Ultrafast energy transfer in biomimetic multistrand nanorings

Article abstract of DOI:10.1021/ja504730j

We report the synthesis of LH2-like supramolecular double- and triple-stranded complexes based upon porphyrin nanorings. Energy transfer from the antenna dimers to the π-conjugated nanoring occurs on a subpicosecond time scale, rivaling transfer rates in natural light-harvesting systems. The presence of a second nanoring acceptor doubles the transfer rate, providing strong evidence for multidirectional energy funneling. The behavior of these systems is particularly intriguing because the local nature of the interaction may allow energy transfer into states that are, for cyclic nanorings, symmetry-forbidden in the far field. These complexes are versatile synthetic models for natural light-harvesting systems.

Full text of DOI:10.1021/ja504730j

Communication
pubs.acs.org/JACS
Ultrafast Energy Transfer in Biomimetic Multistrand Nanorings
Patrick Parkinson,† Christiane E. I. Knappke,‡ Nuntaporn Kamonsutthipaijit,‡ Kanokkorn Sirithip,‡
Jonathan D. Matichak,‡ Harry L. Anderson,‡ and Laura M. Herz*,†
†Department of Physics, University of Oxford, Clarendon Laboratory, Parks Road, Oxford OX1 3PU, United Kingdom
‡Department of Chemistry, University of Oxford, Chemistry Research Laboratory, Oxford OX1 3TA, United Kingdom
S
* Supporting Information
mechanisms of both natural and synthetic light-harvesting
systems.
Here we report the synthesis and energy transfer dynamics of
ABSTRACT: We report the synthesis of LH2-like
supramolecular double- and triple-stranded complexes
based upon porphyrin nanorings. Energy transfer from
the antenna dimers to the π-conjugated nanoring occurs
on a subpicosecond time scale, rivaling transfer rates in
natural light-harvesting systems. The presence of a second
nanoring acceptor doubles the transfer rate, providing
strong evidence for multidirectional energy funneling. The
behavior of these systems is particularly intriguing because
the local nature of the interaction may allow energy
transfer into states that are, for cyclic nanorings, symmetry-
forbidden in the far field. These complexes are versatile
synthetic models for natural light-harvesting systems.
two supramolecular antenna-nanoring complexes of a 12-
porphyrin nanoring, c-P12, with two different free-base
porphyrin dimers, P2py2 and P2py4.15 Coordination of the
pyridyl substituents to the zinc metal centers drives the self-
assembly of the complexes, as shown in Figure 1. The ring−
dimer complex c-P12·(P2py2)6 (Figure 1a) consists of a
porphyrin nanoring and six P2py2 dimers; these free-base
porphyrin dimers have one meso-4-pyridyl substituent on each
porphyrin unit to coordinate to the zinc centers of the
nanoring. The 3,5-bis(trihexylsilyl)phenyl substituents on both
components provide solubility and avoid aggregation. The
ring−dimer−ring complex (c-P12)2·(P2py4)6 (Figure 1b)
features analogous porphyrin dimers with four 4-pyridyl
substituents allowing the coordination to two nanorings,
forming a barrel-shaped architecture. To enhance the solubility
of the dimers, dodecyloxy substituents are attached at the 3-
and 5-position of the pyridyl moiety. Details of the synthesis
and characterization of these compounds are given in the
Supporting Information (SI). The association constant of each
P2py2 unit for c-P12 is 5 × 106 M−1. All of the fluorescence
spectra were recorded at concentrations of around 0.1 mM in
toluene; under these conditions the dimer is >99% bound. The
assembled complexes (shown as structural models in Figure
1c,d) have a diameter16 of 47 Å and a dimer porphyrin center
to nanoring porphyrin center distance of 10.2 Å (see the SI for
details). The absorption spectra of the complexes and their
components are plotted in Figure 1e,f (plotted as molar
absorption coefficient, scaled for the number of components).
The absorption spectra of the complexes show notable shifts
compared with the components, in particular a sharpening and
red shift in the nanoring absorption for the ring−dimer−ring
complex, which is attributed to planarization of the nanoring.17
The absorption spectrum of the nanoring undergoes less
change when it forms the c-P12·(P2py2)6 ring−dimer
complex, reflecting the greater conformational heterogeneity
of this complex compared with the more rigid ring−dimer−ring
complex.
atural photosynthetic light-harvesting systems are highly
Nevolved for efficient energy collection, and their photo-
physics has been thoroughly investigated, particularly for
systems from photosynthetic bacteria.1 Many of the critical
properties of these molecular assemblies have been attributed
to the geometric structure of their key light-harvesting
complexes (known as LH1 and LH2).2−5 Photons can be
captured by a number of B800 chromophores, and their energy
is funneled into a ring motif composed of B850 chromophores
held in place by a protein matrix.1,2 Experimental and
theoretical studies on such chromophore systems have revealed
the importance of symmetry,6 energy funneling, and state
decoherence7 for the photosynthetic efficiency;8 however,
active control over natural systems has not yet been achieved
to test the relative importance of such factors.
We are intrigued by the possibility of creating synthetic
biomimetic light-harvesting structures as a route to under-
standing, utilizing, and possibly surpassing the efficiency of the
natural systems.9 A variety of approaches have been ex-
plored;10−12 most recently, investigation of porphyrin nanor-
ings has provided an insight into fully conjugated macro-
molecules with properties analogous to those of the B850 ring
structures in natural LH2, which exhibit electronic delocaliza-
tion around curved surfaces.13 Research on both natural and
synthetic B850-like acceptor nanorings has revealed the
importance of properties such as static and dynamic disorder-
induced symmetry breaking.6,14 However, studies of energy
transfer from antenna chromophores to a synthetic nanoring
have been limited by the challenges in creating such systems.
Investigating the energy dynamics in synthetic LH2-like
complexes may give important insights into the working
We found that the complexes exhibit efficient energy transfer
from the dimer antennae to the nanoring (Figure 2a,b). When
the complexes are assembled without additional free dimer in
solution, the photoluminescence (PL) spectra are dominated
Received: May 12, 2014
© XXXX American Chemical Society
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Journal of the American Chemical Society
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Figure 1. (a, b) Chemical structures and (c, d) structural models of the ring−dimer complex c-P12·(P2py2)6 (top) and the ring−dimer−ring
complex (c-P12)2·(P2py4)6 (bottom). Ar = 3,5-bis(trihexylsilyl)phenyl, R = trihexylsilyl, R′ = dodecyl. (e, f) Plots of the molar absorption
coefficients of the components in toluene/1% pyridine (dimer in blue, c-P12 nanoring in green), scaled for their relative numbers within the
complex, as functions of wavelength. The absorption spectra of the two complexes in toluene (solid red lines, offset for clarity) are also shown. The
excitation wavelength used for PL measurements (450 nm) is indicated as a dashed vertical blue line. The models shown in (c) and (d) are energy-
minimized geometries calculated using the mm+ force field in HyperChem.
to nanoring resulted in an abrupt onset of dimer emission at the
end point of the titration, revealing the presence of unbound
dimer in the solution. As expected, close to six dimers per
c‑P12 nanoring for the ring−dimer complex and close to three
dimers per nanoring for the ring−dimer−ring complex were
required (Figure 2c,d).
The addition of an excess of a competing ligand such as
pyridine (1% by volume) effectively dissociated the complexes.
In this way, we were able to achieve full control over the
association state of the complexes, allowing for unambiguous
isolation of electronic effects leading to energy transfer from
dimers to nanorings. Figure 3a,b shows the PL spectra for the
complexes in their associated state (blue line) and their
dissociated state following addition of pyridine (red line). The
vertical dashed red lines indicate the dimer PL emission
wavelengths of 731 and 716 nm for the ring−dimer and ring−
dimer−ring complexes, respectively. A qualitative comparison
of the PL from the assembled and disassembled states shows
the expected quenching of dimer emission for associated states.
Figure 2. PL titrations (excitation at 450 nm) of c-P12 with (a, c)
In addition, the effect of decreased planarization for the ring−
dimer complex can be observed through changes in both the
spectral position and intensity of the nanoring emission.13
To explore the rates of energy transfer in these complexes,
we employed ultrafast time-resolved PL spectroscopy. Both PL
upconversion (PLUC) and time-correlated single-photon
counting (TCSPC) techniques were used to provide subpico-
second time resolution and nanosecond range, respectively (a
detailed experimental description is given in the SI). We
experimentally assessed the dimer-to-nanoring energy transfer
process by comparing the dynamics18 of dimer emission in the
associated state with that of the free dimer after dissociation of
the complex upon addition of excess pyridine. In the
supramolecular complex, energy transfer to the nanoring
P2py2 and (b, d) P2py4, normalized to the nanoring emission peaks
in (a) and (b). The end points are indicated by black arrows at
approximately 6 equiv of P2py2 (c) and 3 equiv of P2py4 (d) per c-
P12.
by the emission from the nanoring acceptors (800−900 nm). In
these measurements, the components were excited at a
wavelength of 450 nm (see the dashed blue lines in the
absorption spectra in Figure 1e,f), which gave approximately
2:1 (1:1) selectivity for dimer excitation in the ring−dimer
(ring−dimer−ring) complex. The effective quenching of the
dimer PL (710−730 nm) therefore qualitatively demonstrates
the occurrence of efficient energy transfer to the nanoring
acceptor. Figure 2 shows that an increase in the ratio of dimer
B
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Journal of the American Chemical Society
Communication
the energy transfer in the presented complexes. In general, the
lowest excited state in a molecular ring sustaining fully
delocalized excitonic states is expected to be dipole-forbidden
by symmetry.17 However, natural systems tend to exhibit
disorder-allowed radiative transitions due to flexibility in the
protein scaffold supporting the ring structure.6 In contrast, fully
conjugated porphyrin nanorings ought to exhibit lower
disorder, leading to an absorbing state that is fully delocalized
around the ring23 and an optically dark lowest exciton state.24
As a result, full models of the energy transfer dynamics are
likely to be complex, even in more robust synthetic systems. In
particular, the simple Forster model is expected to fail,5,25 as the
̈
emitting and absorbing moieties in the complex lie around 10 Å
apart at their closest separation, while the dimer is 25 Å in
length. A description in terms of a point dipole can therefore
only ever be a first-order approximation as it suffers from two
primary flaws: the unphysical allocation of the dipole strength
to the geometric center of the nanoring and the neglect of dark
absorption states (states with no far-field oscillator strength).
The former may be addressed through the use of the more
accurate line-dipole approximation26,27 to distribute excitonic
strength around the rim of the nanoring. The latter requires
further knowledge of the electronic states of the acceptor. All of
these states except for the allowed k = 1 state ought to be
forbidden for the high-symmetry nanoring system and should
have no far-field absorption.8 However, as far as energy transfer
from the dimer to the nanoring is concerned, it is not
reasonable to neglect these states, as the donor dimer is close
enough to break the symmetry of the interaction, leading to a
non-negligible energy transfer rate. Since these states are
optically inactive in the far field, they cannot be easily observed
experimentally, and calculations of the exciton energy level
spacing will be essential to allow rigorous modeling of energy
transfer in the complexes. Unfortunately, present computa-
tional techniques are not able to accurately model the large
structures presented here, and a quantitative description of the
energy dynamics is therefore beyond the scope of this work.
Tuning of the exciton-state energies through modification of
the complex size or geometry provides an example of the way
that synthetic complexes may shed light upon energy transfer in
natural LH2 antenna systems. In natural light-harvesting
systems, such optically dark states have been suggested to be
responsible for both the rapid energy transfer and high overall
photosynthetic efficiency of these structures25 and are an
important target for further research.
Figure 3. (a, b) Steady-state PL spectra for the (a) ring−dimer and
(b) ring−dimer−ring complexes in the associated (blue line) and
dissociated (red line) states. The dimer emission wavelength is
indicated by the vertical dashed red lines. (c, d) Time-resolved PL
dynamics for dimer emission for the (c) ring−dimer and (d) ring−
dimer−ring structures for each association state.
provides an additional and dominant decay channel, leading to
rapid PL quenching. Figure 3c,d shows that the energy transfer
is remarkably fast: the dimer PL emission for the associated
states (blue points and lines) drops rapidly in comparison with
that for the dissociated states (red points and lines). By
modeling the ratio of the dimer emissions for the assembled
and disassembled states, we were able to determine energy
transfer rates of (1.25 ps)−1 and (0.65 ps)−1 for the ring−dimer
complex c-P12·(P2py2)6 and the ring−dimer−ring complex
(c‑P12)2·(P2py4)6, respectively. The effective doubling of the
energy transfer rate upon addition of the second nanoring is a
striking demonstration of the effects of adding a second,
symmetric acceptor deactivation channel (see further details in
the SI). These synthetic ring assemblies therefore demonstrate
the feasibility of both uni- and bidirectional energy funneling.
Excitations on c-P12 have lifetimes of 850 and 1150 ps for the
ring−dimer and ring−dimer−ring geometries, respectively (see
the SI for details), comparable to the lifetimes of 600−1200 ps
for the excited states of natural LH2 complexes.19 This is
significantly longer than the typical time required for energy
collection from natural LH2 (2−5 ps)3 or for charge transfer in
synthetic porphyrin−fullerene systems,20 providing ample time
for efficient solar energy harvesting.
In summary, we have reported two synthetic supramolecular
complexes with analogies to natural LH2 antenna systems.
Extremely rapid energy transfer from porphyrin dimer antenna
molecules to the 12-porphyrin nanoring acceptor was observed
in time-resolved PL measurements, and the energy rate doubles
upon the addition of a second acceptor nanoring. These
systems thus have energy transfer rates that are comparable to
those observed in natural light-harvesting systems, making
them interesting for understanding energy transfer in natural
light-harvesting systems. In addition, both uni- and bidirectional
energy transfer was shown to be feasible, highlighting the
potential use of these systems for highly selective energy
channeling in solar-harvesting applications.
It is illuminating to compare the energy transfer rates
observed for these synthetic nanoring assemblies to those of
their intensively studied natural counterparts. In LH2
complexes of purple bacteria, a rate of (0.9 ps)−1 for energy
transfer between B800 antenna chromophores and the B850
chromophore array has been established.8,21 Such a high rate is
in general not well modeled by the standard Forster point-
̈
dipole equation and has been attributed to a variety of more
complex processes. The presence of a virtual intermediate state
(via the carotenoid molecule),5 quantum coherent transfer,7,22
and disorder-assisted4 energy transfer have been proposed. It is
noted that while such effects are not expected to be relevant for
synthetic systems, strikingly similar energy transfer rates are
found. This suggests the possibility of gaining further insight
into the natural light-harvesting systems through modeling of
ASSOCIATED CONTENT
* Supporting Information
Synthesis and characterization of the investigated compounds
and supramolecular complexes, PL quantum yield measure-
■
S
C
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Journal of the American Chemical Society
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Muranaka, A.; Uchiyama, M.; Aida, T. Angew. Chem., Int. Ed. 2008, 47,
5153.
ments, optical spectroscopy experimental details, and effects of
stoichiometry on energy transfer. This material is available free
of charge via the Internet at http://pubs.acs.org.
(16) O’Sullivan, M. C.; Sprafke, J. K.; Kondratuk, D. V.; Rinfray, C.;
Claridge, T. D. W.; Saywell, A.; Blunt, M. O.; O’Shea, J. N.; Beton, P.
H.; Malfois, M.; Anderson, H. L. Nature 2011, 469, 72.
(17) Kondratuk, D. V.; Perdigao, L. M. A.; Sullivan, M. C. O.; Svatek,
S.; Smith, G.; Shea, J. N. O.; Beton, P. H.; Anderson, H. L. Angew.
Chem., Int. Ed. 2012, 51, 6696.
AUTHOR INFORMATION
Corresponding Author
l.herz1@physics.ox.ac.uk
■
(18) Parkinson, P.; Aharon, E.; Chang, M. H.; Dosche, C.; Frey, G.
Notes
L.; Kohler, A.; Herz, L. M. Phys. Rev. B 2007, 75, No. 165206.
̈
The authors declare no competing financial interest.
(19) Bergstrom, H.; Sundstrom, V.; van Grondelle, R.; Gillbro, T.;
̈
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Cogdell, R. Biochim. Biophys. Acta 1988, 936, 90−98.
(20) Kahnt, A.; Karnbratt, J.; Esdaile, L. J.; Hutin, M.; Sawada, K.;
Anderson, H. L.; Albinsson, B. J. Am. Chem. Soc. 2011, 133, 9863.
ACKNOWLEDGMENTS
■
̈
We thank the EPSRC, the ERC, the People Programme (Marie
Curie Actions) of the European Union’s Seventh Framework
Programme (FP7/2007-2013) under REA Grant Agreement
299925, and the Defense Advanced Research Projects Agency
(DARPA) for support. C.E.I.K. further thanks the DAAD
(German Academic Exchange Service) for funding. K.S. was
funded by Strategic Scholarships for Frontier Research
Network for Research Groups (CHE-RES-RG50) from the
Office of Higher Education Council of Thailand. N.K. was
supported by a Royal Thai Government Scholarship. We thank
the National Mass Spectrometry Facility (Swansea) for mass
spectra.
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T.; Scheer, H.; Cogdell, R. J.; Sundstrom, V. Biophys. J. 2000, 78, 2590.
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