REVIEW

Photobiological hydrogen production and artificial photosynthesisfor clean energy: from bio to nanotechnologies

K. Nath1,2 • M. M. Najafpour3,4 • R. A. Voloshin5 • S. E. Balaghi6 •

E. Tyystjarvi7 • R. Timilsina8 • J. J. Eaton-Rye9 • T. Tomo10,11, • H. G. Nam8•

H. Nishihara12 • S. Ramakrishna13 • J.-R. Shen14 • S. I. Allakhverdiev5,15,16

Received: 9 February 2015 / Accepted: 2 April 2015

� Springer Science+Business Media Dordrecht 2015

Abstract Global energy demand is increasing rapidly and

due to intensive consumption of different forms of fuels,

there are increasing concerns over the reduction in readily

available conventional energy resources. Because of the

deleterious atmospheric effects of fossil fuels and the

uncertainties of future energy supplies, there is a surge of

interest to find environmentally friendly alternative energy

sources. Hydrogen (H2) has attracted worldwide attention

as a secondary energy carrier, since it is the lightest carbon-

neutral fuel rich in energy per unit mass and easy to store.

Several methods and technologies have been developed for

H2 production, but none of them are able to replace the

traditional combustion fuel used in automobiles so far.

Extensively modified and renovated methods and tech-

nologies are required to introduce H2 as an alternative ef-

ficient, clean, and cost-effective future fuel. Among several

emerging renewable energy technologies, photobiological

H2 production by oxygenic photosynthetic microbes such

as green algae and cyanobacteria or by artificial photo-

synthesis has attracted significant interest. In this short

review, we summarize the recent progress and challenges

in H2-based energy production by means of biological and

artificial photosynthesis routes.

& S. I. Allakhverdiev

suleyman.allakhverdiev@gmail.com

1 Research Institute for Next Generation (RING), Kalanki,

Kathmandu-14, Kathmandu, Nepal

2 Department of Biological Sciences, Western Michigan

University, Kalamazoo, MI 49006, USA

3 Department of Chemistry, Institute for Advanced Studies in

Basic Sciences (IASBS), 45137-66731 Zanjan, Iran

4 Center of Climate Change and Global Warming, Institute for

Advanced Studies in Basic Sciences (IASBS),

45137-66731 Zanjan, Iran

5 Controlled Photobiosynthesis Laboratory, Institute of Plant

Physiology, Russian Academy of Sciences, Botanicheskaya

Street 35, Moscow 127276, Russia

6 Young Researchers and Elite Club, Shiraz Branch, Islamic

Azad University, Shiraz, Iran

7 Department of Biochemistry / Molecular Plant Biology,

University of Turku, 20014 Turku, Finland

8 Center for Plant Aging Research, Institute for Basic Science,

and Department of New Biology, DGIST, Daegu 711-873,

Republic of Korea

9 Department of Biochemistry, University of Otago,

P.O. Box 56, Dunedin 9054, New Zealand

10 Department of Biology, Faculty of Science, Tokyo University

of Science, Kagurazaka 1-3, Shinjuku-Ku, Tokyo 162-8601,

Japan

11 PRESTO, Japan Science and Technology Agency (JST),

Saitama 332-0012, Japan

12 Department of Chemistry, School of Science, The University

of Tokyo, 7-3-1 Hongo Bunkyo-ku, Tokyo 113-0033, Japan

13 Department of Mechanical Engineering, Center for

Nanofibers and Nanotechnology, National University of

Singapore, Singapore 117576, Singapore

14 Photosynthesis Research Center, Graduate School of Natural

Science and Technology, Faculty of Science, Okayama

University, Okayama 700-8530, Japan

15 Institute of Basic Biological Problems, Russian Academy of

Sciences, Pushchino, Moscow Region 142290, Russia

16 Department of Plant Physiology, Faculty of Biology, M.V.

Lomonosov Moscow State University, Leninskie Gory 1-12,

Moscow 119991, Russia

123

Photosynth Res

DOI 10.1007/s11120-015-0139-4

Keywords Artificial photosynthesis � Hydrogen as clean

energy � Cyanobacteria � Light-harvesting complexes �Nanotechnology � Photobiological hydrogen production

Abbreviations

Chl Chlorophyll

CO2 Carbon dioxide

CH4 Methane

FdOX Oxidized form of ferredoxin

FdRED Reduced form of ferredoxin

H2 Hydrogen

PS I and PS II Photosystem I and photosystem II

LHCs Light-harvesting complexes

NGS Natural gas reformation reaction

HTWS High-temperature thermochemical water

splitting

NHTE Nuclear high-temperature electrolysis

Nm3 Normal cubic meter

TEM Transmission electron microscopy

HRTEM High-resolution transmission electron

microscopy

WOC Water-oxidizing complex

Introduction

The global energy demand is increasing rapidly owing to

increase in the world’s population as well as increase in the

energy consumption in the modernized life style. More

non-renewable fossil fuels are being consumed which may

ultimately lead to the extinction of fossil fuel reserves.

Also, reliance on non-renewable fossil fuels may cause

catastrophic effects in the environment such as global

warming through the greenhouse effect, drought, and pol-

lution. Biofuels have been proposed as an alternative en-

ergy source which would reduce the environmental

pollution significantly (Lynd et al. 2009). However, in-

crease in the biofuel utilization has led to increase in car-

bon emissions, competition with food supplies for humans

and livestock, and loss of habitats of wildlife, since the

recent trend has been to convert grassland, grazing fields,

and forests into new crop land to replace the grain diverted

to biofuel (Searchinger et al. 2008; Rathmann et al. 2010,

2012). Thus, global energy security is of serious concern

and there is an urgent need to find cheap, readily available,

renewable, and environmentally friendly alternative energy

sources. In this regard, production of hydrogen by photo-

biological approaches and artificial photosynthesis may

provide promising solutions.

H2 is an important industrial compound and its current

annual world production is more than 5 9 1011 normal

cubic meters (Nm3). H2 has gained importance in recent

years firstly due to the increased demand in conventional

applications—both in petroleum refining processes such as

hydrotreating and hydrocracking among other uses in the

petrochemical industry (Ewan and Allen 2005) and, sec-

ondly, because global energy demand, which is largely met

by fossil fuels, is projected to increase by 50 % or more by

the year 2030 (Maness et al. 2009). Because of dwindling

resources, growing environmental concerns and stringent

emission norms and uncertainties surrounding future sup-

plies, there is an urgent need to develop cost-effective,

environmentally friendly, and efficient energy sources. H2,

the simplest and most abundant element, meets the re-

quirements to be an energy source. It has higher energy

content per unit mass than alternative fuels; it can be

readily produced as a gas from various resources (Esper

et al. 2006; Kotay and Das 2008; Allakhverdiev et al.

2010a, b; Allakhverdiev 2012; Najafpour and Al-

lakhverdiev 2012; Azwar et al. 2014; Najafpour et al.

2014b) and, when combusted, generates only water. H2 can

be used as a good transportation fuel, because H2 gas-based

fuel cells can be more efficient in power generation than

Fig. 1 Biological H2 production in cyanobacteria and green algae.

Cyanobacteria and green algae may produce H2 with bidirectional

hydrogenase enzymes. The cyanobacterial [NiFe]-hydrogenase a con-

sists of five subunits (HoxE, HoxF, HoxH, HoxU, and HoxY) and

probably functions as a dimer or pentamer, whereas the algal [FeFe]-

hydrogenase b consists of one protein (HydA). The reaction catalyzed

by the bidirectional enzymes is near to equilibrium in cellular

conditions, and the enzymes catalyze both evolution and break-up of

H2. The algal enzyme uses reduced ferredoxin as an electron donor but

there is no consensus about the electron donor of the cyanobacterial

enzyme. Nitrogen-fixing cyanobacteria produce H2 with nitrogenase

c. Three subunits of nitrogenase (2a-subunits, 2a; 2b-subunits, 2b; andfour dinitrogenase reductase, NR) are shown. H2 produced by

nitrogenase is broken up by the uptake hydrogenase consisting of the

HupL and HupS subunits. After the uptake hydrogenase, the electrons

end up in the plastoquinone pool, and the associated pumping of protons

to the thylakoid lumen may power ATP production. Figures partly

drawn after Allakhverdiev et al. (2009). Reprinted with permission from

Allakhverdiev et al. (2009). Copyright (2009) by RSC Group

Photosynth Res

123

traditional combustion fuels. Thus, H2 has the potential to be

a promising clean fuel both in the transportation sector as

well as in power plants (Abraham 2002; Ewan and Allen

2005; Kotay and Das 2008). H2 can be produced from

methane by a reaction called natural gas services reaction

(NGS), where H2 atoms of both CH4 and H2O are converted

to H2 gas due to oxidation of methane. NGS has been one of

the most important industrial processes worldwide for the

past 6–7 decades (Rostrup-Nielsen 1984), and nearly all

industrial H2 gas comes from this reaction. So far NGS

depends on fossil fuels; therefore it cannot sustain the de-

mand of H2 as a fuel (Pena et al. 1996).

Several processes exist with chemistry resembling that of

natural gas reformation, including gasification and renew-

able liquid reforming, and fossil fuels or biomass can be

used as their substrates. H2 can also be produced by splitting

water molecules by high-temperature thermochemical water

splitting (HTWS) and electrolytic water splitting with nu-

clear high-temperature electrolysis (NHTE). Finally, H2 can

be produced by photo-driven water splitting, where the en-

ergy is provided by light from the sun (Allakhverdiev et al.

2009, 2010a; Maurino and Weber 2013).

Solar energy is the most abundant and easily accessible

renewable energy source available for future sustainable

production of fuel (Allakhverdiev et al. 2009). Thus, ef-

fective use of solar energy to develop more cost-effective

systems with improved ability to convert sunlight into

chemical energy conserved in fuel, such as H2, is of utmost

importance. The fact that H2 only yields water when burnt

implies that H2 has the potential to reduce emission of

environmental pollutants such as CO2 and unburned hy-

drocarbons. Researchers are developing a wide range of

technologies to produce H2 economically from a variety of

resources in environmentally friendly ways (Allakhverdiev

et al. 2010b; Allakhverdiev 2012; Najafpour and Al-

lakhverdiev 2012; Maurino and Weber 2013). Among

them, a high rate of photobiological H2 production by

oxygenic photosynthetic microbes has attracted significant

interests (Bandyopadhyay et al. 2010).

Among the emerging renewable and green energy

sources, H2 stands out as an appealing and promising

choice for the next generation energy source. Although,

different types of H2 fuel cells have been developed for H2

production, several major technical challenges remain be-

fore the traditional combustion engine currently used in

automobiles can be replaced by fuel cells. Consequently,

for satisfactory performance, most of these methods require

expensive modifications to introduce H2 as an alternative

environmentally friendly and efficient candidate for future

fuel. Here, we discuss photobiological and artificial pho-

tosynthetic approaches of H2 production and its role in the

energy sector. To minimize the negative environmental

Fig. 2 Tentative model of the photosynthetic electron transport

pathway in thylakoid membranes that support the idea of the

production of H2. Initially, electrons produced due to photolysis of

water are taken by PSII and transferred in the Z-scheme. Initially,

light-activated PSII reaction center extracts electrons from water and

transfers them sequentially to plastoquinone (PQ), cytochrome

b6f (Cyt b6f), plastocyanin (PC), and finally feeds electrons to light-

oxidized PSI. In the linear electron transport scheme in green algae

and cyanobacteria, light-activated PSI-derived electrons are used in

the reduction of ferredoxin (FdRED), which in turn supplies electrons

either to produce NADPH (solid red arrow) and/or to produce

biological H2 in the presence of FeFe-Hydrogenase (dotted red

arrow). Reprinted with permission from Allakhverdiev et al. (2010a,

b). Copyright (2010) by Elsevier. Part of the figure was adapted from

Maness et al. (2009). Copyright (2009) by American Society

Microbiology

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123

impacts of fossil fuels, there is increasing interest in H2-

based energy systems. However, a central question is

whether large-scale H2-based energy utilization, corre-

sponding to a quarter of global mobility needs, is possible?

Hydrogen production by microorganisms

Photosynthesis, directly or indirectly, is pivotal for biolo-

gical H2 production. It has already been more than 70 years

since the discovery of H2 metabolism in green algae (Gaf-

fron 1939). So far cyanobacteria and green algae are the only

known organisms with both oxygenic photosynthesis and H2

production (Schutz et al. 2004). They appear to be an at-

tractive alternative for the future as they have less adverse

effects on the environment than current fossil fuel-based

energy systems (Melis and Happe 2001; Allakhverdiev et al.

2009; Hemschemeier et al. 2009; Allakhverdiev et al.

2010b). Several groups of microorganisms including both

eukaryotes like the green alga Chlamydomonas reinhardtii

and prokaryotes like the cyanobacteria Cyanothece and

Anabaena, and anoxygenic photosynthetic bacteria like

Rhodopseudomonas palustris, produce H2 with the help of

either hydrogenase or nitrogenase (Bandyopadhyay et al.

2010). Cyanobacteria produce H2 with hydrogenases and

nitrogenase, and green algae use only hydrogenase (Fig. 1).

In oxygenic photosynthetic organisms, sunlight is ab-

sorbed by light-harvesting complexes (LHCs) associated

with Photosystem II (PS II) and Photosystem I (PS I) (Nath

et al. 2013a, b). Thus, oxygenic H2 producing organisms

use PS I-derived electrons to produce the reduced form of

ferredoxin (FdRED), which in turn supplies electrons either

to produce H2 or NADPH (Fig. 2). Hydrogenase uses the

reductant directly to reduce protons to H2. Nitrogenase-

Scheme 2 Comparison of the reactions involved in oxygen evolution

from water in the presence of a [Ru(II)(bpy)3]2? and b chlorophyll

and light irradiation (Najafpour 2011). Reprinted with permission

from Najafpour (2011). Copyright (2011) by Taylor & Francis Group

Scheme 1 Schematic

representation of H2 production

by artificial photosynthesis.

Reprinted with permission from

Gust et al. (2009). Copyright

(2009) by American Chemical

Society

Photosynth Res

123

containing cells, in turn, obtain the reductant by oxidizing

organic carbon compounds originally produced by photo-

synthesis (Bandyopadhyay et al. 2010). In addition to

cyanobacteria and green algae, anoxygenic phototrophic

bacteria can use light energy to produce H2 from organic

compounds (Rey et al. 2007). Thus, when H2 is produced

by anoxygenic photosynthetic organisms, protons are pro-

vided by an organic substance and part of the free energy

required for the reaction is derived from sunlight (Bandy-

opadhyay et al. 2010).

Natural photosynthesis as a guide to designartificial photosynthesis for clean energyproduction

Plants provide food, fiber, shelter, oxygen, and fuel to hu-

mans through oxygenic photosynthesis. In this regard, pho-

tosynthesis is directly related to the existence of life in this

planet. Natural photosynthesis involves a series of oxidation–

reduction reactions in which solar radiation is captured and

converted to chemical energy by chlorophyll (Chl)-bearing

organisms ranging from cyanobacteria to higher plants

(Arnon 1959; Bjorkman and Demmig-Adams 1995; Eber-

hard et al. 2008). When a photon strikes a Chl molecule, it

becomes excited by absorbing energy (Muller et al. 2001). In

leaves, photosynthetic light absorption is carried out by Chl-

binding LHCs that are associated with PSI and PSII (Muller

et al. 2001; Bjorn et al. 2009). Energy of light absorbed by

Chl molecules is further transferred from one pigment

molecule to other molecules and eventually to a reaction

center where charge separation takes place (Huner et al.

1998). Some of the light energy absorbed by Chl molecules

can be re-emitted as fluorescence (Flexas et al. 2000; Max-

well 2000; Flexas et al. 2002; Freedman et al. 2002; Zarco-

Tejada et al. 2003; Soukupova et al. 2008; Rascher et al.

2010; Porcar-Castell 2011; Garbulsky et al. 2013). The net

process of photosynthesis is the temporary capture of light

energy in the chemical bonds of ATP and NADPH during the

light reactions and the permanent conversion of captured

energy in long-term energy storage molecules such as glu-

cose during the dark reactions (Allen 1975; Whitmarsh 1999;

Baker 2008; Eberhard et al. 2008; Araujo et al. 2014).

Therefore, photosynthesis is the ultimate source of cellular

energy and for all living activities in this planet.

It has been reported that the use of US crop plants for

biofuels also increases greenhouse gases through emission

from land-use change (Searchinger et al. 2008), it is time to

think about an alternative way to develop some clean en-

ergy to fulfill the current need of energy for the world. In

biological photosynthesis, photolysis of water in thylakoid

membranes is powered by solar radiation, and conversion

of sun light to chemical energy is finalized by the reduction

of CO2 to the carbohydrate level. Photosynthetic water

splitting, coupled to hydrogenase-catalyzed H2 production,

is considered as a promising clean, renewable source of

energy (Allakhverdiev et al. 2009).

Hydrogen production by artificial photosynthesis

Inspired by photosynthesis of plants, Giacomo Ciamician

was the first who suggested the replacement of fossil solar

energy with sunlight (Ciamician 1912). Recently, scientists

from various fields are very interested in Ciamician’s vi-

sion and thus, the creation of artificial systems based on the

principles from natural photosynthesis such as ‘‘artificial

leaf’’ (Nocera 2012) is a promising way for fulfilling global

energy in future. Natural photosynthesis can be divided

into two half reactions, (i) photo-oxidation of water

molecules during light reaction to release proton and

oxygen, and (ii) reduction of carbon dioxide during dark

reaction to convert carbon dioxide into glucose. Recently,

several artificial photosynthetic systems have been used to

develop photocatalysts to perform reaction (i) and reaction

Fig. 3 The structure of the water-oxidizing complex (WOC) in PS II.

a Mn–Ca, Mn–O, Ca–O, Mn–water, and Ca–water distances in the

WOC are in A. b Image is from Suga et al. (2015). Reprinted with

permission from Suga et al. (2015). Copyright (2015) by Nature

Publishing Group

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(ii) separately. However, both half reactions are essential to

produce fuel, but in the current review we only focus on the

mimicking of the light-dependent half reaction (reaction, i)

of natural photosynthesis to design efficient artificial pho-

tosynthesis for H2 production (Scheme 1). The utilization

of better catalysts with suitable photosensitizers can drive

the reduction of protons by light, and it is believed that

such light-driven H2 production schemes can be utilized in

the production of carbon-free solar fuels (Scheme 1). In

this proposal, the protons produced by the splitting of water

molecules can be taken for H2 production. In this regard,

natural photosynthesis acts as the base for the artificial

photosynthesis to design solar energy conversion systems.

Several materials can be used to produce energy efficiently

in artificial photosynthesis, applying the fundamental sci-

entific principles of the natural process (Gust et al. 2009).

In an artificial photosynthetic system, we need com-

pounds for:

1. Absorption of a photon from sunlight efficiently.

2. Formation of a charge-separated state.

3. Transfer of the electron to a reducing catalyst.

4. Catalysts to accept and accumulate electrons. The

catalysts should reduce a compound such as N2, CO2,

or H2O to other helpful compounds such as NH3,

(CHO)n, or H2.

5. Transfer of an electron from the oxidizing catalyst.

6. Substrate to be oxidized by the oxidizing catalyst.

After charge accumulation by the oxidizing catalyst, a

substrate will be oxidized from which, cheap electrons

should be obtained to reduce other compounds. Thus,

we need a cheap compound such as water to be

oxidized.

Thus, in an artificial photosynthetic system usually one-

electron transfer events can be coupled to a charge accu-

mulation and then to a catalytic reaction. These catalysts

may be used in photochemical, electrochemical, or pho-

toelectrochemical devices to split water molecules. A very

usual design in artificial photosynthetic systems is an at-

tached photosensitizer molecule to a semiconductor. In this

condition, a charge separation occurs upon illumination by

the transfer of electron from the photoexcited chromophore

to the conduction band of the semiconductor. A sufficiently

Fig. 4 Transmission electron microscopy (TEM) images (top row)

a mixed-valent porous amorphous Mn oxides, b cryptomelane-type

tunnel Mn oxides, c layered Mn oxides. High-resolution TEM

(HRTEM) images (bottom row) d mixed-valent porous amorphous

Mn oxides, e cryptomelane-type tunnel Mn oxides, f layered Mn

oxides. Reprinted with permission from (Iyer et al. 2012), copyright

(2012) by American Chemical Society. TEM g and HRTEM h images

of MnCaOx-poly-L-glutamic acid. The red arrows show some Mn–Ca

oxide nanoparticles in PGA matrix. Yellow lines in h show layers

(Najafpour et al. 2014a). The distance between two layers is

0.8–0.9 nm related to birnessite structure. Layered Mn oxide i (Na-jafpour et al. 2013). g and h are reprinted with permission from

Najafpour et al. (2014a). Copyright (2014) by RSC publications

Photosynth Res

123

long-lived charge-separated state to allow the chromophore

to abstract an electron from the catalyst is necessary in this

condition. After a few charge separations and electron

abstractions, the catalyst refills the holes by abstracting

electrons from substrate. The cheap electrons from sub-

strate are used for reduction of other molecules by reducing

the catalyst.

Many metal complexes or organic compounds, which

can transfer electron from their excited states to a sacrifi-

cial electron acceptor, were reported (Adamson and Demas

1971; Gafney and Adamson 1972). Among different

compounds, tris(bipyridine)ruthenium(II) ion [Ru(bpy)3]2?

is very interesting in this regard. The complex can play a

role similar to a reaction center Chl in photosynthesis

(Scheme 2) Maitra et al. (2014).

In this and other similar metal complexes, an absorption

in the visible region (k * 450 nm) is observed. The illu-

mination excites one electron from a t2g orbital to a ligand-

centered orbital. The excited molecule is converted to a

long-lived triplet state, 3[Ru(bpy)3]2?*, that has the po-

tential to be engaged in single electron transfer. This ex-

cited state has a long enough life time for reaction by an

electron acceptor. Interestingly, the 3[Ru(bpy)3]2?* is more

reactive toward both oxidizing and more reducing reactions

than [Ru(bpy)3]2?. Thus, the excited complex can be used

as an oxidant or reductant as shown in Scheme 2.

Nature uses two super catalysts for proton reduction and

water oxidation. Hydrogenase enzymes with iron and/or

nickel cofactors are a family of metallo-sulfur enzymes that

perform the oxidation of molecular H2 and the reduction of

protons to H2 near the thermodynamic potential with high

turnover frequencies of 100–10,000 mol of produced H2

per mole of catalyst per second (Concepcion et al. 2008).

Nature also uses a super catalyst for water oxidation.

The research groups of J. Barber and S. Iwata in 2004

found three Mn and one Ca ion form an elongated

CaMn3(l-O)4 cubane structure together with four bridging

oxygen atoms in the structure of the water-oxidizing

complex in PS II (Ferreira et al. 2004). The fourth Mn ion

was connected to the cube by binding to one of the bridging

oxygen atoms, and was thereby positioned as a ‘dangler’.

Shen and Kamiya in 2011 (Umena et al. 2011) uncovered

the detailed structure of this catalyst, revealing that five

metal ions were connected by five oxo-bridged oxygen

atoms. They also found that two water molecules are co-

ordinated to Ca and two others are coordinated to the

dangling Mn (Mn(4)). The structure suggests that the Mn–

Ca cluster could be described as a chemical formula of

Mn4CaO5 (H2O)4 (Fig. 3). Recently, the group further re-

ported a radiation damage-free structure of the catalyst

(Suga et al. 2015).

Because of the efficiency of these enzymes, natural

photosynthesis is a model for artificial photosynthetic

systems to produce H2 as an alternative clean energy fuel.

In addition to H2 production, oxidation of water to O2 is

also very important because it provides cheap electrons for

the reduction reactions. Among different strategies,

Fig. 4 continued

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nanotechnology has an important role to design and syn-

thesize efficient catalysts (Limburg et al. 1999; Chou et al.

2012). In a new view, Fe or Mn clusters may be considered

as nano-sized particles in a protein matrix. An enzyme can

be considered as an efficient nano-sized machine. Many

catalysts such as metal oxides (Fig. 4a–f) or composites

with organic compounds (Fig. 4g, h) with different mor-

phologies Fig. 4i) with high activities compared to bulk

catalysts were reported using different strategies by

nanotechnology.

Gold nanoclusters modified with a self-assembled

monolayer of porphyrin disulfide dimer was also reported

by Imahori et al. (2003) to capture sunlight (Fig. 5).

In artificial photosynthesis, biological compounds and

templates can also be used. Among different strategies,

Nam et al. (2010) with Belcher reported a biologically

templated nanostructure for visible light-driven water

oxidation using a genetically engineered M13 virus scaf-

fold for co-assembly of zinc porphyrins and iridium oxide

hydrosol clusters (catalyst) (Fig. 6).

Recently, several biomimetic approaches to artificial

photosynthesis have been proposed for the photo catalytic

oxidation of water molecules to generate H2 and O2 (Al-

lakhverdiev et al. 2010a; Najafpour et al. 2014b). As we

mentioned above, natural photosynthesis acts as the base

for the artificial photosynthesis to design solar energy

conversion systems. Several materials can be used to pro-

duce energy efficiently in artificial photosynthesis, apply-

ing the fundamental scientific principles of the natural

process (Gust et al. 2009).

Future perspectives and challenges

Despite impressive increases in the energy efficiency of

modern appliances, the demand for energy has increased

globally. Thus, the search for abundant and cheaper energy

to satisfy the growing energy demand of the population is

very important. Due to the uncertainty and ambivalence

about bioenergy among policy makers and the general

public, development of sustainable bioenergy has not been

given the attention it deserves. Hence, feasibility and de-

sirability of large-scale bioenergy production, and ways to

overcome its limitations, should be seriously considered in

Fig. 5 Schematic view of gold

nanoclusters modified with a

self-assembled monolayer of

porphyrin disulfide dimer

(Imahori et al. 2003). Reprinted

with permission from Imahori

et al. (2003). Copyright (2003)

by Elsevier

Photosynth Res

123

order to meet the major fraction of global energy demand

with bioenergy. Although great leaps have been achieved

during the past few years in our understanding of photo-

systems, the knowledge is not yet good enough in order to

materialize our dream to rely upon bioenergy as a major

source of our future energy. In this regard, better under-

standing of natural photosystems and their mimicking to

design an effective artificial photosystem to produce clean

bioenergy like H2 is essential. Despite such challenges, we

imagine a future where a substantial fraction of our energy

production is based on conversion of sunlight to chemical

energy. Since natural photosynthesis needs plenty of space

to provide food for the growing population, aquaculture of

plants, algae and cyanobacteria are apparent choices, as

these organisms can produce biofuels without competing

with food production for land. Future study is required to

find out which strains or species give the highest H2-based

energy in a particular condition. Although, the ability of the

production of H2 gas as clean energy from a unicellular

green algal species, Chlamydomonas reinhardtii, through

iron hydrogenase is well known, the oxygen-sensitive hy-

drogenase is closely linked to the photosynthetic chain in

such a way that H2 and oxygen production need to be

separated temporally for sustained photo-production. As a

recent finding by Williams and Bees (2014) has shown,

production of H2 as clean energy should be produced under

a range of sulfur-deprivation schemes, and such schemes

may provide a new insight to achieve significant biological

H2 production at a commercial scale. Study for artificial

photosynthesis can be focused on the construction of

comfortable conjugations of catalyst and photosensitizer to

produce light-driven carbon-free H2 fuel. The design of

catalysts for different reactions should not be limited to

mimicking of the natural photosystems but novel chemicals

and methods can also be tested. However, important prin-

ciples can be learnt from the natural systems since they

have been developed and utilized effectively for millions of

years.

Acknowledgments MMN is grateful to the Institute for Advanced

Studies in Basic Sciences, and the National Elite Foundation for fi-

nancial support. SEB is grateful to Young Researchers and Elite Club

for financial support. ET was supported by Academy of Finland and

Nordic Energy Research (Aquafeed project). HGN was supported by

Institute for Basic Sciences (IBS-R013-D1-2015-a00), Korea. This

work was also supported by a grant-in-aid for Specially Promoted

Research No. 24000018 from JSPS, MEXT (Japan) to JRS, and by a

grant from the Russian Science Foundation (No: 14-14-00039) to

SIA.

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