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CRITICAL REVIEW www.rsc.org/csr | Chemical Society Reviews

Photosynthetic energy conversion: natural and artificialw

James Barber*
Received 15th September 2008
First published as an Advance Article on the web 10th November 2008
DOI: 10.1039/b802262n

Photosystem II (PSII) is the water splitting enzyme of photosynthesis. Its appearance during
evolution dramatically changed the chemical composition of our planet and set in motion an
unprecedented explosion in biological activity. Powered by sunlight, PSII supplies biology with
the ‘hydrogen’ needed to convert carbon dioxide into organic molecules. The questions now are
can we continue to exploit this photosynthetic process through increased use of biomass as an
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energy source and, more importantly, can we address the energy/CO2 problem by developing new
photochemical technologies which mimic the natural system? (Critical review, 82 references)

Introduction The success of photosynthesis as an energy generating and

Photosynthetic organisms capture sunlight very efficiently and
convert it into organic molecules. These molecules are the
building blocks of all living organisms and without photo-
synthesis life on our planet would not have evolved in the way
that we know. It is estimated that currently, photosynthesis
produces more than 100 billion tons of dry biomass annually,
which would be equivalent to a hundred times the weight of
the total human population on Earth at the present time and
equal to an average energy storage rate of about 100 TW. Oil,
gas and coal are also derived from millions of years of
photosynthetic activity. These fossil fuels provide us with most
of the energy needed to power our technologies, heat our
homes and produce the wide range of chemicals and materials
that support everyday life. Ultimately the reserves of fossil
fuels will dwindle and then what? Even before this, as a
consequence of our ever growing use of oil, gas and coal, we
are faced with the problem of increasing levels of carbon
dioxide and other greenhouse gases in the atmosphere with
implications for global climate change.
storage system stems from the fact that the raw materials and
power needed for the synthesis of biomass are available in
almost unlimited amounts; sunlight, water and carbon dioxide.
At the heart of the photosynthetic process, is the splitting of
water by sunlight into oxygen and ‘hydrogen’. The oxygen is
released into the atmosphere where it is available for us to
breathe and to use for burning fuels to drive our technologies.
The ‘hydrogen’ is not normally released into the atmosphere
but instead is combined with carbon dioxide to make sugars
and other organic molecules of various types. When we burn
fuels (fossil, biomass and other biofuels) to release energy, we
are simply combining the ‘hydrogen’ stored in these organic
molecules with atmospheric oxygen, so completing a cycle
started millions of years ago. Similarly, energy is also released
from the organic molecules which constitute our food, when
they are metabolised within our bodies by the process of

Division of Molecular Biosciences, Faculty of Natural Sciences,

Imperial College London, London, UK SW7 2AZ
w Part of the renewable energy theme issue.

James Barber is the Ernst

Chain Professor of Biochem-
istry at Imperial College London
and is a Fellow of The
Royal Society of London and
Royal Society of Chemistry.
He obtained his BSc in chem-
istry from the University of
Wales in 1964 and MSc and
PhD in biophysics from the
University of East Anglia in
1965 and 1967, respectively.
He has been awarded several
medals and prizes for his con-
James Barber tributions to understanding the
molecular processes of photo-
synthesis with particular focus on Photosystem II, the water
splitting enzyme which underpins the energy cycle of biology.
Fig. 1 A diagrammatic representation of energy flow in biology. The
light reactions of photosynthesis (light absorption, charge separation,
water splitting, electron/proton transfer) provides the reducing equiva-
lents in the form of energised electrons (e) and protons (H+) to
convert carbon dioxide (CO2) to sugars and other organic molecules
which make up living organisms (biomass) including those that
provide humankind with food. The same photosynthetic reactions
gave rise to fossil fuels formed millions of years ago. The burning of
these organic molecules either by respiration (controlled oxidation
within our bodies) or by combustion of biomass and fossil fuels to
power our technologies, is the reverse to photosynthesis, releasing CO2
and reuniting the stored ‘hydrogen’ with oxygen to form water. In so
doing energy is released, energy that originated from sunlight.

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respiration. Thus in the biological world, photosynthesis
brings about the splitting of water into oxygen and ‘hydrogen’
while respiration is the reverse, combining oxygen and hydro-
gen in a carefully controlled and highly efficient way so as to
create metabolic energy. Therefore, from an energetic view,
the synthesis of organic molecules represents a way of storing
hydrogen and therefore storing solar energy in the form of
chemical bonds (Fig. 1).
In this article I will briefly emphasise the enormity of the
energy/carbon dioxide problem that we face within the coming
decades and discuss the contributions that could be made by
fuels derived directly from photosynthesis (biofuels) and from
developing new technologies based on the successful principles
of photosynthesis. I will particularly emphasise the possibility
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of exploiting the vast amounts of solar energy available to split
water to produce dioxygen and the reducing equivalents
required to generate fuels such as hydrogen gas, alcohols
and methane.
Global energy consumption and the enormity
of the problem
At the present time, the rate of global energy consumption is
approaching about 14 TW,1 with the USA and the extended
EU each using about 25% of this. In the future this global
value will rise due to industrialization in underdeveloped and
developing countries coupled with increasing world popula-
tion. Based on current projections the global annual energy
consumption rate will reach 20 TW by 2030, doubled by 2050
and tripled by the end of the century.2–4 About 85% of the
total global energy consumed at present comes from burning
fossil fuels with the proportion approaching 90% for devel-
oped countries. Oil, gas and coal contribute approximately
equally to this demand. The remaining sources of energy are
hydroelectric, nuclear, biomass and renewables, such as solar,
wind, tide and wave. At present, the use of biomass is a major
player and is mainly localised in under-developed regions,
such as Africa and India, where wood and other organic
matter is used as fuel. Much of this is not strictly renewable
since there is no planned regeneration and the trend is towards
more use of fossil fuels.
The low level of contribution of non-fossil energy sources to
present day global energy demand reflects the readily available
resources of oil, gas and coal. Even when oil reserves become
limiting, there will remain large reservoirs of gas and, parti-
cularly, coal to exploit.5 Therefore in the global arena, the
problem for the immediate future is not a limitation of fossil
fuel reserves but the consequences of its combustion. If the
total fossil fuel reserve is burnt then the carbon dioxide level in
the atmosphere and oceans would rise to values equivalent to
those that existed on our planet long before humankind
evolved.6 Despite this concern, it is certain that fossil fuels
will continue to be a major source of energy for humankind for
some years to come but it is vital that they should be used in
such a way as to minimise carbon dioxide release into the
atmosphere. Technologies for sequestration of carbon dioxide
must be developed.7 Hand in hand with this there will almost
certainly be an improvement in the efficiency of energy use and
supplementation whenever possible with non-fossil fuel
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sources. Against this background it seems to me that we must
also strive to develop new technologies based on principles
which have yet to be revealed from basic studies and in
particular those that focus on utilizing the enormous amount
of energy available to us as solar radiation.8 The sun provides
solar energy to our planet on an annual basis at a rate of
100 000 TW. Therefore the energy from one hour of sunlight is
equivalent to all the energy humankind currently uses in a
year. We do have existing technologies to capture sunlight and
produce electricity and the efficiency and robustness of these
photovoltaic systems is improving daily.9,10 Compared with
the present day price of fossil fuels photovoltaic systems
represent an expensive way to generate electricity because of
the high cost of their construction. In time these costs will
decrease relative to the cost of fossil fuel. Moreover a blending
of the principles of photovoltaic systems, especially those
using cheap organic or inorganic materials, with concepts
derived from natural photosynthetic systems may ultimately
provide a long term solution.4,8 In considering this long term
solution, let us take a look at the efficiency of the natural
photosynthetic process.
Efficiency of photosynthesis
As emphasised in Fig. 1, photosynthesis is a process which
converts light energy into the organic molecules of biomass.
To estimate the efficiency of this process two main factors
must be appreciated.
(i) Although photosynthetic organisms can efficiently trap
light energy at all wavelengths of visible solar radiation, the
energy used for splitting water and reducing carbon dioxide is
only equivalent to the red region of the spectrum. Higher
energy photons are degraded to heat by internal conversion
within the light harvesting pigments to the energy level of ‘red’
photons of about 1.8 eV.
(ii) For every electron/proton extracted from water and used
to reduce CO2 the energy of two ‘red’ photons is required. This
is accomplished by linking together, in series, two different
photosystems, photosystem II (PSII), which uses light to
power the extraction of electrons/protons from water, and
photosystem I (PSI) which uses light to provide additional
energy to the ‘‘PSII-energised’’ electrons/protons so as to drive
the CO2 fixation process (see Fig. 2). Therefore photosynthesis
uses the energy of at least 8 ‘red’ photons per O2 molecule
released or CO2 molecules fixed. A typical product of carbon
fixation is glucose (C6H12O6) whose energy content is
672 kcal mol1 (2813 kJ mol1) if burnt in a calorimeter. To
make a glucose molecule, the energy of 48 ‘red’ photons is
required and assuming a wavelength of 680 nm, corresponding
to 42 kcal per quantum mole (176 kJ mol1), gives the
efficiency of conversion at about 30%. Although this is an
impressive number, in reality the overall conversion of solar
energy to glucose and the very large variety of other organic
molecules which constitute biomass is much lower. Energy is
lost in degrading shorter wavelength light (e.g. blue light)) to
the energy of ‘red’ photons, by saturation processes and more
significantly, in driving the enormous number of reactions
which occur in photosynthetic organisms to maintain their
organisation, metabolism, reproduction and survival.
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Fig. 2 A simplified Z-scheme of the light reactions of photosynthesis taken from http://en.wikipedia.org/wiki/Photosynthesis. For every electron
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extracted from water and transferred to CO2, the energy of two photons of light is required. One is absorbed by Photosystem II (PSII) which
generates a strong oxidising species (P680+), able to drive the water splitting reaction and a reduction of pheophytin (Pheo) and then plastoquinol
(Q) to plastoquinol (QH2). The other, Photosystem I (PSI), generates a strong reducing species, NADPH which donates reducing equivalents to
CO2 to produce sugars and other organic molecules, and a weak oxidant P700+. Electron and proton flow from QH2 to P700+ is aided by the
cytochrome b6f (Cyt b6f) complex and plastocyanin (PC) and results in the release of energy to convert ADP to ATP. The ATP produced is
required, along with NADPH, to convert CO2 to sugars. Since the production of O2 requires the splitting of two water molecules, the overall
process involves the removal of two electrons per water (as shown) and therefore four photons per PSII and PSI reaction centre. The reduction of
oxidised nicotinamide adenine dinucleotide phosphate (NADP+) by PS1 is facilitated by membrane bound iron sulfur proteins (Fx, FA and FB)
and soluble ferredoxin (FD).

There are many ways to define and calculate the overall
photosynthetic efficiency but the approach adopted by
Thorndike11 is attractive since it engulfs the whole range of
definitions. He considered free energy stored per photon F:
F = ZTZRZSZLZOhnO
where hnO is the energy of a photon at the optimum frequency
for conversion (i.e. red photon), ZO is the thermodynamic
efficiency (conversion from light energy to chemical free
energy produces an explicit entropy loss), ZL is a factor
accounting for irreversibility energy losses in photochemical
reactions, biochemical pathways and other cellular and physio-
logical processes, ZS a factor accounting for the spectral
distribution of light and the fact that there is a minimum
usable photon energy (close to hnO), ZR is a correction factor
for leaf reflectivity (a scattering factor for algal suspensions)
and ZT a correction for saturation effects. Taking hnO as 680 nm
and adopting reasonable values for the various coefficients
(ZO = 0.73, ZL = 0.50, ZS = 0.32, ZR = 0.80, ZT = 0.5),
Thorndike calculated a maximum efficiency for the conversion
of light to stored chemical energy (dry carbon matter) of about
4.5%. A similar value was calculated by Walker,12Archer and
Barber13 and by others (see refs. 14 and 15).
In fact, an efficiency of 4.5% is rarely achieved. Only in
exceptional cases will dry matter yield exceed 1 or 2%, such as
with the intense growing of sugar cane in tropical climates or
with optimised culturing of algae. Normally agricultural crops
produce yields of biomass at efficiencies less than 1%, even
when pampered with ample supplies of fertiliser and water.
Environmental conditions, degree of light interception, nutrient
and water supply are key factors in reducing the efficiency
below the maximum while specific genetic characteristics
of particular plant species also dictates growth rates and
maximum yields of biomass.
On a global basis the efficiency of photosynthesis is sig-
nificantly lower than for agricultural and energy crops or algal
cultures growing under optimal conditions because of seasonal
changes and the existence of large portions of land and oceans
on our planet which do not sustain significant levels of
photosynthetic activity.13 Thus the 100 TW for the rate of
energy storage averaged over a year by photosynthesis repre-
sents just 0.1% conversion given that solar energy arrives on
our planet at a rate of 100 000 TW over the same time period.
This energy is stored mainly in wood and fibres of terrestrial
trees and plants. A similar amount of photosynthetic activity
occurs in the oceans but the fixed carbon is rapidly recycled
into the food chain.16 Therefore, an approximate efficiency of
global photosynthesis is 0.2% but with only half being stored
in biomass. Of course, it was terrestrial biomass that was the
major source of energy for humankind prior to the exploita-
tion of fossil fuels. It is not surprising therefore that there is
now a growing interest in returning to the use of biomass and
biofuels as an alternative to fossil fuels since their production
and use is carbon dioxide neutral.
Biomass
Wood and other forms of biomass can be used to generate
heat, electricity, biogas (mainly methane and carbon dioxide),
syngas (hydrogen and carbon monoxide) and other biofuels
(mainly bioethanol and biodiesel). Biomass is the end product
of photosynthesis and, as stated above, represents energy
conversion efficiencies in the region of 0.1 to 1.0% depending
on its origin. Many organisations consider ‘‘biomass power’’
as an increasingly attractive option to replace fossil fuels,
including the European Union, U.S. Department of Energy
(USDOE) and many national government departments and
agencies, major companies and utilities in countries like Brazil,
Finland, Sweden, UK and elsewhere. Currently the global use

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of biomass is equivalent to about 1.4 TW. In the US, biomass
surpasses hydroelectric power as a source of renewable energy
in providing over 3% of the country’s energy consumption,
corresponding to about 0.1 TW. However, a recent joint
report from the US Departments of Energy (USDOE) and
Agriculture (USDA)17 has concluded that biomass and
biofuels could provide the US with about 30% of its present
total energy needs. This would be achieved by utilising
non-food producing agricultural land and maximising on
forestry outlets to generate 1.3 billion tons of dry biomass
annually, corresponding to about 1 TW. This optimistic
projection also relies on plant breeding and genetic engineer-
ing strategies to produce new cultivars for high yields of
biomass requiring minimum input of fertilizers, water and
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pesticides. Moreover, improved technologies will be required
to maximise on the use of biomass including those for produ-
cing liquid biofuels to replace gasoline, such as second gen-
eration bioethanol. Also such calculations must take into
consideration the energy costs of maintaining ‘‘energy farms’’,
harvesting the biomass, transporting to a central location and
conversion into a usable form.
The major biomass-derived fuel is ethanol produced from
the fermentation of sugars or starches.18 Two countries, Brazil
and US are major producers of bioethanol, with a total
combined production being equivalent to about 0.02 TW.
Brazil has invested significantly in producing ethanol from
sugar cane which is used as a substitute or as an additive to
gasoline.19–21 Similarly the US has recently invested heavily in
the production of bioethanol from corn starch. Although the
production and use of ethanol, as well as other biofuels, has
been heavily subsidised, improved technologies and the rising
cost of petroleum means that these types of fuels are now
competing favourably with gasoline and, with the introduction
of new technologies to exploit lignocellulose as a source of
sugar for fermentation, could become major players.22,23
For millennia, biomass was the only primary energy source
available to humankind. For the last two centuries, however,
energy demand has outpaced biomass production. Although
biomass and its products such as bioethanol, can still con-
tribute to this demand in different ways and to different
extents depending on climate and available landmass, it is
hard to see how it could match the present level of global fossil
fuel consumption or to cope with increasing demands for
energy in the future. Using the best known plants for energy
production to achieve 20 TW corresponds to almost three
times all cultivatable land currently used for agriculture
globally. To reduce this to a reasonable level so as not to
seriously compete with food production would require the
biomass crops to have solar energy conversion efficiencies
close to the theoretical maximum of about 4.5%. Nevertheless,
if a new generation of energy crops could be produced by plant
breeding or genetic engineering which are environmentally
robust requiring minimal inputs of water and fertilizer and
can convert solar energy at efficiencies well above 1%, biomass
could make a significant contribution to global energy de-
mand. New and improved technologies to convert it into
useable fuel will also have to emerge if this source of energy
is to become available at a significant level. A particular
challenge is to derive new and efficient methods to release
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sugars from the lignocellulose which constitutes the majority
of the biomass and to improve fermentation technologies to
produce bioethanol.22,23
Finally we should remind ourselves that plant biomass is not
just a store of energy but is also a source of complex chemical
molecules that constitute our food and which provides us with
a wide range of valuable materials such as timber, linen,
cotton, oils, rubbers, sugars, starches etc. The increased use
of ‘designer’ plants to produce high value chemicals for the
chemical and pharmaceutical industries should not be under-
estimated.24
Although it may be possible to engineer plants and other
types of photosynthetic organisms (algae) as energy converting
‘machines’ and ‘chemical factories’ the overall efficiency of
solar energy conversion will rarely exceed 1% and will usually
be much less. However, the efficiency of the early photo-
chemical and chemical reactions of photosynthesis, which are
not directly involved in biomass production, is significantly
higher. Because of this there are alternative and complementary
approaches for utilizing solar energy. For example, it may
be possible to develop a highly efficient, artificial, molecular-
based solar energy converting technology which exploits the
principles of the ‘‘front-end’’ of natural photosynthesis.
Indeed, our knowledge of the natural process is sufficient to
provide a blue-print for the design and assembly of such
devices.
Photosynthesis and the water splitting reaction
As emphasised above, photosynthesis has produced most of
the energy that fuels human society and sustains life on our
planet. The process is underpinned by the light driven water
splitting reaction that occurs in PSII of plants, algae and
cyanobacteria (Fig. 2). Solar energy is absorbed by chloro-
phyll and other pigments and is transferred efficiently to the
PSII reaction centre where charge separation takes place. This
initial conversion of light energy into electrochemical potential
occurs in the reaction centre of PSII with a maximum thermo-
dynamic efficiency of about 70% and generates a radical pair
state P680 +Pheo  where P680 is a chlorophyll a molecule
and Pheo is a pheophytin a molecule (chlorophyll molecule
without a Mg ion ligated into its tetrapyrrole head group).
The redox potential of P680 + is very oxidising, estimated to
be more than +1 V while that of Pheo  is about 0.6 V. The
latter is sufficiently negative that, in principle, it could drive
the formation of hydrogen. Instead the reducing equivalent is
passed along an electron transport chain to PSI (see Fig. 2),
where it is excited by the energy of a second ‘red’ photon
absorbed by a chlorophyll molecule, known as P700, to give a
redox potential of 1 V or more. In this way sufficient energy
is accumulated to drive the fixation of carbon dioxide, which
not only requires the generation of the reduced ‘hydrogen
carrier’, nicotinamide adenine dinucleotide phosphate
(NADPH) but also the energy rich molecule adenosine triphos-
phate (ATP) formed by the release of some energy during
electron transfer from PSII to PSI (in the form of an electro-
chemical potential gradient of protons) (Fig. 2 and 3). The
P680 + species generated in PSII drives the splitting of water
at the oxygen evolving centre (OEC). It does so by extracting
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electrons from a catalytic centre composed of a cluster of four
manganese (Mn) ions and a calcium ion (Ca2+). The splitting
of water into dioxygen and reducing equivalents is a four
electron process and therefore PSII must absorb four photons
(4hn) to drive this reaction.
4hn
2H2 O ! O2 þ 4Hþ þ 4e
The reducing equivalents leave PSII in the form of plasto-
quinol (QH2) while the dioxygen is released into the atmo-
sphere.
4H+ + 4e + Q - O2 + 2QH2
The efficiency of this reaction is high being almost 55% when
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between PSII and PSI is aided by a third membrane protein
complex known as the cytochrome b6f (Cyt b6f) as detailed in
Fig. 3. The three complexes, PSI, PSII and Cyt b6f are located in
the photosynthetic membrane such that electron flow from water
to NADP+ is vectorial leading to the generation of a proton
gradient (see Fig. 3). This gradient is used chemiosmotically by a
fourth complex, CF0–CF1 to drive its ATPsynthase activity to
convert ADP to ATP and thus provide chemical energy for the
CO2 reduction process (for details see ref. 25).
In many ways, the photosystems of photosynthesis, includ-
ing those of anoxygenic photosynthetic bacteria (organisms
that do not split water) are highly efficient molecular photo-
voltaic nanomachines in that they use light energy to bring
about electrical charge separation across a membrane of high

driven by the energy of ‘red’ photons but decreases to about
20% when taking into account the fact that light is absorbed
across the whole solar spectrum. Of course, in photosynthetic
organisms the reaction can only proceed continuously when
the QH2 molecules are oxidised by the light absorbed by PSI
thus allowing reducing equivalents to be transferred to
NADH+ and then to carbon dioxide. Because of this the
quantum efficiency of photosynthetic water splitting is further
decreased.
The light-driven transfer of electrons and protons from H2O
to CO2, involves a number of redox active cofactors located in
the PSII and PSI protein complexes (see Fig. 3 and its legend
for specific details). The transfer of reducing equivalents
dielectric strength.26 The organisation of the electron carriers
and other cofactors in these nanomolecular devices are opti-
mised to facilitate forward energy storing reactions and mini-
mising backward and wasteful energy releasing reactions.
There is considerable information about these photosynthetic
photosystems which indicates that they are structurally and
functionally very similar.27,28 Indeed, there are aspects of their
design which could be incorporated into an ‘artificial photo-
synthetic’ device and are similar to existing photovoltaic
systems, particularly the dye-sensitised photoelectrochemical
solar cells developed by Graetzel and his colleagues.10
Similarly the light harvesting systems associated with the
photosystems of different types of photosynthetic organisms

Fig. 3 Schematic diagram of the electron–proton transport chain of oxygenic photosynthesis in the thylakoid membrane, showing how
photosystem I (PSI) and photosystem II (PSII) work together to use absorbed light to oxidise water and reduce NADP+, in an alternative
representation to the Z-scheme shown in Fig. 2. The diagram also shows how the proton gradient generated by the vectorial flow of electrons
across the membrane is used to convert ADP to ATP at the ATP synthase complex (CF0–CF1). In both PSI and PSII, the redox-active cofactors
are arranged around a pseudo-two-fold axis. In PSII, primary charge separation and subsequent electron flow occurs along one branch of the
reaction centre. However, in the case of PSI, it is likely that electron flow occurs up both branches as shown. Electron flow through the cytochrome
b6f complex also involves a cyclic process known as the Q cycle. YZ = tyrosine; P680 = primary electron donor of PSII composed of chlorophyll
(Chl); Pheo = pheophytin; QA and QB = plastoquinone; Cyt b6f = cytochrome b6f complex, consisting of an Fe–S Rieske centre, cytochrome f
(Cyt f), cytochrome b low- and high-potential forms (Cyt bLP and Cyt bHP), plastoquinone binding sites, Q1 and Q0; PC = plastocyanin; P700 =
primary electron Chl donor of PSI; A0 = Chl; A1 = phylloquinone (Q); Fx, FA and FB = Fe–S centres, FD = ferredoxin; FNR = ferredoxin
NADP reductase; NADP+ = oxidised nicotinamide adenine dinucleotide phosphate. YD = symmetrically related tyrosine to YZ but not directly
involved in water oxidation, and QH2 = reduced plastoquinone (plastoquinol), which acts as a mobile electron/proton carrier from PSII to the
cytochrome b6f complex. With the exception of the mobile electron carriers, PQ/PQH2 , PC and FD, the remaining redox active cofactors are
bound to multisubunit protein complexes which span the membrane depicted as coloured boxes. Similarly CF0–CF1 is a multisubunit membrane
spanning complex. Modified from ref. 13.

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have common principles for capturing solar energy across the
whole of the visible spectrum and facilitating efficient energy
transfer to the associated reaction centres with minimum
losses of energy. Again detailed spectroscopic and structural
studies have revealed the molecular basis of these systems,
details which could also be adopted for designing light con-
centrating systems for a new generation of solar energy
converting technologies.29 However it is the water splitting
reaction of PSII which holds the greatest promise for devel-
oping new technologies for converting solar radiation into
usable energy, particularly in generating hydrogen or ‘‘high
energy electrons’’ for reducing carbon dioxide. In this way
PSII is unique when compared with all other types of photo-
systems which are far more limited in the redox chemistry they
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molecules. From that moment, living organisms on Earth
could prosper and diversify on an enormous scale; biology
had solved its energy problem and PSII established itself as the
‘‘engine of life’’.30
Clearly, using solar energy to split water to produce hydro-
gen or ‘‘high energy’’ electrons is also the perfect solution for
humankind. In principle, the technology exists today to do
this. Electricity can be generated by photovoltaic solar cells
and used to carry out the electrolysis of water. With a solar cell
efficiency of 10% and 65% efficiency for the electrolytic
system, the overall efficiency would be 6.5%. Electrolysis relies
on platinum or other catalysts for gas evolution, which are in
limited supply and therefore expensive. At present very little
hydrogen is generated by electrolysis because of the lower

catalyse. price of electricity generated by conventional means. Similarly,

Photosystem II
The photosynthetic water splitting reaction appeared on our
planet about 2.5 billion years ago and was the ‘big bang of
evolution’ since for the first time living organisms had avail-
able an inexhaustible supply of ‘hydrogen’ (in the form of
reducing equivalents) to convert carbon dioxide into organic
the cost of photovoltaic solar cells marginalises this route for
using solar energy to produce hydrogen directly from water.
But perhaps a bio-inspired water splitting catalyst can be
devised which works along similar chemical principles em-
ployed by the OEC of PSII.
Because of the importance of understanding the chemistry
of the water splitting reaction of PSII there has been a wide
range of techniques employed to probe the molecular

Fig. 4 Side view of the structure of Photosystem II, the water splitting enzyme of photosynthesis. This structure was determined by X-ray
crystallography.39 The complex is embedded in the thylakoid membrane spanning between their lumenal and stromal surfaces. It is composed of
two monomers related to each other by a two-fold axis. Each monomer contains 19 different protein subunits with 16 being located within the
membrane matrix and having s-helices (depicted by cylinders). In total there are 35 transmembrane helices. The D1- and D2-proteins that
compose the reaction centre are shown in yellow and orange, respectively. 57 cofactors were assigned to the structure, including 36 chlorophyll a
molecules. Of particular importance was characterisation of the water splitting site consisting of a cubane-like organisation of a Mn3CaO4-cluster
with a fourth Mn linked to the cubane by mono-m-oxo bridges (see insert where Mn ions are shown in magenta, calcium in turquoise and oxygen
atoms in red). This catalytic centre is located on the lumenal side of the complex and is stabilised and shielded by three extrinsic proteins, PsbO,
PsbU and PsbV. Also shown in the insert are the amino acids which provide ligands to the metal cluster. Figure modified from ref. 39.

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mechanisms involved and to investigate the structure of the
catalytic centre (see various articles in refs. 31 and 32), being
particularly spurred by the recent structural analyses of PSII
by X-ray absorption spectroscopy33–36 and X-ray crystallo-
graphy.37–40 These studies, coupled with quantum mechanical
analyses have provided refinement of the structure of the
OEC41–43 allowing detailed schemes to be formulated for the
water splitting chemistry mechanism leading to O–O bond
formation.44–50
Structure of PSII
The first complete and refined crystal structure of PSII was
reported by Ferreira et al.39 which revealed considerable
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information about the organisation of the Mn4Ca-cluster
and the details of its protein environment. Similarly the
protein environments of the other cofactors involve in light
absorption and charge separation where revealed. In this
work, PSII was isolated as a dimeric complex from a cyano-
bacterium called Thermosynechococcus elongatus. Each mono-
mer contained 19 different protein subunits with the reaction
centre, composed of the D1 and D2 proteins, at its heart
(see Fig. 4). A crystal structure published later of cyano-
bacterial PSII had one extra peripheral subunit40 possibly
reflecting different biochemical procedures for its isolation.
The crystal structure of PSII determined by Ferreira et al.
(2004) confirmed earlier models37,38 for the organisation of the
cofactors involved in primary and secondary charge separa-
tion in the reaction centre although these earlier studies did
not provide details about their protein environments. However
the most important outcome of the Ferreira et al. structural
study, was the suggestion that three Mn ions and a Ca ion of
the OEC form a cubane-like structure with the four metal ions
linked by oxo-bridges. It was proposed that a fourth Mn ion is
linked to the cubane by mono-m-oxo bridges via one of the oxo
groups of the cubane (see Fig. 4 inset). Surrounding the
Mn4Ca-cluster are a number of amino acid residues that either
provide ligands to the metal ions or act to facilitate hydrogen
bonding networks which almost certainly play a key role in the
deprotonation of the substrate water molecules. A nearby
tyrosine (residue 161 of the D1 protein), hydrogen bonded
to a histidine (D1His190), is the redox active cofactor YZ
which functions as an intermediate electron carrier between
the Mn4Ca-cluster and P680 + (see Fig. 3). Most of the amino
acids identified in the OEC belong to the D1 protein although
another PSII protein, known as CP43, also provides key
residues. All these amino acids are fully conserved in all
known amino acid sequences of the D1 and CP43 proteins
whether they are from prokaryotic cyanobacteria or eukaryo-
tic algae and higher plants. We can therefore assume based on
current knowledge, that there is no variation on a theme for
this catalytic centre, which is able to carry out one of the most
oxidative and difficult reactions of biology.
With structural information available, realistic chemical
schemes are now being formulated for the water splitting
reaction and the formation of molecular oxygen. It has been
known for some time that there are at least five intermediate
states leading to the formation of dioxygen, known as S-states.
The sequential advancement from S0 to S4 is driven by each
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photochemical turnover of the PSII reaction centre as depicted
in the S-state cycle (Fig. 5)
The progression through the S-states to S4 results in the
storing of four oxidising equivalents, which are reduced in the
final step (S4 to S0) by four electrons derived from two
substrate water molecules with the concomitant formation of
dioxygen.
As explained above, the processes underpinning this cata-
lytic S-state cycle are initiated by the absorption of visible light
by P680 and the crystal structure indicates that this primary
electron donor is composed of four closely located Chls
designated PD1, PD2 ChlD1 and ChlD2 in Fig. 6. Excited
P680 (depicted as P680* in Fig. 2) is probably delocalised
over all four Chls and that initial electron donation to the
primary electron acceptor, pheophytin a (Pheo D1) occurs
from ChlD1. The formation of the primary radical pair takes
place in a few picoseconds and probably involves ‘‘hole’’
migration to PD1 to form PD1 +Pheo . Stabilisation of the
PD1 +Pheo  state is accomplished by electron transfer from
Pheo  to a plastoquinone acceptor QB in the microsecond to
millisecond time domain according to its redox state. This
terminal quinone electron acceptor is bound to the D1 protein
while the intermediate plastoquinone molecule QA, which
facilitates the electron transfer from Pheo  to QB is bound
to the D2 protein of the reaction centre. A non-heam iron (Fe)
is located midway between QA and QB, having four histidine
ligands provided equally by the D1 and D1 proteins coupled
with bidentate ligation of a bicarbonate ion. Unlike QB, QA
plastoquinone is tightly bound to the D2 protein, functions as
a single electron acceptor and does not undergo protonation.
The QB plastoquinone, however, accepts two electrons and is
fully protonated prior to its departure from the reaction centre
via the hydrophobic lipid phase of the membrane and in this
Fig. 5 The S-state cycle showing how the absorption of four photons
of light (hn) by P680 drives the splitting of two water molecules and
formation of O2 through a consecutive series of five intermediates
(S0, S1, S2, S3 and S4). Protons (H+) are released during this cycle
except for the S1 to S2 transition. Electron donation from the Mn4Ca-
cluster to P680 + is aided by the redox active tyrosine YZ. Also shown
are half-times for the various steps of the cycle.
Chem. Soc. Rev., 2009, 38, 185–196 | 191

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Fig. 6 Organisation of the electron transfer cofactors that make up
the reaction centre of Photosystem II as revealed by X-ray crystal-
lography.39 Excitation of the reaction centre via the chlorophylls (Chl)
shown in green leads to the reduction of pheophytin (Pheo) resulting in
the formation of the radical pair P680 +Pheo . The radical cation of
P680 is localized on PD1 while the radical anion is located on PheoD1.
The electron on PheoD1  is rapidly donated to a firmly bound
plastoquinone QA (shown in purple) and then transferred to a second
plastoquinone QB (also shown in purple). This electron transfer is
aided by the presence of a non-haem iron (Fe) located mid-way
between them. When the QB plastoquinone has been doubly reduced
and protonated the resultant plastoquinol (PQH2) diffuses from the
QB-binding site into the lipid matrix of the membrane, P680 + is
reduced by a redox active tyrosine (TyrZ or YZ) which then extracts
electrons from the Mn4Ca-cluster that constitutes the oxygen-evolving
centre (OEC). These electron transfer processes occur mainly on the
D1-side of the reaction centre as shown by the red arrow. Some of the
symmetrically related cofactors located on the D2-side (PheoD2) are
non-functional. Other cofactors shown on the D2-side, however, are
functionally active and seem to play a role in protecting PSII against
photoinduced damage, the haem of cytochrome b559 (Cyt b559 shown
in red), the b-carotene molecule (shown in brown) and ChlZD2. Figure
modified from ref. 39.
way enter the electron/proton transfer chain as described in
Fig. 2 and 3.
On the oxidising side of the PSII reaction centre, which is
localised towards the lumenal surface of the thylakoid mem-
brane, P680 + provides the oxidising potential to split water
with the redox active tyrosine YZ (TyrZ) aiding the electron/
proton removal from the OEC.
As can be in Fig. 6 the electron transfer giving rise to the
reduction of QB and oxidation of water is biased to the D1-
side of the reaction centre. However other side reactions can
occur under some conditions on the D2-side which involve the
P680 + driven oxidation of high potential cytochrome b559
(Cyt b-559), a b-carotene molecule and a Chla molecule
(ChlZ).51–54 These side reactions occur on the tens of milli-
second time scale and therefore do not compete with the
electron transfer pathway leading to water oxidation. Indeed,
they probably only occur when the rate of water oxidation
becomes limited and thus provides a protective mechanism
against the detrimental reactions resulting from the very high
redox potential of the long lived P680 radical cation.
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New developments
The model proposed by Ferreira et al.39 for the OEC has
recently been analysed in considerable depth using quantum
mechanical and molecular mechanical (QM/MM) analyses.41,42
The calculations assumed that the carbonate ion, tentatively
identified as a ligand in the OEC is replaced by a chloride ion
in the active S1 state of the water splitting catalytic cycle and
that the assigned protein ligands were complemented by water
and hydroxyl ligands to satisfy the coordination requirements
of the five metal ions. Even with these adjustments the
calculated model for the metal cluster was remarkably similar
to that proposed by Ferreira et al.39 and confirmed that it is a
chemically stable structure. Despite, the good correlation
between the Ferreira et al. structural model of the OEC and
theoretical calculations there are inconsistencies with distance
and angular information derived from EXAFS. Indeed recent
polarised EXAFS studies conducted on single crystals of PSII
isolated from T. elongatus (Yano et al. 2006) gave at least
four different arrangements for the Mn4Ca-cluster while
more recent crystal structures reported40 suggest yet another
organisation. Radiation damage during the collection of X-ray
diffraction data has been implied as being the cause for
inconsistencies between the different models.55 Recently
Barber and Murray56 have attempted to rationalise the exist-
ing data to provide a series of working models of the OEC.
The differences between them are not large having the same
amino acid environments as first defined by Ferreira et al.39
Fig. 7C shows one such model in which the fourth Mn (Mn4)
is linked to the Mn3CaO4-cubane via one of its Mn rather than
by a bridging oxygen of the cubane.57 As a consequence this
new arrangement has one rather than two mono-m-oxo bonds
and is more compatible with EXAFS analyses.58 The adjust-
ment of the linkage between Mn4 and the cubane requires a
repositioning of the other Mn ions and therefore changes in
the amino acid ligation pattern as emphasised by comparing
Fig. 7B and 7D. Despite uncertainty about the precise orga-
nisation of the Mn4Ca-cluster, the most recent simulation of
the polarised EXAFS data by Sproviero et al.43 continues to
provide support for their QM/MM derived model of the
OEC41,42 and therefore for the original model proposed by
Ferreira et al.39
Mechanism of water splitting and dioxygen formation
Although the geometry of the Mn4Ca-cluster and its exact
ligand field characteristics are not yet known precisely, either
for its relaxed S1-state or for higher S-state conditions, the
models available do provide a basis for developing chemical
mechanisms for water oxidation and dioxygen formation. The
Mn ion outside the cubane (Mn4) is adjacent to the Ca2+.
Their positioning towards the side chains of several key amino
acids, including the redox active YZ suggests that they provide
the ‘catalytic’ surface for binding the two substrate water
molecules and their subsequent oxidation. One well cham-
pioned mechanism45,46,59,60 suggests that the substrate water,
associated with Mn4, is deprotonated during the S-state cycle
and converted to a highly electrophilic oxo (see Fig. 8A). This
mechanism is dependent on Mn4 being converted to a high
oxidation state (possible Mn(V)) during progression to the
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Fig. 7 The water splitting site of PSII showing the Mn4Ca-cluster positioned within the Mn-anomalous difference map of Ferreira et al.39 (A)
Based on the model of Ferreira et al. (39). (B) Schematic representation of the amino acid ligation pattern for model in (A) with distance less than
3 Å shown by connecting lines. (C) Remodelling the water splitting site using the native electron density maps of Ferreira et al.39 and Loll et al.40
and Mn-anomalous difference map of Ferreira et al.,39 keeping the Mn3CaO4 cubane of Ferreira et al. but with the fourth Mn linked to it via a
single 3.3 Å mono-m-oxo bridge (D) Schematic representation of the amino acid ligation pattern for model in (C) with distance less than 3 Å shown
by connecting lines. The Mn-anomalous difference map is shown in red and contoured at 5s with the fitting of the metal ions into this density by
real-space refinement using the molecular graphics programme. Arrow indicates the direction of the normal to the membrane plane (taken from
refs. 56 and 57).

S4-state just prior to O–O bond formation. The other three

Mn ions are progressively driven into high valency states
(Mn(IV) and act as a further ‘‘oxidising battery’’ for the
Mn(V)-oxo species in the S4-state (see Fig. 8A). In this way
the reactive oxo is electron deficient, so much so that it makes
an ideal target for a nucleophilic attack by the oxygen of the
second substrate water bound within the coordination sphere
of the Ca2+ (see Fig. 8A). An alternative mechanism proposed
by Siegbahn, which is based on in depth density function
theory (DFT) calculations,49 suggests that the deprotonated
water molecule on Mn4 forms an oxyl radical and that this
attacks an oxo-ligand of the Mn3CaO4-cubane (see Fig. 8B.)

Fig. 8 Two different mechanisms for the final step of the S-state cycle
when the dioxygen bond of O2 is formed. (A) Mechanism 1. The very
high oxidation state of the Mn-cluster, particularly the Mn ion outside
the Mn3CaO4-cubane, leads to a highly electron deficient oxo (after
deprotonation of water molecules during the S-state cycle). Nucleo-
philic attack by the hydroxide of the second substrate water within the
coordination sphere of Ca2+ leads to O2 formation. (B) Mechanism 2.
The formation of a oxyl radical after deprotonation of the substrate
water molecule ligated to the Mn outside the cubane leads to a radical
attack of an oxo-ligand within the Mn3CaO4-cubane.
Artificial photosynthesis
While some progress has been made in mimicking photosynth-
esis in artificial systems, researchers have not yet developed
components that are both efficient and robust for incorpora-
tion into a working system for solar fuel production. To date
the main focus of research has been to design and synthesise
molecular systems consisting of electron donors and acceptors
and mimic light driven charge separation which occurs in
photosynthetic reaction centres.61,62 These studies have
allowed rigorous analyses of the dependencies of electron
transfer efficiency on the physical and chemical properties

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(donor/acceptor distance and orientation, free energy of the
reaction and electronic interactions) of the system thus pro-
viding basic rules for their construction, including the desir-
ability for multi-step charge separation.63
The bio-inspired systems employ chromophores to absorb
light energy which are analogous with the photosynthetic
pigments, such as chlorophyll. Often, however, the chromo-
phores are directly engaged in electron transfer processes64
and in this way act like redox active chlorophylls within
photosynthetic reaction centres, for example P680 and P700.
Having an antenna, or light harvesting array, without carrying
out charge separation itself, is an engineering design adopted
by natural photosynthesis to maximise solar energy absorp-
tion. Covalently linked arrays of light harvesting chromo-
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phores that funnel energy to a central site where charge
separation can occur have been demonstrated in artificial
systems.65,66 However the synthesis of such arrays requires
significant effort and it would be desirable to create self-
assembly, functional antenna arrays using robust dyes such
as those used as pigments in industrial paints.
Despite the fact that PSII contains the chemical machinery
to split water into oxygen and ‘‘hydrogen’’ no artificial photo-
chemical system has been built to mimic this reaction.
However the insights gleaned from the recent structural
determination of PSII have major implications for the design
of an artificial catalytic system for using solar energy to release
hydrogen from water.67 The hydrogen produced could be used
directly as a source of energy but could also be used, as it is in
photosynthesis, to reduce carbon dioxide to other types of
fuels such as methane. Artificial catalysts designed to repro-
duce the reactions of PSII may also have to incorporate other
bio-inspired features, particularly the employment of light
harvesting systems which can capture the energy of all the
colours of the visible solar spectrum and efficiently use this
energy to drive the chemistry of water splitting. Our under-
standing of natural photosynthetic light harvesting systems
and how they are coupled to reaction centres is at an advanced
level such that the basic principles of their construction and
operation are now well established.
The challenge is to have a molecular arrangement in the
artificial catalyst which will use light energy to split water,
allow the dioxygen bond to form and concomitantly provide
reducing potential for hydrogen gas production or CO2
reduction. It has been demonstrated that catalysts based on
Mn are capable of water splitting and the generation of
dioxygen occurs when a strong oxidant is used to drive the
Mn into high oxidation states; believed to be Mn(V).68,69
Complementing this was the earlier discovery that ruthenium
based catalysts, such as the ‘‘blue dimer’’ can photooxidise
water to dioxygen.70–72
Light driven water splitting can also be accomplished using
semiconductor-based photocatalysis as first demonstrated by
Fujishima and Honda in 1972.73 These workers initially used
TiO2 but it was necessary to replace TiO2 by SrTiO3 in order
to produce both hydrogen and oxygen. Since these reactions
are driven by high energy UV radiation they are of limited use
for fuel generation. Current efforts are being made to dope
these types of semiconductors with dyes which can carry out
photo-driven redox reactions using visible light.74 Combining
194 | Chem. Soc. Rev., 2009, 38, 185–196
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photovoltaic technology with appropriate electrochemical cat-
alysts is a complementary approach. For example, recently
Kanan and Nocera75 have described a self-assembling catalyst
composed of cobalt and phosphate ions which can efficiently
produce molecular oxygen from water at neutral pH
with a low over potential akin to that which operates in
the OEC of PSII. The next step will be to couple this oxygen
producing system to another catalyst which will use
the electrons and protons derived from the water splitting
reaction to produce hydrogen gas or reduce carbon dioxide.
In the case of the former, considerable progress is being
made, in part by mimicking the natural hydrogenase enzymes
found in a wide variety of microorganisms.76–78 The reduction
of carbon dioxide, however, is more difficult because multi-
electron reactions are required and the emergence of catalysts
for generating useful carbon fuels will require considerable
effort.79,80
Conclusions
It is anticipated that the global demand for energy will more
than double by the mid-century and perhaps more than triple
by the end of the century. Satisfying this demand will be
necessary in order to achieve vibrant technological progress,
economic growth and most importantly, political stability over
the coming decades. Already we are faced with the prospect of
catastrophic climate change due to the release of carbon
dioxide into the atmosphere brought about by the burning
of fossil fuels. In the short term we must exploit all technol-
ogies known to us to produce energy while at the same time
reduce carbon dioxide emission. The nature of the mix will
vary between different countries depending on their resources
and populations with some dominating (e.g. geothermal in
Iceland, biomass in Brazil, etc). Coupled with this challenge
is to use energy more efficiently. Here again we can learn
from Nature. In biology the ‘combustion’ of fuel (food) is
accomplished isothermally by highly efficient and subtle bio-
logical reactions involving a host of clever enzymes. For
example, when the ‘hydrogen’ of glucose is combined with
oxygen during the process of respiration to produce water
and carbon dioxide, 38 ATP molecules are made. ATP is
the energy currency of cells. Since ATP stores 12 kcal mol1
(50 kJ mol1) of usable energy and the energy content of
glucose is 672 kcal mol1 (2813 kJ mol1) the efficiency of
energy conversion is 68%. It therefore seems to me that
mankind should follow biology’s example and strive to devel-
op new technologies that are as energy efficient as those in
biology. In a sense the invention of the World Wide Web is an
example of how new technologies based on microelectronics
has provided a way to communicate throughout the globe
which is far more energy efficient compared with conventional
mailing. This significant advance and many other similar
examples were unthinkable a few years back and give opti-
mism for the development of new technologies which will
generate energy and use it with maximum efficiency.
For the long term we will have very few options to replace
fossil fuels and satisfy the increased energy demands of a
global population of 10 billion. Renewables such as hydro-
power, wind, wave, geothermal and biomass will not be able to
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supply energy equivalent to 20 TW even when taken
together.4,81 Nuclear fission is a short term solution but in
the long run will probably not be a realistic option. Nuclear
fusion is a possibility but the construction of a working reactor
is proving problematic. Nevertheless we must continue to
research this technology with the hope that it will come on
stream sooner or later. But there is another nuclear reaction
which is already up and running, namely the Sun. Our sun is
the champion of energy sources: delivering more energy to the
earth in an hour than we currently use in a year from fossil,
nuclear and all renewable sources combined. Its energy supply
is inexhaustible in human terms, and its use is harmless to our
environment and climate.
The enormous untapped potential of solar energy is
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an opportunity which should be addressed with urgency.
Biology chose this energy source and there is no reason why
the chemical reactions devised by photosynthetic organisms
cannot be mimicked by ingenuity of humans. We already have
a considerable knowledge base and emerging nanotechnologies
to exploit. With a concerted input of the talents of scientists
trained in different disciplines it should be possible to move
the technologies of solar energy conversion forward. The
recognition of a Manhattan- or Apollo-like initiative
to develop new sustainable energy technologies in response
to the CO2 problem as suggested by Hoffert et al.2,82 should be
the driver for encouraging basic and applied research in
this area.
Abbreviations used
ATP Adenosine triphosphate
CF0–CF1 ATPsynthase complex
Chl Chlorophyll
CP43 Chlorophyll binding PsbC protein of PSII
Cyt b6f Cytochrome b6f
DFT Density Functional Theory
EXAFS Extended X-ray absorption fine structure
OEC Oxygen Evolving Centre
PSI Photosystem I
PSII Photosystem II
Pheo Pheophytin
P680 Primary electron donor chlorophyll in PSII
P700 Primary electron donor chlorophyll in PSI, NADP+,
nicotinamide adenine dinucleotide phosphate
QM/MM Quantum Mechanical and Molecular Mechanical
Acknowledgements
I wish to thank the Biotechnology and Biological Science
Research Council (BBSRC) for the financial support that led
to the determination of the structure of PSII. I have drawn on
information from a wide range of sources but I would
particularly like to acknowledge that my thinking has been
significantly influenced by discussion with Professors Nathan
Lewis and Harry Gray of Caltech and Professor Daniel
Nocera at MIT, all of whom are strong advocates of using
solar energy as an inexhaustible and non-polluting source of
energy for the long term benefit of humankind.
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References
1 Energy Information Administration 2005 Annual Energy Outlook,
US Dept of Energy, Washington DC.
2 M. T. Hoffert, K. Caldeira, A. K. Jain, E. F. Haites, L. D. Harvey,
S. D. Potter, M. E. Schlesinger, T. M. L. Wigley and
J. J. Wuebbles, Nature, 1998, 395, 881.
3 Special Report on Emissions Scenarios, Intergovernmental Panel on
Climate Change, ed. N. Nakicenovic and R. Swart, Washington,
DC, 2000, pp. 48–55.
4 N. S. Lewis and D. G. Nocera, Proc. Natl. Acad. Sci. U. S. A.,
2006, 43, 15729.
5 United Nations Development Program 2003 World Energy
Assessment Report: Energy and the Challenge of Sustainability
(United Nations, New York).
6 Intergovernmental Panel on Climate Change 2001, Synthesis Re-
port Summary for Policymakers (Intergovernmental Panel on
Climate Change, Washington, DC) Third Assessment Report.
7 Carbon Dioxide Capture and Storage, ed. B. Metz, O. Davidson,
X. deConinck, H. M. Loos, L. Meyer, Intergovernmental Panel on
Climate Change, Washington, DC, 2005.
8 Solar Energy Utilization Workshop, Basic Science Needs for Solar
Energy Utilization, US Dept of Energy, Washington, DC, 2005.
9 S. E. Shaheen, D. S. Ginley and G. E. Jabbour, MRS Bull., 2005,
30, 10–19.
10 D. P. Hagberg, J.-H. Yum, H.-J. Lee, F. De Angelis, T. Marinado,
K. M. Karlsson, R. Humphry-Baker, L.-C. Sun, A. Hagfeldt,
M. Graetzel and M. K. Nazeeruddin, J. Am. Chem. Soc., 2008,
130, 6259.
11 E. H. Thorndike, Energy and the Environment, Pub Addison-
Wesley, Reading Mass, USA, 1996.
12 D. A. Walker, Energy Plants and Man, Pub Packard Publishing
Ltd, Chichester UK, 1977.
13 M. D. Archer and J. Barber, in: Molecular to Global Photosynthesis,
ed. M. D. Archer and J. Barber, Pub Imperial College Press,
London, UK, 2004, pp. 1–41.
14 J. R. Bolton, Solar Power and Fuels, Academic Press, New York,
USA, 1977.
15 J. R. Bolton, in: The Chemical Conversion and Storage of Solar
Energy, ed. J. B. King, R. R. Hautala and C. R. Kutal, Humana
Press, Clifton, NJ, USA, 1979, pp. 31–50.
16 P. G. Falkowsky and J. A. Raven, Aquatic Photosynthesis, Blackwell,
Oxford, 1997.
17 USDA/DOE Report 2005 A billion to feedstock supply for a
bioenergy and bioproducts industry.
18 A. V. Bridgewater and K. Maniatis, in Molecular to Global
Photosynthesis, ed. M. D. Archer and J. Barber, Imperial College
Press, London, UK, 2004, pp. 521–611.
19 H. S. Geller, Ethanol fuel from sugar cane in Brazil, Annu. Rev.
Energy, 1985, 10, 135.
20 J. Goldemberg, Ethanol for a Sustainable Energy Future Science,
2004, 315, 808.
21 J. Goldemberg, S. T. Coelho, O. Lucon and P. M. Nastari,
Biomass Bioenergy, 2004, 26, 301.
22 M. D. Bullard, in Molecular to Global Photosynthesis, ed.
M. D. Archer and J. Barber, Imperial College Press, London,
UK, 2004, pp. 453–519.
23 C. Somerville, S. Bauer, G. Brininstool, M. Facette, T. Hamann,
J. Milne, E. Osborne, A. Paredez, S. Persson, T. Raab, S. Vorwerk
and H. Youngs, Science, 2004, 306, 2206.
24 A. J. Ragauskas, C. K. Williams, B. H. Davison, G. Britovsek,
J. Cairney, C. A. Eckert, J. Frederick, J. P. Hallett, D. Leak,
C. L. Liotta, J. R. Mielenz, R. Murphy, R. Templer and
T. Tschaplinski, Science, 2006, 311, 484.
25 R. E. Blankenship, Molecular Mechanisms of Photosynthesis,
Blackwell Science, Oxford UK, 2002.
26 J. Barber and B. Andersson, Nature, 1994, 370, 31.
27 W. D. Schubert, O. Klukas, W. Saenger, H. T. Witt, P. Fromme
and N. Krauss, J. Mol. Biol., 1998, 280, 297.
28 K.-H. Rhee, E. P. Morris, J. Barber and W. Kühlbrandt, Nature,
1998, 396, 283.
29 H. van Amerongen, L. Valkunas and R. van Grondelle, Photo-
synthetic Excitons, World Scientific, Singapore, 2000.
30 J. Barber, Photosystem II: The engine of life, Biophys. Q. Rev.,
2003, 36, 71.
Chem. Soc. Rev., 2009, 38, 185–196 | 195

31 T. J. Wydrzynski and K. Satoh, Photosystem II: The Light-Driven
Water Plastoquinone Oxidoreductase, in Vol. 22 Advances in Photo-
synthesis and Respiration, Springer, Dordrecht, The Netherlands,
2005, pp. 1–786.
32 J. Barber and A. W. Rutherford, Revealing how nature uses
sunlight to split water, Philos. Trans. R. Soc. London, Ser. B,
2003, 363, 1123.
33 J. Yano, J. Kern, K. Sauer, M. J. Latimer, Y. Pushkar,
J. Biesiadka, B. Loll, W. Saenger, J. Messinger, A. Zouni and
V. K. Yachandra, Science, 2006, 314, 821.
34 K. Sauer, J. Yano and V. K. Yachandra, Coord. Chem. Rev., 2008,
252, 318.
35 J. Yano and V. K. Yachandra, Inorg. Chem., 2008, 47, 1711.
36 Y. Pushkar, J. Yano, K. Sauer, A. Boussac and V. K. Yachandra,
Proc. Natl. Acad. Sci. U. S. A., 2008, 105, 1879.
37 A. Zouni, H. T. Witt, J. Kern, P. Fromme, N. Krauss, W. Saenger
and P. Orth, Nature, 2001, 409, 739.
Published on 10 November 2008. Downloaded on 2/12/2020 5:47:48 AM.
38 N. Kamiya and J. R. Shen, Proc. Natl. Acad. Sci. U. S. A., 2003,
100, 98.
39 K. N. Ferreira, T. M. Iverson, K. Maghlaoui, J. Barber and
S. Iwata, Science, 2004, 303, 1831.
40 B. Loll, J. Kern, W. Saenger and J. Biesiadka, Nature, 2005, 438, 1040.
41 E. M. Sproviero, J. A. Gascon, J. P. McEvoy, G. W. Brudvig and
V. S. Batista, J. Chem. Theory Comput., 2006, 2, 1119.
42 E. M. Sproviero, J. A. Gascon, J. P. McEvoy, G. W. Brudvig and
V. S. Batista, Curr. Opin. Struct. Biol., 2007, 17, 173.
43 E. M. Sproviero, J. A. Gascon, J. P. McEvoy, G. W. Brudvig and
V. S. Batista, J. Am. Chem. Soc., 2008, 130, 3428.
44 J. P. McEvoy and G. W. Brudvig, Phys. Chem. Chem. Phys., 2004,
6, 4754–4763.
45 J. Messinger, Phys. Chem. Chem. Phys., 2004, 6, 4764–4771.
46 J. P. McEvoy and G. W. Brudvig, Chem. Rev., 2006, 106, 4455.
47 P. E. M. Siegbahn and M. Lundberg, Photochem. Photobiol. Sci.,
2005, 4, 1035.
48 P. E. M. Siegbahn, Chem.–Eur. J., 2006, 12, 9217.
49 P. E. M. Siegbahn, Inorg. Chem., 2008, 47, 1779.
50 E. M. Sproviero, J. A. Gascon, J. P. McEvoy, G. W. Brudvig and
V. S. Batista, Coord. Chem. Rev., 2008, 252, 395.
51 D. H. Stewart and G. W. Brudvig, Biochim. Biophys. Acta, 1998,
1367, 63.
52 P. Faller, A. Pascal and A. W. Rutherford, Biochemistry, 2001, 40,
6431.
53 A. Telfer, Philos. Trans. R. Soc. London, Ser. B, 2002, 357, 1431.
54 C. A. Tracewell and G. W. Brudvig, Biochemistry, 2003, 42, 9127.
55 J. Yano, J. Kern, K. D. Irrgang, M. J. Latimer, U. Bergmann,
P. Glatzel, Y. Pushkar, J. Biesiadka, B. Loll, K. Sauer,
J. Messinger, A. Zouni and V. K. Yachandra, Proc. Natl. Acad.
Sci. U. S. A., 2005, 102, 12047.
56 J. Barber and J. W. Murray, Philos. Trans. R. Soc. London, Ser. B,
2008, 363, 1129.
57 J. Barber and J. W. Murray, Coord. Chem. Rev., 2008, 252, 233.
58 V. K. Yachandra, Philos. Trans. R. Soc. London, Ser. B, 2002, 357, 1347.
59 J. Messinger, M. Badger and T. Wydrzynski, Proc. Natl. Acad. Sci.
U. S. A., 1995, 92, 3209.
60 V. L. Pecoraro, M. J. Baldwin, M. T. Caudle, M. W.-Y. Hsieh and
N. A. Law, Pure Appl. Chem., 1998, 70, 925.
196 | Chem. Soc. Rev., 2009, 38, 185–196
View Article Online
61 D. Gust, T. A. Moore and A. L. Moore, Acc. Chem. Res., 2001, 34,
40.
62 L. Sun, L. Hammarström, B. Åkermark and S. Styring, Chem. Soc.
Rev., 2001, 30, 36.
63 C. C. Page, C. C. Moser, X. Chen and P. L. Dutton, Nature, 1999,
427, 607.
64 L. Hammerstrom and S. Styring, Philos. Trans. R. Soc. London,
Ser. B, 2008, 363, 1283.
65 S. Kirstein and S. Daehne, Int. J. Photoenergy, 2006, Article ID
20363, 21 pp.
66 J. L. Allwood, A. K. Burrell, D. L. Officer, S. M. Scott, K. Y. Wild
and K. C. Gordon, Chem. Commun., 2000, 747.
67 R. Eisenberg and H. B. Gray, Inorg. Chem., 2008, 47, 1697.
68 J. Limberg, J. S. Vrettos, L. M. Liable-Sands, A. L. Rheingold,
R. H. Crabtree and G. W. Brudvig, Science, 1999, 283, 1524.
69 R. Tagore, R. H. Crabtree and G. W. Brudvig, Inorg. Chem., 2008,
47, 1815.
70 S. W. Gersten, G. J. Samuels and T. J. Meyer, J. Am. Chem. Soc.,
1982, 104, 4029.
71 F. Liu, J. J. Concepcion, J. W. Jurss, T. Cardolaccia,
J. L. Templeton and T. J. Meyer, Inorg. Chem., 2008, 47, 1727.
72 I. Romero, M. Rodriguez, C. Sens, J. Mola, M. R. Kollipara,
L. Francas, E. Mas-Marza, L. Escriche and A. Llobet, Inorg.
Chem., 2008, 47, 1824.
73 A. Fujishima and K. Honda, Nature, 1972, 238, 37–38.
74 L. Schmidt-Mende, W. M. Campbell, Q. Wang, K. W. Jolley,
D. L. Officer, M. K. Nazeeruddin and M. Graetzel, Chem-
PhysChem, 2005, 6, 1253.
75 M. W. Kanan and D. G. Nocera, Science, 2008, 321, 1072.
76 F. A. Armstrong and S. P. J. Albracht, Philos. Trans. R. Soc.
London, Ser. A, 2005, 363, 937.
77 C. Tard, X. Liu, S. K. Ibrahim, M. Bruschi, L. De Gioia,
S. C. Davies, X. Yang, L.-S. Wang, G. Sawers and C. J. Pickett,
Nature, 2004, 433, 610.
78 S. J. Borg, T. Behrsing, S. P. Best, M. Razavet, X.-M. Liu and
C. J. Pickett, J. Am. Chem. Soc., 2004, 126, 16988.
79 E. Fujita, in The 2001 McGraw-Hill Yearbook of Science &
Technology, ed. M. D. Licker, McGraw-Hill Book Co, New York.
NY, pp. 71–74.
80 H. Arakawa, M. Aresta, J. N. Armor, M. A. Barteau,
E. J. Beckman, A. T. Bell, J. E. Bercaw, C. Creutz, E. Dinjus,
D. A. Dixon, K. Domen, D. L. Dubois, J. Eckert, E. Fujita,
D. H. Gibson, W. A. Goddard, D. W. Goodman, J. Keller,
G. J. Kubas, H. H. Kung, J. E. Lyons, L. E. Manzer,
T. J. Marks, K. Morokuma, K. M. Nicholas, R. Periana,
L. Que, J. Rostrup-Nielson, W. M. H. Sachtler, L. D. Schmidt,
A. Sen, G. A. Somorjai, P. C. Stair, B. R. Stults and W. Tumas,
Chem. Rev., 2001, 101, 953–996.
81 N. S. Lewis, Chemical Challenge in Renewable Energy, Lecture
2005, text on http://www.cce.caltech.edu:16080/faculty/lewis/
research.htm.
82 M. I. Hoffert, K. Caldeira, G. Benford, D. R. Criswell, C. Green,
H. Herzog, A. K. Jain, H. S. Kheshgi, K. S. Lackner, J. S. Lewis,
H. D. Lightfoot, W. Manheimer, J. C. Mankins, M. E. Mauel,
L. J. Perkins, M. E. Schlesinger, T. Volk and T. M. L. Wigley,
Science, 2002, 298, 981.
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