Review Article

Mimicry and functions of photosyntheticreaction centersShunichi Fukuzumi1,2, Yong-Min Lee1 and Wonwoo Nam1

1Department of Chemistry and Nano Science, Ewha Womans University, Seoul 03760, Korea; 2Graduate School of Science and Engineering, Meijo University, Nagoya, Aichi468-8502, Japan

Correspondence: Shunichi Fukuzumi (fukuzumi@chem.eng.osaka-u.ac.jp), Yong-Min Lee (yomlee@ewha.ac.kr), Wonwoo Nam (wwnam@ewha.ac.kr)

The structure and function of photosynthetic reaction centers (PRCs) have been modeledby designing and synthesizing electron donor–acceptor ensembles including electronmediators, which can mimic multi-step photoinduced charge separation occurring inPRCs to obtain long-lived charge-separated states. PRCs in photosystem I (PSI) or/and photosystem II (PSII) have been utilized as components of solar cells to convertsolar energy to electric energy. Biohybrid photoelectrochemical cells composed ofPSII have also been developed for solar-driven water splitting into H2 and O2. Such astrategy to bridge natural photosynthesis with artificial photosynthesis is discussed inthis minireview.

IntroductionThe primary process of solar energy conversion in photosynthesis is photoinduced multi-step chargeseparation performed by the photosynthetic reaction centers (PRCs) in photosystem II (PSII), whereelectrons and protons are taken from water to generate the proton gradient and NADPH throughredox shuttle reactions in photosystem I (PSI) through the Z-scheme in Figure 1, leading to the reduc-tion of CO2 into carbohydrates [1–12]. Two photosystems in Z-scheme in Figure 1 are required forthe water oxidation coupled with the NADP+ reduction to occur, because one photosystem alone doesnot provide enough energy to drive the overall reaction. The development of efficient charge-separation systems is essential for artificial photosynthesis to produce solar fuels as alternatives offossil fuels that are the products of photosynthesis for billions years [13–16]. Thus, there have beenextensive studies on mimicry of PRCs by designing and synthesizing electron donor–acceptor ensem-bles linked with electron mediators, the photoexcitation of which results in multi-step photoinducedelectron transfer to produce charge-separated states with long lifetimes [17–32]. PRC mimics havebeen used as organic photocatalysts for hydrogen evolution from water with electron donors by use ofproton reduction catalysts such as metal nanoparticles [33–50]. In contrast, few PRC mimics havebeen used as photocatalysts for oxygen evolution from water with sacrificial electron acceptors thataccept electrons before they are used for production of fuels such as hydrogen [51–53]. There hasbeen no report on water splitting to produce both H2 and O2 with use of organic PRC mimics,although there have been extensive reports on solar-driven water splitting using inorganic semicon-ductors and metal complexes [54–61]. Light-driven H2 production has been developed by use ofPSI-catalyst hybrids that require an electron source or an applied potential [62–68]. Because the PRCin PSII contains the oxygen evolving complex that catalyzes four-electron oxidation of H2O to O2,biohybrid catalysts composed of PSII can be developed for solar-driven water splitting to produce H2

and O2 [69]. This minireview focuses on PRC model compounds that can mimic both the structureand function of PRCs. Then, how the charge-separation function of PRCs in PSI and/or PSII and thecatalytic functions of water oxidation and reduction can be combined is discussed for efficient solar

Version of Record published:9 October 2018

Received: 2 January 2018Revised: 24 June 2018Accepted: 2 July 2018

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Biochemical Society Transactions (2018) 46 1279–1288https://doi.org/10.1042/BST20170298

energy conversion to electric power and to water splitting to produce H2 and O2 by use of biohybrid photosys-tems. It is desired to develop PRC mimics that can be combined with biohybrid photosystems.

Mimicry of structure and function of PRCsPhotoinduced electron-transfer properties of natural photosystems with the reported structure of PRCs frompurple bacteria are illustrated in Figure 2 (left) [70–74]. Energy transfer from the light harvesting unit to thespecial pair (P) results in formation of the singlet excited state (P*), followed by electron transfer from theprimary donor (referred to the special pair) to the primary quinone (QA) along the L branch to produce thecharge-separated state P�+QA

�- within the time range of 200–250 ps at room temperature (Figure 2) [70–74].There is another quinone called QB next to QA, which can accept an electron from QA

·– for further charge sep-aration [70–74]. The subsequent electron transfer from QA

�- to QB occurs at the time range of 100 μs [70–74].When PRCs lack a quinone at the QB site, the electron on QA

�- recombines with the hole on P·+ with a 100 mslifetime at room temperature [70–74].Instead of bacteriochlorophylls and quinones, the related compounds such as porphyrins and fullerenes have

frequently been used to synthesize PRC model compounds that undergo multi-step photoinduced charge-separation processes (Figure 2, right) [74–90]. The ‘special pair (P)’ porphyrins ‘(MP)2’ in (MP)2Q-Q2HP-C60

(M = Zn and 2H) are connected directly through a Tröger’s base bridge on the porphyrin β-pyrrolic positionand the X-ray crystal structure of (ZnP)2Q-Q2HP-C60 confirms the pseudo-C2 symmetry of the porphyrindimer, which mimics the ‘special pair’ of natural PRCs [74]. The center to center distance between two porphy-rin rings of (MP)2 is 6.2 Å [74], which is close to the interchromophore separation of 7.0 Å observed withinthe special pair in the PRC [73,74]. (ZnP)2Q-Q2HP-C60 contains additional functionality through the bondingof the C60 electron acceptor, which allows the secondary charge-separation process to occur [74].(MP)2Q-Q2HP-C60 exhibited charge separations within the picosecond time range to afford the final charge-separated state within the microsecond time scale. The π-delocalization of the dimer porphyrin radical cationnot only facilitate the initial charge-separation process but also retard the charge-recombination processbecause of the small reorganization energy of electron transfer [91]. The observed long lifetimes of the charge-separated states are much longer than those of other special pair mimics [92–95]. Thus, the(MP)2Q-Q2HP-C60 molecules have provided the closest structure and function mimics to the natural PRC sofar synthesized [74].

Figure 1. Z-scheme in photosynthesis.

Two photosynthetic reaction centers (RCs) in Photosystem I (PSI) and Photosystem II (PSII).

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Biochemical Society Transactions (2018) 46 1279–1288https://doi.org/10.1042/BST20170298

Solar cell applications of PSI and PSIIBiophotovoltaic solar cells have attracted increasing attention because of advantages such as low cost produc-tion, environmentally friendly, and easy waste management compared with other photovoltaic devices [96–98].A biophotovoltaic cell was constructed by combining a PSI-based photocathode and a PSII-based photoanodewith use of an Os complex modified hydrogel (Figure 3), working with no sacrificial electron donors or accep-tors [99]. Under visible light irradiation, water is oxidized to O2 in the PSII photoanodic, whereas O2 isreduced in the PSI cathode via methyl viologen (MV2+), which is reduced by PSI to produce MV·+ that is oxi-dized by O2 to regenerate MV2+. The cell performance is described by the open-circuit voltage (VOC), which isthe difference of electrical potential between two terminals of a device when disconnected from any circuit, theshort-circuit current density (ISC) and the maximal cell power output (Pcell) that is the maximum value ofvoltage times current. The VOC, ISC and Pcell values were determined to be 90 ± 20 mV, 2.0 ± 0.7 mA cm−2 and23 ± 10 nW cm−2, respectively [99]. The fill factor (ff ) is defined as the ratio of maximum obtainable power tothe product of Voc and ISC and short-circuit current that is a measure of quality of the solar cell. The ff valuewas evaluated as 0.128 [99]. The power conversion efficiency (PCE), which is the ratio of power output topower input of solar energy, was determined to be 3.6 × 10−7 at the power input of 349 W m−2 [99]. At thisstate, however, the performance of the biophotovoltaic cell is limited by the relatively small potential differencebetween the two redox hydrogels [99]. PSI crystals by themselves were reported to generate very large photovol-tages compared with any semiconductor, ferroelectric and/or organic crystals [100].A solid biophotovoltaic cell was constructed by depositing the photoactive PSI layer on a poly(3,4-ethylene-

dioxythiophene):polystyrenesulfonate (PEDOT:PSS) film by spin coating (Figure 4) [101]. The PEDOT:PSStransparent conductive layer decreases the surface roughness, increases the adhesion, resulting in a lower elec-tric resistance of FTO glass to improve the electric performance of the device [101]. The VOC and ff valueswere determined to be 0.25 V and 31%, respectively [101]. The PCE value was determined to be 0.069% [101].The PCE value of a solid biophotovoltaic cell based on the PSI pigment–protein complex was improved to

0.51% by optimizing the PSI isolation method, compatible inter-layers, effective interface area, heat-free depos-ition techniques, and low vacuum situations [102]. The fabricated biophotovoltaic solar cell exhibited an

Figure 2. Structure of PRC from Rhodopseudomonas viridis with the distances between the components and lifetimes

of charge-separated states (left).

Structure of (MP)2Q-Q2HP-C60 and the inter-chromophoric distances and lifetimes of charge-separated states (right).

Abbreviations: P, ‘special pair’; BL, auxiliary bacteriochlorophyll; HL, bacteriopheophytin; QA, menaquinone; M in MP, Zn(II) or

2H; Ar, 3,5-di-tert-butylphenyl. Reprinted with permission from ref. [74]. Copyright 2016, Royal Society of Chemistry.

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Biochemical Society Transactions (2018) 46 1279–1288https://doi.org/10.1042/BST20170298

impressive increase in short-circuit current density up to the average value of 0.96 mA cm−2 [102]. Althoughthe PCE value is still low as compared with the best fabricated perovskite solar cell with certified power conver-sion efficiency of 22.1% [103], it may be improved by controlling the assembly of PSI layer by layer, designinga perfect device architecture, matchable energy-levels and engineering the PSI’s electron-transfer chain forbetter charge carrier mobility [102].

Figure 3. A biophotovoltaic cell composed of a PSII-based photoanode and a PSI-based photocathode (PSII = PS2 and

PSI = PS1).

Water splitting into electrons, protons and O2 occurs at the PSII-based photoanode upon photoirradiation. The electrons

produced in PSII are transferred to the PSI-based photocathode via the outer circuit to generate a reductive force of 580 mV

vs. SHE (standard hydrogen electrode), reducing MV2+ to MV·+ that reduces O2. Reprinted with permission from ref. [99].

Copyright 2013, WILEY-VCH Verlag GmbH.

Figure 4. A solid solar cell device composed of PSI.

The arrow indicates the direction of electron flow. Reprinted with permission from ref. [101]. Copyright 2017, American

Chemical Society. A painting of PS I by David Goodsell is released under a CC-BY-4.0 license.

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Biochemical Society Transactions (2018) 46 1279–1288https://doi.org/10.1042/BST20170298

Water splitting by biohybrid catalysts composed of PSIIBiohybrid catalysts composed of PSII have recently been developed for production of hydrogen by visible light-driven water splitting into H2 and O2 using the PSII-artificial Z-scheme hybrid system [69,104]. A hybridphotosystem is composed of plant photosystem II (PSII) and inorganic Ru/SrTiO3:Rh (Rh-doped) photocatalystusing electron relay with 2,6-dichloro-1,4-benzoquinone (DCBQ) and ferricyanide (Fe(CN)3-6 ) as shown inFigure 5 [104]. There are two pathways of electron transfer from PSII protein to Ru/SrTiO3:Rh photocatalyst inthe hybrid system: (1) direct transfer via DCBQ at the interfacial microdomain and (2) indirect transfer fromDCBQ to Fe(CN)3�6 in the bulk solution. The combination of DCBQ and Fe(CN)3-6 as electron transport relay inthe hybrid system enhanced the activity of overall water splitting up to 21.9 mmol H2 h

−1 and 10.1 μmol O2 h−1,

which increased by 3.3 times compared with the only Fe(CN)3-6 [69,104]. Correspondingly, the solar-to-hydrogen(STH) conversion efficiency, which is defined by the H2 energy generated divided by the entire solar irradiance,was increased from 0.012% to 0.043% under simulated sunlight (AM 1.5G; 100 mW cm−2) [104]. The electro-chemical measurements indicated that the redox potential of the Fe(CN)3�=4�6 couple is more positive than thatof the DCBQ couple [104]. Thus, electron transfer from the reduced DCBQ to Fe(CN)3-6 is thermodynamicallyfeasible and photogenerated electrons in PSII are transferred to DCBQ and then to Fe(CN)3-6 rapidly. In such acase, the use of the DCBQ–Fe(CN)3�6 electron relay system increased the efficiency of electron transport fromPSII to Ru/SrTiO3:Rh in the hybrid system, leading to the higher solar-to-H2 conversion efficiency [104].The much higher solar-to-H2 conversion efficiency has been attained by using a CdS–PSII hybrid photoelec-

trochemical cell, where PSII and CdS are connected via two redox shuttles, 2,6-dimethylbenzoquinone/2,6-dimethylhydroquinone (DMBQ/DMBQH2) (Cell A) and [Fe(CN)3-6 =Fe(CN)4-6 ] (Cell B), coupled withgraphite electrodes (Figure 6) [105]. A well-ordered electron transport from PSII to the CdS electrode wasmade possible by the redox shuttle reactions driven by the potential difference between the two redox pairs.The spatially separated multi-step electron transfer prohibited the back electron transfer during the water split-ting reactions [105].The CdS photoanode absorbed the UV and UVA (ultraviolet A; 315–400 nm) light, whereas PSII absorbed

visible light, leading to more efficient solar energy utilization and protection of PSII from photodamage by UVad UVA light illumination. The STH conversion efficiency was determined to be 0.34% under solar simulatorillumination (AM 1.5G; 100 mW cm−2) with no applied bias potential, when the overall water splitting activitywas obtained as 17.7 mmol H2 h

−1 and 8.5 mmol O2 h−1 [105]. The STH value is still lower than the best value

of 1.1% achieved by photocatalyst sheets that consist of La- and Rh-codoped SrTiO3 and Mo-doped BiVO4

powders anchored in an Au layer [106].A Z-scheme splitting of water into H2 and O2 has also been achieved by using a bio-free photocatalytic system

composed of K2[CdFe(CN)6]-modified metal sulfides as H2-evolving photocatalysts and an O2-evolution photo-catalyst (CoOx-loaded TaON photoanode) in the presence of Fe(CN)3�=4�6 as an electron mediator [107]. Thefurther combination with the biohybrid system in Figure 6 may increase the STH efficiency.

Figure 5. Visible light-driven water splitting into H2 and O2 by using electron transport relay combined

2,6-dichloro-1,4-benzoquinone (DCBQ) and ferricyanide in the PSII-Ru/SrTiO3:Rh hybrid system.

Reprinted with permission from ref. [104]. Copyright 2017, American Chemical Society.

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Biochemical Society Transactions (2018) 46 1279–1288https://doi.org/10.1042/BST20170298

ConclusionThe structure and function of PRCs have been well mimicked by electron donor–acceptor ensembles composedof a porphyrin dimer that mimics the ‘special pair (P)’ of natural PRCs and electron mediators, which canreproduce multi-step photoinduced charge separation to obtain long-lived charge-separated states. The charge-separation processes in PSI and PSII have been combined to construct a biohybrid solar cell to convert solarenergy to electric energy. Biohybrid catalysts composed of the PSII-artificial Z-scheme hybrid system havemade it possible to perform solar-driven water splitting into H2 and O2. The solar-to-hydrogen conversion effi-ciency has been improved by using a biohybrid CdS–PSII PEC cell, where PSII and the CdS-based PEC cell areconnected by two redox shuttles, Fe(CN)3-6 =Fe(CN)4-6 and DMBQ/DMBQH2. The bridging between naturaland artificial photosynthetic systems discussed in this minireview may provide new methods for sustainableenergy production. It is expected to combine PRC mimics with PSI or PSII for more efficient biohybrid solarcells and solar-driven water splitting.

AbbreviationsPRCs, photosynthetic reaction centers; PSI, photosystem I; PSII, photosystem II; STH, solar to hydrogen.

AcknowledgementsThe authors appreciate significant contributions of their collaborators and co-workers cited in the listedreferences and support by a SENTAN project (to S.F.) from Japan Science and Technology Agency, a grant forscientific research from Japan Society for the Promotion of Science (no. 16H02268 to S.F.), the NRF of Koreathrough CRI (NRF-2012R1A3A2048842 to W.N.), GRL (NRF-2010-00353 to W.N.) and also Basic ScienceResearch Program (2017R1D1A1B03029982 to Y.-M.L. and 2017R1D1A1B03032615 to S.F.).

Competing InterestsThe Authors declare that there are no competing interests associated with the manuscript.

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