LETTERS
Self-regulation of photoinduced electron
transfer by a molecular nonlinear transducer
STEPHEN D. STRAIGHT, GERDENIS KODIS, YUICHI TERAZONO, MICHAEL HAMBOURGER,
THOMAS A. MOORE*, ANA L. MOORE* AND DEVENS GUST*
Department of Chemistry and Biochemistry, Center for Bioenergy and Photosynthesis, Arizona State University, Tempe, Arizona 85287, USA
*e-mail: [email protected]; [email protected]
Published online: 4 May 2008; doi:10.1038/nnano.2008.97
Organisms must adapt to survive, necessitating regulation of
molecular
and
subcellular
processes.
Green
plant
photosynthesis responds to potentially damaging light levels
by downregulating the fraction of excitation energy that drives
electron transfer. Achieving adaptive, self-regulating behaviour
in synthetic molecules is a critical challenge that must be met
if the promises of nanotechnology are to be realized1. Here we
report a molecular pentad consisting of two light-gathering
antennas, a porphyrin electron donor, a fullerene electron
acceptor and a photochromic control moiety. At low whitelight levels, the molecule undergoes photoinduced electron
transfer with a quantum yield of 82%. As the light intensity
increases, photoisomerization of the photochrome leads to
quenching of the porphyrin excited state, reducing the
quantum yield to as low as 27%. This self-regulating molecule
modifies its function according to the level of environmental
light,
mimicking
the
non-photochemical
quenching
mechanism2–8 for photoprotection found in plants.
Organisms exist in non-equilibrium states by using complex
regulatory systems that adjust metabolic responses to stimuli.
Because photosynthetic conversion of solar energy to chemical
potential energy is optimized for the ambient light level, an
increase in light flux can overdrive photosynthesis and cause the
buildup of toxic intermediates that destroy cellular components.
In plants, a vital regulatory mechanism—non-photochemical
quenching (NPQ)—is controlled by the pH of the aqueous
lumen in the thylakoids, the membrane-bound compartments in
which the light-dependent reactions of photosynthesis occur.
Under high light levels the proton activity in the lumen increases,
triggering a complex series of events, centred around chemical
modification of a carotenoid polyene, which reduces the
percentage of absorbed photons whose excitation energy is
delivered to the reaction centre for photosynthetic work. The
NPQ results in nonlinear transduction of absorbed photon
energy into chemical potential energy.
The realization of analogous self-regulation in synthetic
molecular systems is an important but challenging step in the
development of molecular machines and devices. Molecular
pentad 1 (Fig. 1) is an adaptive, self-regulating artificial
antenna –reaction centre complex that operates in a manner
functionally analogous to NPQ. This molecule contains a
photochromic moiety that serves as the regulatory unit. We and
others have previously used photochrome molecular ‘switches’ to
change the fluorescence yield or other properties of attached
280
OCH3
BPEA
antenna
OCH3
Fullerene
acceptor
Porphyrin
donor
CH3
N
O
N
H
NH N
N HN
1c
DHI
HN
O
CH3O
BPEA
antenna
CH3O
N
NC
Photochrome
control moiety
Blue light
CN
Heat or
red light
HN
O
N
1o
CN
NC
BT
Figure 1 Structure of pentad 1. This molecule includes a porphyrin excited
state electron donor linked to a fullerene electron acceptor and two
bis(phenylethynyl)anthracene (BPEA) light-absorbing antennas. The pentad also
features a photochromic control moiety that can exist in two forms: a
dihydroindolizine (DHI), which has no effect upon the porphyrin photochemistry,
and a betaine (BT), which quenches the porphyrin excited singlet state.
Isomerization between these two forms is initiated by light or heat, as indicated.
chromophores, mostly in the context of molecular logic9–15. The
porphyrin and the two bis(phenylethynyl)anthracene (BPEA)
antennas absorb light, excitation energy migrates from the
antennas to the porphyrin, and photoinduced electron transfer
from the porphyrin first excited singlet state to the fullerene
generates a charge-separated state that preserves a large fraction
of the absorbed energy as electrochemical potential. When a
solution of 1 in 2-methyltetrahydrofuran is illuminated with low
levels of white light, the quantum yield of charge separation is
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LETTERS
1.5
0.018
0.02
ΔA
1.0
0.50
Amplitude (a.u.)
Absorbance
0.5
0.0
425
450
475
0.25
0.00
0.012
0 10
1,000 2,000 3,000
τ (ps)
0.006
0.00
300
400
500
600
Wavelength (nm)
700
500
Absorbance
550
600
650
Wavelength (nm)
700
750
Figure 3 Femtosecond transient absorption. Decay-associated spectra of
pentad 1c in 2-methyltetrahydrofuran following excitation with a 300-fs
light pulse at 480 nm. The time constants associated with the three
spectra are 4.0 ps (open squares), 2.0 ns (open circles) and non-decaying
on this timescale (filled diamonds). The inset shows absorbance
change (DA) at 660 nm (filled squares) and at 700 nm (filled circles)
versus time (t ).
0.6
0.4
0.2
0.0
300
0.000
800
400
500
600
Wavelength (nm)
700
800
Figure 2 Steady-state absorption. a, Absorption spectra of the pentad in
2-methyltetrahydrofuran with the photochromic moiety in the closed
(1c, solid line) and open (1o, dashed line) forms. The inset shows the Soret
band and the BPEA absorption. b, Absorption spectra of a model DHI
photochromic moiety (compound 12, see Supplementary Information) in
the thermally stable, closed DHI form (solid line) and the open betaine (BT)
form (dotted line).
82%. Increasing the illumination level leads to a reduction of the
quantum yield to values as low as 27%, and subsequently
decreasing the illumination intensity returns the quantum yield
to its initial value.
This markedly nonlinear transduction of light energy to
electrochemical potential is due to the quinoline-derived
dihydroindolizine (DHI) photochrome attached to the
hexaphenylbenzene moiety. The closed, spiro form of the
photochrome (DHI, structure 1c), is thermodynamically more
stable. Thermal isomerization at ambient temperatures and
photoisomerization by red light both favour this form of the
molecule. The DHI has no effect upon the photophysics of the
remainder of the molecule. The open betaine isomer (BT,
structure 1o), generated by photoisomerization of 1c resulting
from absorption in the ultraviolet (UV) to blue-green portions of
the spectrum, strongly quenches the porphyrin excited singlet
state, thereby reducing the quantum yield of photoinduced
electron transfer. Increasing the white-light flux changes the
isomer distribution in the pentad, increasing the fraction of
molecules present in the less thermally stable BT form, leading to
the observed reduction in the quantum yield of charge separation.
Pentad 1 was prepared by synthesis of a substituted
hexaphenylbenzene, construction of the porphyrin on this core16,
attachment of the two BPEA antennas17, linkage of the
photochrome18 to the hexaphenylbenzene, and finally coupling to
the fullerene through an amide linkage. (See Supplementary
Information for details of the synthesis and spectroscopic
procedures.) The absorption spectrum of 1c, which has the
photochrome in the DHI form, features bands due to the
porphyrin at 424, 519, 556, 593 and 650 nm, the BPEA at 450
(sh) and 474 nm, and the DHI at 395 nm, overlapping the
porphyrin Soret band (Fig. 2a). The DHI absorption extends to
475 nm, as can be seen more readily in Fig. 2b, which shows
the absorption spectra of a model photochrome. Irradiation with
UV light photoisomerizes 1c to 1o, in which the photochrome is
now in the open BT form with absorption maxima at 485 and
685 nm (Fig. 2a,b). Isomer 1o thermally reverts to 1c with a time
constant of 37 s at 25 8C, and irradiation of 1o with red light
into the 685-nm absorption band photoisomerizes it to 1c, albeit
with low quantum yield.
The photochemistry of 1 was investigated using a variety of
time-resolved techniques (see Supplementary Information).
Figure 3 shows decay-associated spectra obtained by the pumpprobe technique after exciting 1c into the BPEA absorption at
480 nm with a 300-fs laser pulse. The shortest of the three
lifetime components, 4 ps, corresponds to decay of the BPEA first
excited singlet state by singlet energy transfer to the porphyrin.
Based on the first excited singlet state lifetime of a model BPEA
antenna (2.80 ns)17, the quantum yield of energy transfer to the
porphyrin is 1.0, and BPEA thus serves as an effective antenna
for the porphyrin. The porphyrin first excited singlet state decays
in part by the usual photophysical processes of intersystem
crossing, internal conversion and fluorescence, the time constant
for these processes (reciprocal of the sum of the rate constants)
being 11.4 ns. Figure 3 shows that in the pentad, the porphyrin
excited state decays with a time constant of 2.0 ns due to the
influence of an additional process: photoinduced electron
transfer to the fullerene to generate a charge-separated state
(quantum yield F ¼ 0.82). The charge-separated state does not
decay on the timescale of Fig. 3, but measurement on the
nanosecond timescale gives a lifetime of 14.0 ns (see
Supplementary Information).
The situation changes when 1c is converted to 1o by irradiation
with UV light. Time-resolved measurements on a solution highly
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281
282
1.0
1.0
0.8
0.8
0.6
0.6
0.4
0.4
0.2
0.2
Relative white light intensity ( )
0.0
0.0
0
2
4
6
8
10
Experiment number
12
0.8
Overall yield of charge separation
enriched in 1o revealed that the porphyrin first excited singlet state
lifetime is quenched to 33 ps by the BT form of the photochrome.
This strong quenching reduces the quantum yield of the charge
separated state to only 1%, effectively shutting off photoinduced
electron transfer. The transient spectral data for 1o and model
compounds are consistent with quenching by singlet energy
transfer from the porphyrin to BT (see Supplementary
Information). The lifetime of the resulting excited state of BT,
measured in model compounds, is only 0.9 ps. Quenching by
electron transfer from the porphyrin to BT is thermodynamically
allowed, but no evidence for the porphyrin radical cation was
noted in the transient spectra of model compounds, and the
large number of bonds in the covalent linkage between the
porphyrin and BT suggests that electron transfer, unlike energy
transfer, requires electronic orbital overlap, which would be slower.
The transient spectroscopic results demonstrate that pentad 1c
is an efficient artificial photosynthetic antenna –reaction centre
complex, converting light absorbed over much of the visible
region into electrochemical energy in the form of intramolecular
charge separation. In isomeric pentad 1o, however, photoinduced
electron transfer is prevented due to quenching of the porphyrin
excited singlet state by the betaine. These properties, coupled
with the fact that 1o and 1c may be readily interconverted by
photoisomerization or thermal effects, allow the pentad to
function as an adaptive, self-regulating molecular nonlinear
transducer. This behaviour is demonstrated in Fig. 4a. Along the
abscissa are plotted the results of experiments carried out on a
solution of the pentad in degassed 2-methyltetrahydrofuran. Each
point was obtained after 20 s of white light illumination of 1c at
relative intensities indicated by the open circles. The fluorescence
emission from the porphyrin, excited at 480 nm, was
immediately measured at each point, and the corresponding
quantum yield of charge separation was determined. This was
done by assuming that the fluorescence magnitude in the absence
of white light irradiation reflects pure 1c with a quantum yield
for photoinduced electron transfer of 82%, and using the fraction
of fluorescence quenching that results from white light
illumination (due to conversion to 1o) to calculate the quantum
yield of electron transfer under those conditions (solid circles).
Porphyrin excited state quenching by BT decreases porphyrin
fluorescence and photoinduced electron transfer proportionally.
The quantum yield of charge separation decreased smoothly as
the white light intensity increased, dropping from 82% at low
light levels to 37% at the highest levels of white light used in this
particular experiment. More intense white light further decreases
the quantum yield (see Supplementary Information). The squares
in Fig. 4b represent the overall relative yield of charge separation,
which was obtained by multiplying the quantum yield of
photoinduced electron transfer by the relative white light
intensity. The dashed line shows the calculated relative overall
yield in the absence of photoregulation, where the quantum yield
would be 0.82 at all light intensities.
In the spectral region where the BPEA antennas absorb, the
reduction in quantum yield for 1o at high light levels could in
principle be somewhat greater than that shown in Fig. 4 if the
BPEA excited singlet states are quenched by energy transfer to
BT. Such energy transfer would have to be extremely rapid, given
the already strong quenching of the BPEA singlets by energy
transfer to the porphyrin, but could not be ruled out in
our experiments.
In additional experiments, the variation in the yield of fullerene
radical anion as a function of white light irradiation was also
measured directly by transient absorption spectroscopy, and the
results were consistent with those in Fig. 4 (see Supplementary
Information). Figure 5 shows the transient absorption signal
Quantum yield of charge separation ( )
LETTERS
0.6
0.4
0.2
0.0
0.0
0.2
0.4
0.6
0.8
Relative white light intensity
1.0
Figure 4 Demonstration of white-light photoprotection. a, Results from a
sample of pentad in 2-methyltetrahydrofuran following irradiation (12 V, 100 W
tungsten-halogen bulb equipped with a 360-nm long-pass filter) with different
white light fluxes (open circles, right axis). The quantum yield of photoinduced
electron transfer for the solution (filled circles, left axis) decreases as the white
light intensity increases, because white light converts increasing amounts of
pentad 1c to 1o, in which the porphyrin excited singlet state lifetime is
quenched. b, Relative overall yield of photoinduced electron transfer as a
function of white light intensity. These points were obtained by multiplying
relative light intensity values by the corresponding quantum yield of
electron transfer.
amplitude of 1 at 1,000 nm following 3 min of thermal
isomerization in the dark, and following 20 s of white light
irradiation. The transient absorption after dark periods is due to
the fullerene radical anion formed by photoinduced electron
transfer from the porphyrin first excited singlet state. The
amplitude is reduced after white light illumination because
under these conditions some of the DHI chromophores
photoisomerize to the BT form, which quenches the porphyrin
first excited singlet state, precluding significant photoinduced
electron transfer. After 15 cycles no significant decomposition of
the sample was observed.
Thus, pentad 1 functions as a nonlinear transducer of light into
electrochemical potential energy in the form of charge separation.
The efficiency of photoinduced electron transfer is high at low light
levels, but smoothly decreases as the level of white light increases.
This phenomenon occurs because the rate of formation of the
photochromic quencher BT (and therefore the fraction of the
pentad in the open form) increases as the white light intensity
increases, but the rate of thermal reversion of BT to the nonquenching DHI is unaffected by light. This self-regulating
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ΔA at 1,000 nm
LETTERS
0.007
must continuously adapt both to changing external environments
and to the function of neighbouring devices.
0.006
Received 17 December 2007; accepted 2 April 2008; published 4 May 2008.
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0.005
0.004
Irradiation periods
Figure 5 Nanosecond transient absorption demonstration of switching
cyclability. The transient absorbance signal amplitude of 1 at 1,000 nm
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of chlorophyll excited singlet states available for initiating the
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Self-regulation is crucial to biological function, but has been
difficult to realize in synthetic systems at the molecular level.
However, molecular self-regulation will be required for many
proposed applications of nanotechnology where components
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Acknowledgements
This work was supported by the U.S. National Science Foundation (CHE-0352599).
Author contributions
S.D.S. contributed to the synthesis and spectroscopic study of the molecules. G.K. performed the transient
absorption experiments and interpreted them. Y.T. contributed to the synthesis. M.H. carried out
electrochemical studies. All authors discussed the results and commented on the manuscript.
Author information
Reprints and permission information is available online at http://npg.nature.com/reprintsandpermissions/.
Correspondence and requests for materials should be addressed to D.G.
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