Chem. 1999, 111, 1524 – 1527.

[146] V. Ganesan, D. Sivanesan, S. Yoon, Inorg. Chem. 2017, 56, 1366 – 1374.[147] X. Wang, T. Saba, H. H. P. Yiu, R. F. Howe, J. A. Anderson, J. Shi, Chemis-

try 2017, 2, 621 – 654.[148] J. Ryu, D. H. Nam, S. H. Lee, C. B. Park, Chem. Eur. J. 2014, 20, 12020 –

12025.[149] R. Wienkamp, E. Streckhan, Angew. Chem. Int. Ed. Engl. 1983, 22, 497 –

497.[150] K. T. Oppelt, E. Wçß, M. Stiftinger, W. Schçfberger, W. Buchberger, G.

Knçr, Inorg. Chem. 2013, 52, 11910 – 11922.[151] H. C. Lo, C. Leiva, O. Buriez, J. B. Kerr, M. M. Olmstead, R. H. Fish, Inorg.

Chem. 2001, 40, 6705 – 6716.[152] D. Mandler, I. Willner, J. Chem. Soc. Perkin Trans. 2 1986, 805 – 811.[153] I. Willner, R. Maidan, B. Willner, Isr. J. Chem. 1989, 29, 289 – 301.[154] S. H. Lee, Y.-C. Kwon, D.-M. Kim, C. B. Park, Biotechnol. Bioeng. 2013,

110, 383 – 390.[155] D. H. Nam, S. K. Kuk, H. Choe, S. Lee, J. W. Ko, E. J. Son, E.-G. Choi, Y. H.

Kim, C. B. Park, Green Chem. 2016, 18, 5989 – 5993.[156] J. H. Kim, M. Lee, J. S. Lee, C. B. Park, Angew. Chem. Int. Ed. 2012, 51,

517 – 520; Angew. Chem. 2012, 124, 532 – 535.[157] H. Y. Lee, J. Ryu, J. H. Kim, S. H. Lee, C. B. Park, ChemSusChem 2012, 5,

2129 – 2132.[158] X. Ji, C. Liu, J. Wang, Z. Su, G. Ma, S. Zhang, J. Mater. Chem. A 2017, 5,

5511 – 5522.[159] D. H. Nam, C. B. Park, ChemBioChem 2012, 13, 1278 – 1282.[160] Y.-Z. Wang, Z.-P. Zhao, R.-L. Zhou, W.-F. Liu, J. Mol. Catal. B Enzym.

2017, 133, S118 – S193.[161] J. H. Kim, D. H. Nam, C. B. Park, Curr. Opin. Biotechnol. 2014, 28, 1 – 9.

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim134

Minireviews

[162] E. J. Son, J. W. Ko, S. K. Kuk, H. Choe, S. Lee, J. H. Kim, D. H. Nam, G. M.Ryu, Y. H. Kim, C. B. Park, Chem. Commun. 2016, 52, 9723 – 9726.

[163] Y. Maenaka, T. Suenobu, S. Fukuzumi, J. Am. Chem. Soc. 2012, 134,367 – 374.

[164] Y. Maenaka, T. Suenobu, S. Fukuzumi, Energy Environ. Sci. 2012, 5,7360 – 7367.

[165] H. A. Reeve, L. Lauterbach, O. Lenz, K. A. Vincent, ChemCatChem 2015,7, 3480 – 3487.

[166] C. Zor, H. A. Reeve, J. Quinson, L. A. Thompson, T. H. Lonsdale, F.Dillon, N. Grobert, K. A. Vincent, Chem. Commun. 2017, 53, 9839 – 9841.

[167] X. Wang, H. H. P. Yiu, ACS Catal. 2016, 6, 1880 – 1886.[168] J. A. Kim, S. Kim, J. Lee, J.-O. Baeg, J. Kim, Inorg. Chem. 2012, 51,

8057 – 8063.[169] S. S. Bhoware, K. Y. Kim, J. A. Kim, Q. Wu, J. Kim, J. Phys. Chem. C 2011,

115, 2553 – 2557.[170] H. A. Reeve, P. A. Ash, H. Park, A. Huang, M. Posidias, C. Tomlinson, O.

Lenz, K. A. Vincent, Biochem. J. 2017, 474, 215 – 230.[171] B. Siritanaratkul, C. F. Megarity, T. G. Roberts, T. O. M. Samuels, M. Win-

kler, J. H. Warner, T. Happe, F. A. Armstrong, Chem. Sci. 2017, 8, 4579 –4586.

[172] B. S. Lane, K. Burgess, Chem. Rev. 2003, 103, 2457 – 2473.[173] G. De Faveri, G. Ilyashenko, M. Watkinson, Chem. Soc. Rev. 2011, 40,

1722 – 1760.[174] C. Wang, H. Yamamoto, Chem. Asian J. 2015, 10, 2056 – 2068.[175] G. Olivo, O. Cussj, M. Borrell, M. Costas, J. Biol. Inorg. Chem. 2017, 22,

425 – 452.[176] M. Yamada, K. D. Karlin, S. Fukuzumi, Chem. Sci. 2016, 7, 2856 – 2863.[177] I. Garcia-Bosch, Synlett 2017, 28, 1237 – 1243.[178] J. M. Campos-Martin, G. Blanco-Brieva, J. L. Fierro, Angew. Chem. Int.

Ed. 2006, 45, 6962 – 6984; Angew. Chem. 2006, 118, 7116 – 7139.[179] Y. Guo, C. Dai, Z. Lei, Chem. Eng. Sci. 2017, 172, 370 – 384.[180] C. Samanta, Appl. Catal. A General 2008, 350, 133 – 149.[181] J. Garc&a-Serna, T. Moreno, P. Biasi, M. J. Cocero, J.-P. Mikkola, T. O.

Salmi, Green Chem. 2014, 16, 2320 – 2343.[182] J. K. Edwards, S. J. Freakley, A. F. Carley, C. J. Kiely, G. J. Hutchings, Acc.

Chem. Res. 2014, 47, 845 – 854.[183] R. Dittmeyer, J.-D. Grunwaldt, A. Pashkova, Catal. Today 2015, 248,

149 – 159.[184] M.-g. Seo, H. J. Kim, S. S. Han, K.-Y. Lee, Catal. Surv. Asia 2017, 21, 1 –

12.[185] J. K. Edwards, G. J. Hutchings, Angew. Chem. Int. Ed. 2008, 47, 9192 –

9198; Angew. Chem. 2008, 120, 9332 – 9338.[186] S. Shibata, T. Suenobu, S. Fukuzumi, Angew. Chem. Int. Ed. 2013, 52,

12327 – 12331; Angew. Chem. 2013, 125, 12553 – 12557.[187] S. Fukuzumi, S. Kuroda, T. Tanaka, J. Am. Chem. Soc. 1985, 107, 3020 –

3027.[188] S. Fukuzumi, K. Tanii, T. Tanaka, Chem. Commun. 1989, 816 – 818.[189] T. Suenobu, S. Shibata, S. Fukuzumi, Inorg. Chem. 2016, 55, 7747 –

7754.[190] S. Kato, J. Jung, T. Suenobu, S. Fukuzumi, Energy Environ. Sci. 2013, 6,

3756 – 3764.[191] J. W. Han, J. Jung, Y.-M. Lee, W. Nam, S. Fukuzumi, Chem. Sci. 2017, 8,

7119 – 7125.

[192] S. Fukuzumi, M. Patz, T. Suenobu, Y. Kuwahara, S. Itoh, J. Am. Chem.Soc. 1999, 121, 1605 – 1606.

[193] S. Fukuzumi, K. Ohkubo, Chem. Eur. J. 2000, 6, 4532 – 4535.[194] A. Melis, Plant Sci. 2009, 177, 272 – 280.[195] Y. Isaka, S. Kato, D. Hong, T. Suenobu, Y. Yamada, S. Fukuzumi, J. Mater.

Chem. A 2015, 3, 12404 – 12412.[196] Y. Aratani, K. Oyama, T. Suenobu, Y. Yamada, S. Fukuzumi, Inorg. Chem.

2016, 55, 5780 – 5786.[197] Y. Aratani, T. Suenobu, K. Ohkubo, Y. Yamada, S. Fukuzumi, Chem.

Commun. 2017, 53, 3473 – 3476.[198] Y. Shiraishi, S. Kanazawa, Y. Kofuji, H. Sakamoto, S. Ichikawa, S. Tanaka,

T. Hirai, Angew. Chem. Int. Ed. 2014, 53, 13454 – 13459; Angew. Chem.2014, 126, 13672 – 13677.

[199] Y. Kofuji, Y. Isobe, Y. Shiraishi, H. Sakamoto, S. Tanaka, S. Ichikawa, T.Hirai, J. Am. Chem. Soc. 2016, 138, 10019 – 10025.

[200] Y. Kofuji, S. Ohkita, Y. Shiraishi, H. Sakamoto, S. Tanaka, S. Ichikawa, T.Hirai, ACS Catal. 2016, 6, 7021 – 7029.

[201] Y. Li, S. Ouyang, H. Xu, X. Wang, Y. Bi, Y. Zhang, J. Ye, J. Am. Chem. Soc.2016, 138, 13289 – 13297.

[202] R. Wang, K. Pan, D. Han, J. Jiang, C. Xiang, Z. Huang, L. Zhang, X.Xiang, ChemSusChem 2016, 9, 2470 – 2479.

[203] S. Thakur, T. Kshetri, N. H. Kim, J. H. Lee, J. Catal. 2017, 345, 78 – 86.[204] S. Lia, G. Dong, R. Hailili, L. Yang, Y. Li, F. Wang, Y. Zeng, C. Wang, Appl.

Catal. B 2016, 190, 26 – 35.[205] M. Jakesov#, D. H. Apaydin, M. Sytnyk, K. Oppelt, W. Heiss, N. S. Saricift-

ci, E. D. Głowacki, Adv. Funct. Mater. 2016, 26, 5248 – 5254.[206] K. Fuku, K. Sayama, Chem. Commun. 2016, 52, 5406 – 5409.[207] Y. Isaka, Y. Yamada, T. Suenobu, T. Nakagawa, S. Fukuzumi, RSC Adv.

2016, 6, 42041 – 42044.[208] K. Fuku, Y. Miyase, Y. Miseki, T. Funaki, T. Gunji, K. Sayama, Chem. Asian

J. 2017, 12, 1111 – 1119.[209] T. W. Kim, K. S. Choi, Science 2014, 343, 990 – 994.[210] K. Mase, K. Ohkubo, S. Fukuzumi, J. Am. Chem. Soc. 2013, 135, 2800 –

2808.[211] K. Mase, K. Ohkubo, S. Fukuzumi, Inorg. Chem. 2015, 54, 1808 – 1815.[212] K. Mase, M. Yoneda, Y. Yamada, S. Fukuzumi, ACS Energy Lett. 2016, 1,

913 – 919.[213] K. Mase, M. Yoneda, Y. Yamada, S. Fukuzumi, Nat. Commun. 2016, 7,

11470.[214] Y. Yamada, M. Yoneda, S. Fukuzumi, Energy Environ. Sci. 2015, 8, 1698 –

1701.[215] S. Fukuzumi, Y. Yamada, ChemElectroChem 2016, 3, 1978 – 1989.[216] S. Fukuzumi, Y. Yamada, Aust. J. Chem. 2014, 67, 354 – 364.[217] S. Fukuzumi, Y. Yamada, K. D. Karlin, Electrochim. Acta 2012, 82, 493 –

511.

Manuscript received: August 30, 2017

Revised manuscript received: October 25, 2017

Accepted manuscript online: November 3, 2017Version of record online: November 22, 2017

ChemPhotoChem 2018, 2, 121 – 135 www.chemphotochem.org T 2018 Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim135

Minireviews