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Birck Nanotechnology Center
10-2011
Biomimetic strategies for solar energy conversion: a
technical perspective
Ardemis A. Boghossian
Massachusetts Institute of Technology (MIT)
Moon-Ho Ham
Gwangju Institute of Science & Technology
Jong Hyun Choi
Birck Nanotechnology Center, Purdue University, [email protected]
Michael S. Strano
Massachusetts Institute of Technology (MIT)
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Boghossian, Ardemis A.; Ham, Moon-Ho; Choi, Jong Hyun; and Strano, Michael S., "Biomimetic strategies for solar energy
conversion: a technical perspective" (2011). Birck and NCN Publications. Paper 940.
http://dx.doi.org/10.1039/c1ee01363g
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PERSPECTIVE
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Biomimetic strategies for solar energy conversion: a technical perspective
Published on 22 August 2011. Downloaded by Purdue University on 18/07/2013 21:34:39.
Ardemis A. Boghossian,†a Moon-Ho Ham,†b Jong Hyun Choic and Michael S. Strano*a
Received 28th March 2011, Accepted 7th July 2011
DOI: 10.1039/c1ee01363g
Plants have evolved highly sophisticated light-harvesting mechanisms that allow for increased
environmental tolerances and robustness, enhanced photo-efficiencies and prolonged lifetimes. These
mechanisms incorporate the dynamic, cyclic self-assembly of proteins necessary for continual plant
regeneration. Synthetic solar conversion devices, on the other hand, are designed to be static devices.
Material and processing costs continue to be important constraints for commercial devices, and the
earth abundance of requisite elements have become a recent concern. One potential solution to these
problems lies in the development of biomimetic solar conversion devices that take advantage of the low
material costs, negative carbon footprint, material abundance and dynamic self-assembly capabilities
of photosynthetic proteins. Although research in this area is ongoing, this review is intended to give
a brief overview of current biomimetic strategies incorporated into light-harvesting and energyconversion mechanisms of synthetic solar devices, as well as self-repair and regeneration mechanisms
adapted from plant-based processes.
Introduction
a
Department of Chemical Engineering, Massachusetts Institute of
Technology, Cambridge, Massachusetts, 02139, USA. E-mail: strano@
mit.edu
b
School of Materials Science and Engineering, Gwangju Institute of Science
and Technology, Gwangju, 500-712, Republic of Korea
c
School of Mechanical Engineering, Purdue University, Birck
Nanotechnology Center, Bindley Bioscience Center, West Lafayette,
Indiana, 47907, USA
† These authors contributed equally
Ardemis Boghossian received
her B.S. degree in Chemical
Engineering from the University of Michigan – Ann Arbor
in 2007. She is currently
a graduate student in the
Chemical Engineering Department at the Massachusetts
Institute of Technology (MIT),
working under the supervision
of Professor Michael S.
Strano. The focus of her
research includes the study of
Ardemis A: Boghossian
dynamic, self-repair mechanisms and the development of
biomimetic devices demonstrating regenerative properties, with a focus on solar energy
applications.
3834 | Energy Environ. Sci., 2011, 4, 3834–3843
To become widespread for energy generation, solar cells must
satisfy four essential criteria: efficiency, stability, cost effectiveness, and material availability. Although several solar cells
to date meet, or even exceed, several of these criteria, the
existence of a device that meets all these criteria remains an
objective for scientific research. Mono-crystalline silicon-based
solar cells,1–4 for instance, demonstrate efficiencies approaching
the Shockley-Queisser limits of 33.7%5 with stabilities on the
order of decades.6 The abundance in material availability,
Dr. Moon-Ho Ham is currently
an assistant professor in Materials Science and Engineering at
Gwangju Institute of Science
and Technology in South Korea.
He received his B.S. and Ph.D.
degrees in Materials Science
and Engineering at Yonsei
University. He was a postdoctoral associate in Chemical
Engineering at Massachusetts
Institute of Technology under
the supervision of Professor
Moon-Ho Ham
Michael S. Strano. His research
focuses
on
nanomaterials
including semiconductor nanowires, carbon nanotubes and graphene for nanoelectronic and solar
energy applications.
This journal is ª The Royal Society of Chemistry 2011
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however, is offset by the relatively high processing costs affiliated
with silicon purification.2,7 Thin-film technologies,8–13 which offer
low-cost alternatives to silicon-based energy devices, tend to
suffer from lack of material abundance14 and lower device
efficiencies.15–17
Ongoing research in this area focuses on not only improving
existing technologies by lowering processing costs,18–22 replacing
scarce, high-cost, or unstable materials23–26 and enhancing
device efficiencies,27–29 but also developing devices that are
entirely new to the field by utilizing new materials27,30,31 or
alternative mechanisms27,32,33 for solar energy conversion.
Among the most promising of these candidates is the dyesensitized solar cell (DSSC),34,35 which incorporates a Ru-based
dye reminiscent of natural dyes found in the chlorophyll of
plants. Like several solar cells that seek to minimize processing
costs via self-assembling mechanisms,36,37 DSSCs rely on selfassembly of the Ru dye for solar cell fabrication.38–41 Though
demonstrating promising efficiencies of up to 11%,42,43 limitations in Ru availability14 and the replacement of unstable,
liquid-based electrolytic cells26,44–47 are the focus of ongoing
research in this field.
This brief overview in solar cell technology outlines key
transitions recurring in research developments: the transition
from the inorganic to the organic realm,27,48,49 from rigid and
static to thin, flexible, dynamic technologies,50,51 from high-cost,
high efficiency to low-cost, low efficiency devices.7,52 These
transitions parallel the underlying tendency of the field towards
the utilization of biomimetic strategies for solar energy
conversion.
In this review, we discuss in detail solar energy conversion in
plants, reviewing plant physiology and discussing several key
processes that occur during photosynthesis. We next provide
a non-exhaustive, general overview of solar cell technologies that
exploit biomimetic means of energy conversion to overcome
deficiencies that currently plague leading devices in the solar
technology field.
Jong Hyun Choi is currently an
assistant professor in Mechanical Engineering at Purdue
University. He received his B.S.
and M.S. degrees in Mechanical
Engineering
from
Yonsei
University in South Korea, and
earned his doctoral degree, also
in Mechanical Engineering, in
2005 from the University of
California at Berkeley. His
main research interests are in
nanomaterial interactions with
Jong Hyun Choi
radiative and molecular environments,
and
the
use
of observed phenomena for
various applications including bioengineering and energy conversion.
This journal is ª The Royal Society of Chemistry 2011
Plant physiology
In plants, the smallest unit of comprehensive energy conversion
is the plant chloroplast (Fig. 1). The chloroplast converts solar
photons into usable chemical energy via photosynthesis with an
overall synthesis balance
hn
6CO2 þ 6H2 O ƒƒƒƒƒ! C6 H12 O6 þ 6O2
Like most organelles in the plant cell, chloroplasts are surrounded by outer and inner membranes. The inner membrane
contains stacks of photoactive thylakoid membranes, or grana,
surrounded by stroma fluid. Stroma lamellae serve to connect the
multiple grana throughout the chloroplast. The stacks of thylakoid membranes that compose the grana are embedded with
multiple protein complexes, including photosystem II (PSII),
cytrochrome b (cyt b6f), photosystem I (PSI) and ATP synthase
Each of the photosystems, PSII and PSI, is surrounded by lightabsorbing antennas. The first stage of photosysnthesis, or the
light-dependent reactions, occurs within these protein complexes
within the thylakoid membrane.53–56
The series of light-dependent reactions are initiated in PSII,
where light is initially absorbed by the P680 site to generate
electron-hole pairs, with an overall half reaction of
hn
2H2 O ƒƒƒƒƒ! O2 þ 4e þ 4H þ
In addition to P680 absorption, light is also absorbed at
various wavelengths by the pigments within the surrounding
antenna. Electron excitation within the pigment is followed by
resonance energy transfer to the P680 site, where electron-hole
pairs are generated (Fig. 2a). The hole remains at the site, where
it is used in the oxidation reaction of water to produce oxygen via
oxygen-evolving complexes (OECs). Meanwhile, the electron is
initially transferred to the pheophytin (Phe) and QA sites,
resulting in the reduction of QA. The potential difference between
Professor Michael S. Strano is
currently the Charles and Hilda
Roddey Associate Professor in
the
Chemical
Engineering
Department at the Massachusetts Institute of Technology.
His research focuses on biomolecule/nanoparticle interactions
and the surface chemistry of low
dimensional systems, nano-electronics, nanoparticle separations, and applications of
vibrational spectroscopy to
Michael S: Strano
nanotechnology. He received his
B.S from Polytechnic University
in Brooklyn, NY and Ph.D.
from the University of Delaware both in Chemical Engineering. He
was a postdoctoral research fellow from 2001 to 2003 at Rice
University in the departments of Chemistry and Physics under the
guidance of Nobel Laureate Richard E. Smalley.
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Fig. 1 Chloroplast Structure. The chloroplast (left) consists of an outer membrane surrounding stacks of photoactive membranes, or granum. The
thylakoid membrane contained within each of these stacks (right) is embedded with several protein complexes, including PSII, cyt b6f, PSI, and ATP
synthase. Initial electron-hole separation occurs largely within PSII, with subsequent electron transport via successive redox reactions occurring in the
following complexes. Synthesis of ATP, the end product of the reaction scheme, occurs within the ATP synthase of the membrane.
the reduced QA site and the oxidized QB site drives electron
transport towards QB. Upon reduction of QB, an electron
transport chain is used to extract the electron from the QB site to
create a proton gradient across the thylakoid membrane using
cyt b6f. (This proton gradient aides in ATP synthesis via ATP
synthase, as described below). Like PSII, the following protein
complex, PSI, is responsible for photon absorption at the P700
site (Fig. 2b). Similarly, surrounding antennae also absorb light
at various wavelengths, transferring energy to P700 through
resonance transfer. Electrons gained from PSI are raised in
energy via the photoelectric effect, expelling the excited electron
to the ferredoxin site. From here, the electron may follow one of
two possible pathways: cyclic or noncyclic phosphorylation.
Under conditions where the plant produces excess NADPH
relative to ATP, the cyclic phosporylation reaction takes place,
where the electron is used to pump H+ across the membrane to
create a proton concentration gradient that is ultimately used to
power ATP synthase. Under conditions where NADPH
concentration is less sufficient, the electron enters a noncyclic
phosphorylation reaction which ultimately reduces NADP+ to
NADPH in the stroma according to the reaction
NADPþ þ 2H þ þ 2e ƒƒƒƒƒ! NADPH þ H þ
The final major protein complex, ATP synthase, extracts
charged hydrogen atoms from previous oxidation reactions, such
as water oxidization in PSII, to ultimately store energy in the
form of the ATP with the addition of a phosphate group, Pi
ADP + Pi / ATP
The energy released as protons are pumped from the interior
of the thylakoid membrane to the stroma is used to carry out this
reaction. Overall, the net yield of the first stage of photosynthesis
becomes56–58
hv
2H2 O þ 2NADPþ þ 3ADP þ 3Pi ƒƒƒƒƒ! O2 þ 2NADPH
þ3ATP þ 2H þ
The second stage of photosynthesis, or the light-independent
reactions, occurs within the stroma of the chloroplast
Fig. 2 PSII and PSI Structure. (a) Photon absorption at the P680 site in PSII results in electron-hole separation. The hole is used in the oxidization of
water to produce oxygen, whereas the electron is driven to the Phe and QA sites of the complex. The potential difference between the quinone sites drives
electron transport to the QB site, where it is subsequently removed to enter the electron transport chain in cyt b6f. Except for the QA site, which is located
on the D2 protein, the remaining sites (P680, Phe, QB), are located on the D1 protein, which is susceptible to damage with a high turnover rate. (b)
Photon absorption at the P700 site in PSI results in electron excitation and expulsion. Subsequent electron extraction to the ferredoxin site occurs,
leaving the P700 in the oxidized state. The electron in the ferredoxin site is then used to ultimately reduce NADP+ to NADPH. The surrounding antenna
allow for increased absorption of light at wavelengths throughout the solar spectrum. Resonance transfer from the surrounding antenna to P700 is
similar to that demonstrated by PSII.
3836 | Energy Environ. Sci., 2011, 4, 3834–3843
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surrounding the grana. In these reactions, carbon dioxide and
water are converted into glucose according to the Calvin-Benson
cycle that occurs within the chloroplast, and the net yield of this
subset of reactions becomes59
6CO2 + 12NADPH + 12H+ + 18ATP / C6H12O6 + 6H2O +
12NADP+ + 18ADP + 18Pi
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Chloroplast generation and repair machinery
In addition to carrying out the carbon-fixation processes in the
form of the Calvin-Benson cycle, the stroma of the chloroplast
also contains genetic material needed to reproduce itself and
synthesize necessary proteins, along with the necessary
machinery to continually repair photodamaged proteins that
accumulate during the first stage of photosynthesis.60 The D1
protein in particular, which contains the P680 site required for
light absorption, and the Phe and QB sites required for electron
separation, demonstrates the highest turnover rate.61 The selfrepair cycle associated with photosynthesis is an evolutionary
adaptation allowing plants and photosynthetic organisms a wide
range of adaptability.60 These self-repair processes enable plants,
for examples, to not only adapt in a manner that minimizes
damage, but also fully recover from a state of excessive protein
denaturation. Without these self-repair processes, plants would
produce less than 5% of their typical photosynthetic yields60 with
lifetimes on the order of minutes under intense illumination.62
Upon continuous illumination, the D1 protein in PSII
becomes photo-damaged, resulting in the total photo-inactivation of the protein complex. Upon photo-inactivation, PSII
partially disassembles to release the damaged protein. The
damaged D1 protein is replaced with a newly biosynthesized D1
protein and PSII spontaneously re-assembles, incorporating the
new protein to create a fully functional PSII (Fig. 3). In the
meantime, the damaged D1 protein undergoes protease
degradation.63
Under non-saturating light conditions, this D1 degradation
and synthesis occurs at the same rate as D1 protein damage,
which is determined by light intensity, among other factors.
Thus, the D1 turnover rate increases with increasing light
intensity. However, under excessive light intensities, the damage
rate is too large for the repair rate to match, resulting in the
overall inhibition in PSII activity. When stressed plant cells are
returned to moderate, non-saturating conditions, they recover
their photosynthetic activity via replacement of the photodamaged D1 protein.64–67 However, after prolonged stress
conditions, the cells reach an inactive, irreversible state from
which there is no recovery,62 which is in part due to damage to the
transcriptional and translational machinery used to synthesize
D1 proteins, as well as other proteins involved in the cell cycle.
Although the exact nature of the cause behind PSII photodamage and repair are still under investigation, several key
players in the process have been identified. For instance, it is
known that toxic oxygen radicals are produced under excessive
light intensities.68 These radicals are not only responsible for
protein cleavage and denaturation, but also for bleaching lightharvesting antennas that surround the photosystem and for
general damage to the gene expression machinery used to
synthesize new proteins. It is hypothesized that the production of
the above reactive species is limited when cells are exposed to
saturating light conditions for only limited periods of time, since
the cells initially demonstrate virtually no decrease in photoactivity. This limitation may be due to the inherent presence of
scavengers such as xanthophylls, carotenes, and specific enzymes
that work to deactivate the oxygen radicals, until they are no
longer sufficient to buffer against prolonged exposure to saturating light intensities.62 Further evidence also suggests that
radical occupancy of the QB site of the D1 protein is specifically
linked to photo-inhibition sensitivity69,70 and that it is the first
target of high light stress.71,72 The D1 protein, which contains an
abundance of proline, glutamine, serine, and threonine, is
hypothesized to undergo cleavage at the Arg-238 or Phe-239 site
upon photodamage.73 Degradation at QB would account for the
Fig. 3 Self-Repair and Regeneration of D1 Protein in PSII. The self-repair process in plants is driven by the molecular recognition of parts as the system
transitions through a series of metastable states. Upon photodamage (right), the photo-inactivated D1 protein becomes denatured, triggering the partial
disassembly of the PSII complex (bottom). The damaged D1 protein diffuses towards the outer regions of the membrane scaffold for degradation in
exchange with a newly synthesized D1 protein that diffuses towards the disassembled complex. Introduction of the new D1 protein triggers the
spontaneous re-assembly of the complex (left) to create a functional, light-harvesting PS II (top).
This journal is ª The Royal Society of Chemistry 2011
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decrease in the electron transport from the QA to the QB site
observed upon photo-inactivation, where QA remains in the
reduced state.
Not only does the exact cause of photo-damage remain
unclear, but also the precise mechanism by which the plant
initiates protein degradation and synthesis is elusive.64 It has
been suggested that phosphorylation may play an active role in
regulating D1 degradation and synthesis.74 The steady-state level
of D1 phosphorylation increases with increasing D1 protein
photodamage,75 and degradation of the phosphorylated form of
the protein is reduced.76 Several studies have examined protein
self-assembly by artificially inducing phosphorylation66,67 at
decreased temperatures and monitoring re-assembly at elevated
temperatures. However, nothing is known about the D1 protein
phosphorylation when PSII is under repair and new photosynthetic reaction centers (RCs) have been formed.65 Regardless of
the details of the molecular mechanism, one fact remains certain:
for plant regeneration, both D1 protein degradation and
synthesis must occur at a rate sufficient to match that of protein
damage.
Biomimetic solar energy conversion devices
Although plants have evolved highly sophisticated, dynamic
mechanisms that allow them to replace photo-damaged proteins
to prolong lifetime and enhance efficiencies, as well as structures
that seek to optimize light absorption, man-made energy devices
lack this capability of dynamic assembly, repair and possible selfreplication. Several studies have made progress towards applying
energy conversion and self-repair processes used by plants to
synthetic devices.77–85
Artificial photosynthesis via water-splitting catalysis
As discussed, photosynthesis ultimately results in the formation
of an electron-hole pair upon absorption of sunlight. The electron is captured and shuttled to PSI, whereas the hole is used by
the OEC for the oxidation of water, resulting in the formation of
hydrogen. In an effort to duplicate photosynthesis, researchers
have sought the creation of a device capable of electron-hole
separation upon light absorption where the hole is used in water
oxidation such that solar energy is stored chemically in the bond
formation of H2 and O2. For decades, researchers have focused
on mimicking the OEC near PSII by creating catalysts capable of
converting water, carbon dioxide and light into carbohydrates,
releasing hydrogen as a source of fuel.79 A synthetic, non-protein
based form of catalysis that can oxidize water as efficiently as the
OEC is the ruthenium ‘‘blue dimer’’, which requires activation via
a strong oxidizing agent (Fig. 4a).86,87
Ruthenium
0
bluedimer0
4CeðIV Þ þ 2H2 O ƒƒƒƒƒƒƒƒƒ! 4CeðIIIÞ þ O2 þ 4H þ
However, unlike the OEC, this catalyst can only catalyze the
reaction for a limited number of cycles prior to demonstrating
decreasing efficiencies due to the generation of reactive catalytic
intermediates. A tetra-ruthenium-based catalyst developed by
K€
orgerler, Botar and co-workers82 is able to catalyze water
oxidation with enhanced stabilities. The next generation of
3838 | Energy Environ. Sci., 2011, 4, 3834–3843
Fig. 4 Key Contributions in Artificial Photosynthesis. (a) The ruthenium ‘‘blue dimer’’ catalyzes the oxidation of water into oxygen
and hydrogen with efficiencies approaching those of the OEC. (Ref. 119
Reproduced by permission of The Royal Society of Chemistry).119–121 (b)
Iridium-based catalyst demonstrates larger turnover frequencies for the
catalysis of the oxidation of water. (Reprinted with permission from
ref. 88. Copyright 2008 American Chemical Society).88
catalysts, which utilize an iridium-based complex, also requires
a strong oxidizing agent (Fig. 4b). These catalysts maintain
efficiencies on the order of 66% well over 2000 cycles.88 Though
they are the first non-ruthenium-based catalyst for photochemical water oxidation with a known structure, unfortunately, they
rely on the utilization of costly iridium.
In an alternative approach to address issues of stability, efficiency and cost of water splitting catalysis, Nocera and coworkers89 developed a homogenous rhodium-based catalyst with
efficiencies less than those demonstrated by plants naturally. The
most recent developments from the group have led to the
synthesis of a biomimetic, Co-based catalyst capable of performing under ambient conditions (pH 7, 1 atm, 25 C) using
earth-abundant elements in an aqueous solution.90 To address
issues of instability, this catalyst is capable of utilizing biomimetic mechanisms of self-repair wherein the different oxidative
states occupied by Co during a catalytic reaction demonstrate
varying degrees of solubility and reactivity. The suitable choice
of an appropriate anion in solution can counter increased
dissolution of the appropriately oxidized Co by establishing
equilibrium in solution.
Coupling artificial photosynthesis with hydrogenases
An extension of the bio-inspired systems for hydrogen production interfaces natural photosystems for hydrogen production
with synthetic hydrogenases.80 Like plants, cyanobacteria and
green algae synthesize glycogen and starches from CO2 when
under illumination. Under anaerobic conditions, hydrogenases
catalyze the recombination of hydrogen ions with electrons to
produce hydrogen gas according to the reaction
2H+ + 2e /H2
To couple the water-splitting reactions during photosynthesis
with hydrogenases that remain active under aerobic conditions,
a synthetic PSI-hydrogenase hybrid was assembled onto a gold
electrode using a genetically engineered, cyanobacteria-derived
PSI and a soil bacterium-derived hydrogenase. Light-activated
hydrogen production in these biomimetic devices occurs at
higher potential and lower energies than synthetic (bio)nanoelectronic devices that did not implement a photosynthetic
apparatus. Although the high costs affiliated with protein isolation make future prospects of PS-based hybrid systems infeasible
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for solving the global energy crisis, cellular-based systems still
hold promise in this field.91 In this sense, the future of this field
will tend towards devices consisting of photosynthetic organisms
and mechanisms, rather than just protein complexes. In fact,
several recent studies have taken steps in this direction with the
development of nanoprobes capable of direct electron extraction
from intact algal cells.92 Some studies have even advocated for
the development of biofuel cells that utilize algal cells,93 as well as
living plants and bacteria.94
Biomimetic systems utilizing plant-derived photosystems
Conventional technology cannot equal the molecular circuitry
found in photosynthetic complexes.95 PSI, for example, which
has yet to be synthesized synthetically, has external quantum
efficiencies of approximately 100% and energy yields of 58%.96
Several studies have focused on the assembly of monolayers of
PSI onto various substrates, including Au. One such study
examined the adsorption of PSI extracted from commercial
spinach leaves onto gold surfaces coated with various amine
groups.97 Based on the result of these studies, PSI adsorption was
conducted onto a hydroxyl-coated Au electrode surface.81 To fill
in the electrode-exposed areas between the adsorbed PSIs, the
interstitial, shorter hydroxyl chains were replaced with longer
thiol chains, confining the protein layer between hydrocarbon
chains. This incorporation of the PSI amongst long, hydrocarbon chains closely resembles the natural environment in the
thylakoid membrane, thus stabilizing the PSI and conserving
secondary structure upon exposure to various solvents.
In addition to PSI assembly, monolayer assembly has also
been extended to RCs in photoelectrochemical cells.78 Immobilization of His-tagged RCs onto an electrode was demonstrated
using a nickel-nitrilotriacetic acid (NI-NTA) terminated
substrate. To enhance device efficiency, RC configuration was
altered to more closely mimick the native orientation of the
protein complex with cytochrome such that the primary donor is
facing the electrode surface. Photoelectrochemical measurements
were obtained with the immersion of the decorated electrode into
a ubiquinone-contained redox solution, as the redox potential of
ubiquinone closely matches that of the QB site for electron
extraction.
The effect of varying orientations of PSI monolayers was
studied by Greenbaum and co-workers.98 Au electrodes were
coated with negative, positive and hydrophilic surfaces and
incubated with spinach-extracted PSIs for adsorption. Depending on the hydrophobicity and charge of the electrode surface,
the PSI would orientate itself horizontally, upwards, or downwards, with I–V characteristics similar to semiconducting and
diode-like behaviors. Monodispersion of PSI onto chemically
treated Au surfaces allowed for the first single PSI photoelectric
measurements using Kelvin force probe microscopy (KFPM).99
Covalent attachment of spinach-derived PSI through imine
binding with lysine residues upon vacuum-assisted solution
evaporation was also used in device fabrication.100 Upon evaporation, the decreased solubility of PSI and selective precipitation out of solution was used to create highly dense layers on
a functionalized Au substrate. Using this fabrication, the PSI is
orientated such that its electron transfer vector is directed away
from the Au surface. Photoelectrochemical measurements reveal
This journal is ª The Royal Society of Chemistry 2011
that such dense monolayers of PSI yield enhanced photocurrents
of 100nA/cm2.
Alternative approaches for monolayer assembly have focused
on obtaining covalent attachment of PSI in specific orientations.
An approach to directly tether PSIs as a monolayer onto a gold
surface required genetic mutation at various cysteine sites in the
vicinity of P700.101 Since the PSIs were isolated from the cyanobacteria Synechocystis sp., they require no stabilizing agents,
since the antenna chlorophylls are integrated within the core
subunits of the photosystem rather than as a peripheral attachment as in plants (Fig. 1). Although the fundamental optoelectronic properties of PSI remain conserved upon attachment to
gold, attached PSI demonstrated an increase in spectral range
and a loss in photopotential.
Dry multilayers of PSI onto gold substrates were also achieved
to fabricate bio-inspired solid-state devices.102 As with the
monolayer devices developed by Carmeli and co-workers in
2005,101 genetically-altered, cysteine mutants were attached via
sulfide binding in the stacked configured shown in Fig. 5, with
binding events occurring on the Au substrate for the first
monolayer, and on sequentially depositing Pt for the subsequent
layers. Such high-density devices resulted in enhanced absorption
and increased device efficiencies.
A more direct attempt at reconstructing leaf-like structures
using PSI was obtained using similar lysine-binding chemistries
onto a nanoporous gold leaf (NPGL), wherein PSI was immobilized onto structured, rather than planar, electrodes for
increased surface area.84 Greater control in layer assembling
mechanisms was shown to enhance photoelectrochemical efficiency.103 This surface enhancement quadrupled photocurrents,
producing photocurrents of 400 nA/cm2.
Another attempt at enhancing surface area coverage of PSI
onto electrode surfaces was made using nanoparticle-PSI hybrid
systems.104 Gold nanoparticles were deposited onto a planar gold
electrode through sedimentation. Electrostatic deposition of
cyanobacteria-isolated PSI onto the negatively charged gold
nanoparticles to create a bio-nanohyrbid material with photoelectrochemical currents exceeding analogous planar-based
electrodes.
As opposed to non-covalent deposition, direct tethering of PSI
to a functionalized surface is another approach used by research
scientists to extract photoelectrical output.105 In one such study,
Au nanoparticles were decorated with artificial vitamin K1
tethers, and native vitamin K1 tethers were removed from
bacteria-extracted PSIs. Incubation of the modified PSI
complexes with the functionalized nanoparticles creates
synthetically tethered PSIs with direct electron extraction from
the quinine pocket. In a similar study, planar gold electrodes
were coated with electrostatically adsorbed, synthetic vitamin K1
wires.77 Incubation of the adsorbed wires with PSI where natural
vitamin K1 tethers have been removed covalently attaches the
photoactive protein complex to the Au electrode surface.
An extension of this work also resulted in a similar, direct
binding of PSI to carbon nanotubes106–108 and a tethered, indirect
binding to a GaAs substrate.109,110 To improve the efficiency,
Lebedev and co-workers used arrayed carbon nanotube electrodes.111 The RCs were encapsulated inside carbon nanotube
arrays and bound to the inner tube walls in a unidirectional
orientation using organic molecular linkers. The efficiency was
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Fig. 5 High-density Stacked Configuration for Enhanced Efficiencies. (a) Multilayers of genetically altered PSI covalently attached to a Au substrate
result in high-density arrays with enhanced absorption properties and increased efficiencies. (Reprinted with permission from ref. 102. Copyright 2005
Wiley).102 (b) Self-assembled device based on densely-packed, stacked PSII along a SWCNT substrate was proposed to enhance biomimetic device
efficiency.83
considerably improved by increasing the number of RCs
attached onto the electrode surface by about 5-fold compared to
that obtained with the same proteins when immobilized on
a planar graphite (HOPG) electrode. In an alterative study,
carbon nanotubes were covalently functionalized with diazonium salt to attach RCs, and the his-tagged RCs were reversibly
assembled to a single-walled carbon nanotube (SWCNT)-NTANi2+ complex.112
In contrast to liquid-based devices, photosystem-based solidstate versions were also explored in a research study by Baldo
and co-workers wherein both PSI- and RC-based devices with
12% internal quantum efficiencies were developed.113 These
photosynthetically-derived proteins were immobilized onto
a gold-coated ITO substrate using NTA functionalized surfaces
with His-tagged protein subunits. Self-assembly of the PSI onto
the functionalized surface relies on the exchange of an intrinsic
subunit from the PSI complexes with an immobilized, functionalized subunit. Such replacement is similar to the exchange
process used by plants to naturally replace photodamaged
subunits. To stabilize the immobilized protein in the solid-state
device, peptide surfactants and amorphous organic semiconducting layers were deposited during device fabrication.
These thin films impart the device with not only protein stability,
but also ‘‘solid-state antennae’’ reminiscent of light-harvesting
antennae used to enhance optical absorption in natural systems.
Such studies85,101,106 often rely on the labor-intensive isolation of
PSI and mutation of specific subunits in order to achieve densely
packed layers with increased efficiencies.
The most recent development in photosystem-based solar
energy devices not only incorporates intact RCs, but also utilizes
the self-repair mechanism used by plants in D1 synthesis and
degradation to develop the first photoelectrochemical cell
capable of biomimetic regeneration.83 In our recent study, an
aqueous solution containing RCs, carbon nanotubes, lipid, and
surfactant is dialyzed to selectively remove surfactant. The
remaining components spontaneously self-assemble into a photoactive complex where lipid bilayer disks align along the length
of a nanotube, each housing an individual RC. The RC orientation within the lipid bilayer is reminiscent of that within
naturally occurring thylakoid membranes: the hydrophobic
regions of the RC are buried within the hydrophobic chains of
the bilayer and the hydrophilic ends are pointed towards the
3840 | Energy Environ. Sci., 2011, 4, 3834–3843
aqueous solution. The self-assembly of this complex is
completely reversible in that the re-addition of surfactant to the
system spontaneously disassembles the complex into its initial
micellar state. Hence, the cyclic assembly and disassembly of the
photoactive complex is driven by the molecular recognition of
parts, kinetic trapping of metastable thermodynamic states, and
chemical signaling to switch between the assembled and disassembled states; the key components involved in the plant selfrepair cycle. Photoelectrochemical measurements of the assembled complex realized a 40% per complex external quantum
efficiency based on the produced photocurrent. Overall cell efficiency, which is strongly dependent on complex concentration,
was increased by over 300% by utilizing a regeneration cycle
incorporating the cyclic disassembly and re-assembly of the
complex upon protein photodamage using the cell design shown
in Fig. 6. As the light is irradiated, the photocurrent appears in
the assembled state and decreases over time upon photodamage.
When the photocurrent reaches about 25% of the initial value,
the sodium cholate surfactant is introduced to break apart the
complexes and remove the photodamaged components using the
second dialyzer while maintaining the nanotube scaffold. The
complexes are subsequently re-formed with new components by
removing the surfactant using the first dialyzer, resulting in the
recovery of the photocurrent to the previous maximum. This is
the first demonstration of a synthetic photoelectrochemical
complex mimicking the self-repair process used by plants, which
is shown in Fig. 3. As with the previously discussed studies,102
enhanced device efficiencies are expected for high-density,
stacked arrangements (Fig. 5).
Bio-inspired light-harvesting antennas for enhanced efficiencies
As discussed above, enhancing biomimetic photoelectrical efficiency remains an active area of research. In addition to maximizing surface area exposure84,104 and synthesizing high-density
arrays,83,102 researchers have also developed enhanced lightabsorption antennas that mimick the light-harvesting antennas
used by both PSI and PSII.114–117 These antennas absorb light at
a broader range of wavelengths. The energy absorbed by the
antenna complexes is directed to the RCs which absorb photons
at a specific wavelength, where the electron-hole pairs are
generated using the absorbed energy, and the electrons are
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Fig. 6 Biomimetic Regeneration for Cell Efficiency Enhancement. (a) A solution consisting of RC-lipid bilayer-nanotube complexes and a dual
mediator system comprised ferrocyanide/ferricyanide and ubiquinone/ubiquinol redox couples is illuminated at 785 nm. Photoresponse is measured
using a SWCNT working electrode and a Pt counter-electrode. Surfactant removal is used for complex assembly (left dialyzer), and surfactant addition is
used for complex disassembly (right dialyzer). (b) Photocurrent is measured under continuous illumination as photoresponse decreases over time. When
approximately 25% of the initial photoactivity is achieved, surfactant is introduced into the system to initiate complex disassembly. The photodamaged
proteins are replaced, and surfactant is once more removed from the system to re-assemble the complex, incorporating the photoactive proteins. This
regeneration cycle is applied over 168 h, increasing overall cell efficiency by over 300% relative to efficiencies demonstrated in the absence of regeneration. (Reprinted with permission from ref. 83. Copyright 2010 Nature Publishing Group).83
Fig. 7 Nanotube-based Exciton Antenna. (a) An optical image of core-shell antenna (left, scale bar 2 mm) and a corresponding schematic (right). (b) A
cross-sectional view of the antenna illustrates an outer layer consisting of larger bandgap, (6,5) nanotubes and an inner core consisting of smaller
bandgap nanotubes. Light is absorbed by the outer shell tubes. This energy is transferred to the inner core tubes via electron energy transfer (EET), as
indicated by the black arrows. (Reprinted with permission from ref. 118. Copyright 2010 Nature Publishing Group).118
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transferred to electron acceptors. In another recent report from
our group,118 carbon nanotubes were used to synthesize multishell, one-dimensional optical antennas with different bandgap
energies which consist of smaller bandgap nanotubes inside and
(6,5) nanotubes outside (Fig. 7). This core-shell nanofiber funnels
excitation to the photon energy of the smallest bandgap nanotubes in the core of the antenna, which is analogous to energy
transfer mechanisms from antenna complexes surrounding PSI
and PSII.
Conclusions and outlook
As it stands, the high costs affiliated with protein isolation and
purification undermines the development of a low-cost, biobased solar conversion device for both hydrogen generation91
and photoelectrochemical/photovoltaic applications. These high
costs are partially offset by advancements that boost solar
conversion efficiencies, whether it be via textured surfaces that
resemble leaf-life porosity in plants,84,104 stacked arrays with
densities that approach that of the stacked grana in chloroplasts,83,102 regeneration cycles that rival the self-repair mechanisms used by plants,83 or solar concentrators that funnel energy
to photoactive complexes analogous to light-harvesting antennae
found in plants.118 Regardless of the device (water-splitting,
photovoltaic, etc.), and regardless of the approach used to
enhance device efficiency, the solution scientists converge to is
consistently something already addressed in nature. As
researchers continue to venture out of the realm of rigid, inorganic, pricey photovoltaics and into the realm of thin, flexible,
organic, quasi-fluidic devices, one thing remains certain; the
tendency towards biomimetic devices is a recurring theme in this
field that will continue to sculpt the fabrication of solar cells for
the future.
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