Excitation Energy Transfer Pathways in Asymmetric Covalent

May 19, 2009 - We report the observation of multiple excitation energy transfer (EET) pathways in a covalently linked, chlorophyll (Chl) tetramer havi...
1 downloads 0 Views 707KB Size
Download PDF
11936

J. Phys. Chem. C 2009, 113, 11936–11942

Excitation Energy Transfer Pathways in Asymmetric Covalent Chlorophyll a Tetramers† Victoria L. Gunderson, Thea M. Wilson, and Michael R. Wasielewski* Department of Chemistry and Argonne-Northwestern Solar Energy Research (ANSER) Center, Northwestern UniVersity, EVanston, Illinois 60208-3113 ReceiVed: March 19, 2009; ReVised Manuscript ReceiVed: April 30, 2009

We report the observation of multiple excitation energy transfer (EET) pathways in a covalently linked, chlorophyll (Chl) tetramer having three different fixed Chl-Chl distances. The tetramer was synthesized by covalently attaching 20-(4-ethynylphenyl)Chl to the 1,3,6,8-positions of pyrene to give Chl4-py. Reference Chl oligomers were prepared by attaching 20-(4-ethynylphenyl)Chl to the 1-position of pyrene (Chl-py), the 1,8 and 3,6 positions of pyrene (para-Chl2-py and ortho-Chl2-py, respectively), and the 1,3,5-positions of benzene (meta-Chl3). The Chlx-py derivatives were studied using femtosecond transient absorption (TA) and transient absorption anisotropy (TAA) spectroscopy, and compared with data obtained earlier on meta-Chl3. Using femtosecond TA, the decay of 1*Chl4-py was monitored after photoexcitation of its Qy band with a 655 nm, 130 fs laser pulse. A triexponential decay of 1*Chl4-py (τ ) 7 ps, 152 ps, and 4.2 ns) was observed, with the two shorter time constants being laser intensity dependent. This dependency is indicative of singlet-singlet annihilation and is attributed to EET via two pathways, those involving the two closest Chl’s (ortho/meta), which are kinetically indistinguishable, and the two most distant (para) Chl’s. Further confirmation of multiple EET pathways was made by femtosecond TAA measurements. Fo¨rster energy transfer lifetimes were calculated for the three possible energy transfer pathways (ortho, 20 ps; meta, 34 ps; and para, 150 ps) and compared to the experimental results. Our results indicate that EET between nonadjacent chromophores having high oscillator strengths, such as the para Chl’s in Chl4-py, is significant, and the additional utilization of the minor EET contributing pathways may provide greater avenues for designing efficient light harvesting in future artificial photosynthetic systems. Introduction Photosynthetic organisms use antenna proteins containing multiple chlorophylls (Chl’s) to harvest light energy. Following absorption of a photon, the resulting exciton undergoes excitation energy transfer (EET) among the Chl’s within the antenna proteins and is ultimately trapped by Chl’s within the reaction center protein that uses the excitation energy to drive photochemical charge separation.1 Nature has tuned EET to take place at high efficiency, so that a clear understanding of EET mechanisms between Chl’s is important for understanding the natural process, designing artificial photosynthetic systems, and developing light-harvesting strategies for solar cell applications.2-4 Linear,5-7 cyclic,8,9 and more complex10,11 covalent biomimetic multiporphyrin structures have been investigated as models for EET in photosynthetic antenna proteins. While porphyrins and Chl’s are structurally similar, their electronic properties are different because the reduced pyrrolic D-ring in Chl’s both orients and greatly increases the magnitude of the transition dipole moment of their lowest energy Qy optical transition. This increase produces the characteristic ability of Chl’s to absorb light throughout the visible spectrum. Moreover, the strongly directional nature of the Qy transition moment relative to the Chl molecular framework results in significant spectral shifts of the Chl electronic absorption bands due to exciton coupling between the Qy transition moments of neighboring Chl’s. To a large degree, these shifts result in the wide variety of Chl a spectral forms observed in both antenna and reaction center †

Part of the “Hiroshi Masuhara Festschrift”. * Address Ccorrespondence to this author. E-mail: m-wasielewski@ northwestern.edu.

proteins.12-14 Despite the advantages of using Chl’s to study these phenomena, porphyrins have typically been used as surrogates for Chl’s because multiporphyrin arrays having welldefined distances and orientations between the porphyrins are generally easier to synthesize than the corresponding Chl arrays. Lindsey, Bocian, Holten, and co-workers have demonstrated differences in energy transfer rates between both adjacent and nonadjacent porphyrins in multichromophore arrays.10,15,16 Their studies probed energy transfer steps within porphyrin arrays containing zinc, magnesium, and free base porphyrins. Using femtosecond transient absorption (TA) spectroscopy to observe energy transfer from metalloporphyrins to a free base porphyrin energy trap site in multiporphyrin arrays, they found that energy transfer to nearest neighbor porphyrins dominates, but energy transfer between more distant porphyrins also contributes to the observed overall EET efficiency. While porphyrin arrays have elucidated important features of EET, the inherent electronic asymmetry of Chl may offer additional insights into EET mechanisms. Previous studies of synthetic chlorins have focused largely on the role of the covalent linker on EET in dyads.17-19 Time-resolved spectroscopic studies on Chl-containing pigment proteins have shown the importance of well-defined geometries for efficient EET,2,20,21 while synthetic modifications to Chl at the 3-, 8-, and 17-carbon positions have helped to explain and replicate the self-assembly of the bacteriochlorophylls associated with the peripheral antenna complexes of green sulfur bacteria.22-24 These bacteriochlorophylls are actually chlorins that are closely related structurally and electronically to Chl a. However, synthetic modifications of these pigments often result in large changes to the Chl absorption spectrum upon aggregation, which are intrinsically interesting but can adversely affect EET

10.1021/jp902515p CCC: $40.75  2009 American Chemical Society Published on Web 05/19/2009

Asymmetric Covalent Chlorophyll a Tetramers

J. Phys. Chem. C, Vol. 113, No. 27, 2009 11937

Figure 1. Structures of molecules used in this study.

efficiencies and complicate the interpretation of EET mechanisms.25 Recent work has shown that functionalization of the 20-position of Chl a provides a convenient method for building multi-Chl arrays having fixed Chl-Chl distances that largely retain the overall spectral features of the monomeric Chl absorption spectrum,26-28 while leaving the central metal and the 131 carbonyl group of the Chl available for self-assembly of these building blocks into larger structures for light harvesting as well as charge separation and transport.29-34 For example, covalently linked Chl trefoils (meta-Chl3, Figure 1) have demonstrated both energy and charge transfer that varies with both chromophore distance and bond connectivity.27 In this fixed distance Chl system, the Fo¨rster EET mechanism35-37 is largely responsible for EET between the adjacent chromophores. However, multi-Chl arrays having fixed Chl-Chl distances that probe multiple EET pathways have yet to be examined. Two pump-probe spectroscopic methods are widely used to measure EET rates in multichromophore arrays having identical chromophores: transient absorption anisotropy (TAA)26,38-40 and singlet-singlet annihilation (SSA).11,26,27,41,42 Briefly, TAA monitors changes in the transition dipole moment direction over time. Upon photoexcitation, an excited chromophore with a well-defined transition moment direction may undergo EET to a different chromophore having a transition moment oriented in a new direction. This change in the dipole moment direction directly monitors the EET rate between the two chromophores. Alternatively, SSA depends on the fact that, under typical laser photon fluxes, two or more chomophores may be excited in a multichromophore array, provided that their electronic transitions have significant oscillator strengths. Upon absorption of two photons, the excited singlet states, S1 (excitons), produced within a multichromophore array will migrate by means of energy transfer within the array until they collide. The two singlet excitons annihilate, placing one

chromophore in a higher energy excited state, Sn, while the other chromophore undergoes nonradiative decay to the ground state, S0. Rapid internal conversion of Sn to S1 results in a single excited chromophore in its S1 state. Thus, SSA results in an overall loss of S1 population at a rate that reflects the energy transfer rate, and is most often much faster than the intrinsic S1 decay rate. By increasing the pump laser intensity, the probability for multiple chromophore excitation and subsequent SSA increases. To study multiple EET pathways between the pairs of fixed distance Chl’s, we have synthesized an asymmetric Chl tetramer (Chl4-py, Figure 1) along with a series of appropriate reference molecules, and we have determined the singlet energy transfer rates within them using femtosecond time-resolved optical spectroscopy. Our results indicate that all EET pathways are viable and most likely occur by the Fo¨rster EET mechanism within these covalent Chl arrays. However, significant deviations from the Fo¨rster model occur for energy transfer rates between Chl’s at the closest distances. Experimental Section Synthesis. The syntheses of Chl4-py, Chl1-py, para-Chl2-py, and ortho-Chl2-py (Figure 1) are briefly described below and outlined explicitly in the Supporting Information, while the synthesis of meta-Chl3 has been reported earlier.27 Chl a was extracted from the cyanobacterium Spirulina maxima and converted to methyl pyropheophorbide a.43 Selective hydrogenation of the double bond at the 3 position yielded methyl 3-ethylpyropheophorbide a, and the resulting compound was then brominated at the 20-position.44 Methyl 20-bromo-3-ethylpyropheophorbide a underwent a series of reactions to yield zinc 2′-octyldodecyl-3-ethyl-20-(4-ethynylphenyl)-pyrochlorophyllide a.27 This was further used in a 4-fold, copper-free

11938

J. Phys. Chem. C, Vol. 113, No. 27, 2009

Gunderson et al.

Sonogashira reaction45,46 with 1,3,6,8-tetrabromopyrene47 to yield Chl4-py. Model compounds Chl1-py, ortho-Chl2-py, and para-Chl2-py were synthesized in a similar manner. Intermediates and the resulting products were characterized by 1H NMR, HR-MALDI-TOF, and UV-vis spectroscopy. Optical Spectroscopy. Steady-state absorption spectroscopy was performed using a Shimadzu 1601 UV/vis spectrophotometer. A single-photon-counting fluorimeter (Photon Technology International) was used for emission experiments. Measurements were performed at room temperature in a 1 cm quartz cuvette with excitation/emission geometries at right angles. All solvents were spectroscopic grade and used as is, except for tetrahydrofuran (THF), which was further purified by passing it twice through alumina (GlassContour) immediately prior to use. Femtosecond TA and TAA measurements were made using a Ti:sapphire laser system detailed previously.26,48 The instrument response function (IRF) for the pump-probe experiments was 180 fs. Typically 5 s of averaging was used to obtain the transient spectrum at a given delay time. Samples were photoexcited with 655 or 416 nm, 130 fs, 0.25-1.00 µJ laser pulses focused to a 200 µm spot in a 2 mm path length quartz cuvette. The optical density at the pump wavelength was kept between 0.5 and 0.7. Analysis of the kinetic data was performed at multiple wavelengths using a Levenberg-Marquardt nonlinear least-squares fit to a general sum-of-exponentials function convoluted with a Gaussian instrument response function. For transient absorption anisotropy (TAA) experiments, the polarization of the probe light in the transient absorption apparatus was set to 45° with respect to the pump light before reaching the sample. After passing through the excited sample, the probe beam was split into its parallel and perpendicular polarization components using a polarizing beamsplitter cube. Data for both the pump-probe orientations were simultaneously detected by a dual channel spectrometer (DS 2000 and ADC2000-PCI+, Ocean Optics). The anisotropy decays were then calculated from eq 1:

r(t) )

∆APAR(t) - G∆APERP(t) ∆APAR(t) + 2G∆APERP(t)

(1)

where ∆APAR(t) and ∆APERP(t) correspond to the intensity of the transient absorption changes when the pump-probe orientations are parallel and perpendicular, respectively. The factor G is defined as ∆APAR(t)/∆APERP(t) and was used to correct for differences in the sensitivities of the detection system for vertically and horizontally polarized light. Kinetic analyses of this data were also performed at several wavelengths using the same method described above. Time-resolved fluorescence (TRF) lifetimes were determined using a frequency doubled, cavity-dumped Ti:sapphire laser as the excitation source and a Hamamatsu C4780 ps fluorescence lifetime measurement system as described previously.28,49 The energy of the 400 nm, 25 fs pulses was attenuated to e1.0 nJ/ pulse for all fluorescence lifetime experiments. The total instrument response function of the streak camera system was 25 ps. The samples were prepared in 1 cm quartz cuvettes, and the optical density at the excitation wavelength was typically 0.020-0.035. All fluorescence data were acquired in single photon counting mode using the Hamamatsu HPD-TA software, and the data was analyzed using the Hamamatsu fitting module and deconvoluted using the laser pulse profile.

Figure 2. Steady-state absorption spectra of Chl4-py, para-Chl2-py, ortho-Chl2-py, and Chl1-py in THF.

Figure 3. Femtosecond TA of Chl4-py in THF excited at 655 nm. The inset shows normalized kinetic traces (to unity at the absorption minimum) taken at 666 nm with pump-pulse powers varying from 0.25 µJ/pulse to 1.00 µJ/pulse.

Results Steady-State Spectroscopy. The ground-state absorption spectra of the Chlx-py series in THF are shown in Figure 2. The Soret bands occur at 430 nm, and the Qy band (0,0) maxima occur at 655 nm. The shoulder seen for Chl4-py at 475 nm results from the tetrakis(phenylethynyl)pyrene spacer. The Chl1-py and Chl4-py fluorescence spectra are shown in Figure S1 and exhibit emission maxima at 658 nm in THF. No significant spectral changes are observed upon increased Chl substitution about the pyrene core. Fluorescence quantum yields range from 0.18 for Chl1-py to 0.11 for Chl4-py and were determined using zinc 3-ethyl-pyrochlorophyllide a as a fluorescence standard.28 Time-Resolved Spectroscopy. Femtosecond TA measurements on Chl4-py were performed in THF using 655 nm, 130 fs excitation pulses (Figure 3). The ground-state bleaches of the Soret and Qy (0,0) bands are seen at 430 and 655 nm, respectively. Stimulated emission is also evident from the asymmetry of the red edge of the 655 nm bleach and from the small negative feature at 722 nm. The broad positive features throughout the spectrum are attributed to 1*Chl4-py absorption and are punctuated by ∆A due to the ground-state bleach. The decay of 1*Chl4-py was monitored at 666 nm. The 666 nm ∆A exhibits triexponential decays having τ ) 7 ps, 152 ps, and 4.2 ns (Table 1). Excitation at 655 nm of the model compounds Chl1-py, ortho-Chl2-py, and para-Chl2-py yields the transient absorption spectra shown in Figures 4, S2, and S3, respectively. No large spectral differences were observed between the molecules in the Chlx-py series, but their 1*Chlx-py lifetimes vary significantly. Chl1-py exhibits a 4.0 ns monoexponential decay, while the ortho-Chl2-py and para-Chl2-py kinetics are both biexponential with 8 ps and 3.9 ns decays, and 170 ps and

Asymmetric Covalent Chlorophyll a Tetramers

J. Phys. Chem. C, Vol. 113, No. 27, 2009 11939

TABLE 1: Kinetic Time Constants for the Chlx-py Series TAA lifetimesb (ps) Chl1-py 387 ( ortho-Chl2-py 3 ( 2 386 ( 305 ( para-Chl2-py meta-Chl3a Chl4-py 2 ( 1 385 ( 921 (

TRF lifetimes

TA lifetimesb (ps)

(ps)

40 56 8 ( 1 95 170 ( 49 3(1 42 7 ( 2 152 ( 55 74

(ns) 4.0 3.9 4.0 4.1 4.2

( ( ( ( (

0.3 0.1 0.2 0.2 0.8

(ns) 3.7 3.9 3.7 3.9 3.5

( ( ( ( (

0.1 0.1 0.1 0.1 0.1

a Reference 27. b Femtosecond TAA kinetics were determined at 597 nm, and femtosecond TA spectroscopy kinetics were determined at 666 nm.

Figure 5. Femtosecond TAA spectroscopy parallel and perpendicular kinetic traces at 597 nm for Chl4-py. The inset shows the calculated anisotropy kinetics at 597 nm as determined by eq 1.

Figure 4. Femtosecond TA of Chl1-py in THF excited at 655 nm. The inset shows a kinetic trace taken at 666 nm with a pump-pulse power of 1.00 µJ/pulse.

4 ns decays, respectively (Table 1). Furthermore, the amplitudes of the 7 and 152 ps components of Chl4-py, the amplitude of the 8 ps component of ortho-Chl2-py, and the amplitude of the 170 ps component of para-Chl2-py are all laser intensity dependent, while Chl1-py displays no such dependence. As reported earlier,27 comparable data for meta-Chl3 also show biexponential kinetics with 3 ps and 4.1 ns decay components, with the short component amplitude being laser intensity dependent. The femtosecond TA measurements were repeated with Soret band excitation at 416 nm, yielding transient spectra (Figures S4-S5) identical to those obtained using 655 nm excitation (Figures 3 and 4). The decay kinetics for the transient absorption features are also identical regardless of the excitation wavelength, thereby showing that S2 to S1 internal conversion occurs on a time scale shorter than the 180 fs IRF of our femtosecond TA apparatus. Time-resolved fluorescence (TRF) experiments on the Chlxpy series using 400 nm, 25 fs laser excitation show that the long-lived (∼4 ns) fluorescence lifetimes for all Chlx-py molecules match the long-lived stimulated emission decay components seen in the femtosecond TA studies (Table 1). The data are presented in the Supporting Information (Figures S6-S9). TAA spectroscopy was performed on all Chlx-py molecules using 655 nm, 130 ps laser pulses and probing with a white light continuum. The individual parallel and perpendicular components for each molecule were combined using eq 1 to give the time-resolved anisotropy changes monitored at 597 nm shown for Chl4-py in Figure 5 and for the remaining reference molecules in Figures S10-S12. The kinetic fits to the data are summarized in Table 1. Multiple depolarization channels exist

Figure 6. Schematic diagram of possible EET pathways for Chl4-py after excitation of one Chl chromophore.

for all four molecules and lead to multiple observed lifetimes; that is, Chl4-py exhibits a triexponential decay (τ ) 2, 385, and 921 ps). Discussion Two distinct SSA time constants have been previously observed for polyphenyl,50 porphyrin,11 and perylene-3,4dicarboximide dendrimers,51,52 as well as for porphyrin boxes.53 In these studies, multiple annihilation lifetimes are attributed to EET in molecules that exhibit some degree of flexibility. Variations in their conformations can be used to explain the multiple observed lifetimes. However, the center-to-center distances between the Chl’s within Chl4-py as well as the reference dimers and trimer are restricted by the stiff phenylethynyl linker, so that the observation of multiple SSA time constants in these systems can be analyzed in terms of distinct EET pathways. Three possible EET pathways exist within Chl4py, which are labeled ortho, meta, and para (Figure 6). Steric hindrance between the phenyl attached to the 20-position of the Chl and the adjacent Chl methyl groups makes the dihedral angle between their π systems about 70°, thereby limiting electronic interaction between them.27 Rotation about the ethynylphenyl and ethynylpyrene linkages is essentially unre-

11940

J. Phys. Chem. C, Vol. 113, No. 27, 2009

Gunderson et al.

TABLE 2: EET Time Constants for the Chlx-py Series SSA data (ps) Chl4-py ortho-Chl2-py para-Chl2-py meta-Chl3a a

8(2 16 ( 2 6(2

304 ( 110 340 ( 100

TABLE 3: Rotational Diffusion Lifetimes in THF Calculated Using the Modified Perrin Equation

TAA data (ps) 6(3 9(6

385 ( 42 305 ( 95

Reference 27.

stricted, so that the dihedral angles between the Chl and pyrene π systems are expected to adopt a nearly flat distribution. As a consequence, the Chl transition dipole, which is polarized along the ring A-ring D direction should have a significant net component along the axis joining the Chl 10 and 20 positions, which is parallel to the axis of its attachment to pyrene. A comparison between the femtosecond TA kinetics of Chl4py and those of the model compounds ortho-Chl2-py and paraChl2-py along with data obtained previously on meta-Chl327 helps to assign the two observed SSA time constants of Chl4py to EET between specific pairs of Chl’s. As shown in Table 1, the 7 ps SSA component of Chl4-py agrees well with the observed single 8 ps SSA component in ortho-Chl2-py. Similarly, the 152 ps SSA component of Chl4-py agrees reasonably well with the 170 ps single SSA component observed for paraChl2-py. While no distinct third SSA component was observed for Chl4-py, meta-Chl3 was previously shown to have a 3 ps SSA lifetime.27 The individual time constants for the ortho and meta pathways within Chl4-py are indistinguishable within the error limits of the data,26 so that we can model the SSA data assuming that the energy transfer rates between Chl’s that are ortho or meta to each other are the same, while the longer, para pathway is distinct. If we assume that SSA for the ortho and meta pathways is the result of random exciton transfer between nearest neighbor molecules that constitute EET around a four Chl ring, then we can employ the following equation, as previously described by Trinkunas54 for EET around a finite molecular ring structure. Therefore, the EET lifetime, τEET, can be derived from the SSA lifetime, τSSA, for any N equivalent chromophores:

ring τSSA )

τEET 8 sin2(π/2N)

(2)

This treatment assumes that any transannular EET pathways are slow relative to EET around the ring, a condition that the data for Chl4-py shows is fulfilled. Using eq 2, the observed 7 ps SSA lifetime, and N ) 4 yields τEET ) 8 ps. For the slow transannular (para) pathway, the EET lifetime is approximated by the time constant for annihilation of two Chl singlet excitons, τEET ) 2τSSA ) 304 ps. These data and those for the reference molecules are summarized in Table 2. In our femtosecond TA spectroscopy experiments, the angle between the pump and probe beam polarizations is set to the magic angle (54.7°), so that the effects of rotational diffusion are removed from the observed transient kinetics. However, in TAA spectroscopy, rotational diffusion frequently dominates the observed TAA decays. To better understand our TAA decay kinetics (Table 1), the rotational diffusion time constants of the Chl compounds were estimated using the Perrin equation55

r0 τ ) 1 + ) 1 + 6Dτ r θ

(3)

molecule

volume (Å3)

τrot (ps)

Chl1-py ortho-Chl2-py para-Chl2-py Chl4-py

1540 3451 2590 6070

202 461 346 811

where τ is the fluorescence lifetime, θ is the rotational correlation time, and D is the rotational diffusion coefficient. Assuming that the molecule is spherical, eq 3 can be approximated as

r(t) ) r0e-t/θ ) r0e-6Dt

(4)

In this expression, the rotational correlation time (θ) is represented by

θ)

ηV RT

(5)

where η is the viscosity, V is the volume of the rotating unit, R is the gas constant, and T is the temperature in Kelvin. As shown, θ ) (6D)-1 relates time to the rotational diffusion coefficient. Since the rotational diffusion time constant (τrot) is the rotational correlation time per molecule, τrot can be expressed by the Debye equation

τrot )

ηV kBT

(6)

where kB is the Boltzmann constant. The volumes of the Chlxpy molecules were estimated from MM+ optimized geometries using HyperChem56 and are shown in Table 3. Using eq 6, η ) 0.48 cP, and the calculated volumes, τrot was determined for each molecule at room temperature (Table 3). The 921 ps component in the observed TAA decay kinetics of Chl4-py correlates well with the calculated rotational diffusion time (Table 3). The remaining shorter anisotropy lifetimes can be analyzed in terms of the EET pathways. The 385 ps TAA decay component agrees within experimental error with the 304 ps SSA component, both of which are assigned to the para pathway. The fast (2 ps) TAA decay component observed for Chl4-py is due to EET by the ortho and meta pathways. Once again, these pathways are indistinguishable within the limits of the data and will be treated as equivalent. In that case, the TAA decay time constant can be related to the EET time constant for a ring structure using eq 7,57

τEET ) 4(1 - cos2(R))τTAA

(7)

where R is the angle between the transition moments of the adjacent chromophores. For Chl4-py the average value of R for the ortho and meta pathways is 60°, so that τEET ) 3τTAA. Thus, using the experimental TAA decay time constant for Chl4-py, τEET ) 6 ps, which agrees within experimental error with the 8 ps time constant obtained from SSA measurement. The calculated rotational diffusion time constants for the ortho-Chl2-py and para-Chl2-py reference molecules are both ∼400 ps. In the case of para-Chl2-py, the rotational diffusion time constant is essentially the same as the EET time constant

Asymmetric Covalent Chlorophyll a Tetramers

J. Phys. Chem. C, Vol. 113, No. 27, 2009 11941

TABLE 4: Parameters and Results for Fo¨rster Energy Transfer Calculations for Chl4-py EET Pathways (n ) 1.407) EET pathway

κ2

R (Å)

ΦF

τ (ns)

Fo¨rster lifetime (ps) S 1 f Sn

ortho meta para

0.58 0.61 0.68

16.9 21.5 28.1

0.18 0.18 0.18

3.72 3.72 3.72

20 34 150

measured using SSA. Thus, the TAA data does not provide an independent check of the EET time constant for that case, yet the observation of a single TAA decay time constant for paraChl2-py is consistent with the coincidental similarity of the EET and rotational diffusion time constants. On the other hand, the 9 ps EET time constant for ortho-Chl2-py agrees to within experimental uncertainty with the 16 ps value determined from the SSA data. Both the SSA and TAA results are consistent with EET via the three pathways, ortho, meta, and para; however, the data can only distinguish the para pathway from the faster ortho and meta pathways. Unlike previous multipathway EET studies,11,50-52 the rigidity of the ethynyl linkage limits the conformational flexibility in the Chlx-py series, so that the observed differences in energy transfer rates largely reflect the different Chl-Chl distances within these molecules. Further characterization of the EET pathways requires modeling the EET mechanism. Two energy transfer mechanisms are typical: Fo¨rster,35-37 or through-space EET, and Dexter,58 or throughbond EET. To determine the EET mechanism in the Chlx-py series, EET time constants (τEET ) 1/kEET) were calculated using Fo¨rster theory for each of the three viable EET pathways (Figure 6) using eq 8

kEET(r) )

(

φDκ2 9000(ln 10) τDr6 128π5Nη4

)∫

∞

0

FD(λ) εA(λ)λ4 dλ

(8)

where κ2 is the geometrical factor, φD is the quantum yield of the donor in the absence of the acceptor, n2 is the refractive index of the solvent, N is Avogadro’s number, r is the distance between the donor and acceptor, τD is the fluorescence lifetime of the donor, FD(λ) is the fluorescence intensity of the donor normalized to unity, λ is the wavelength, and εA is the extinction coefficient of the acceptor.35-37 Because energy transfer occurs between identical Chl’s, the spectra of Chl1-py were used for both the donor and acceptor. Distances between Chl’s were determined from MM+ optimized geometries using HyperChem.56 The spectral overlap between the donor and acceptor Chl’s for EET for the SAA experiments was calculated from the emission spectrum (S1 f S0) of one Chl and the absorption spectrum (S1 f Sn) of the second Chl. The latter was estimated using the transient absorption spectrum of 1*Chl1-py (Figure 4), as described earlier.59 The orientation factor, κ2, was calculated assuming that both the donor Chl and acceptor Chl exhibit free rotation about the ethynyl group of the 20-position phenylethynyl linkage. Using the relative orientations of the donor and acceptor Chl’s for each pair, the average value of κ2 was calculated using rotation matrix methods,60,61 which are outlined in the Supporting Information. Given the rotational freedom about the phenylethynyl axes, the calculated values of κ2 are very close to those of a orientationally averaged system (κ2 ) 2/3).55 Using the input parameters given in Table 4, the Fo¨rster energy transfer lifetimes were computed using PhotochemCAD.62 The 150 ps calculated lifetime (Table 4) for the para pathway is about a factor of 2 faster than the

measured ∼350 ps EET time constant for Chl4-py, while the 20 and 34 ps calculated lifetimes for the ortho and meta pathways are both slower than the ∼7 ps measured lifetime. Distance dependence plays a critical role in determining Fo¨rster energy transfer rates, as evident from eq 8. If the Fo¨rster mechanism were solely responsible for the observed EET rates, then the diverse Chl-Chl distances for the ortho, meta, and para pathways (16.9, 21.5, and 28.5 Å, respectively) should result in a diverse set of observed rates. The fact that the calculated rates differ from the observed rates suggests that the Fo¨rster mechanism is not the only EET mechanism in these molecules and/or the Fo¨rster model is not appropriate in this case. Concerning the former possibility, through-bond, Dextertype,58 exchange-driven energy transfer is frequently invoked for short distance EET. It is evident that the measured EET time constants for the ortho and meta pathways are both faster than those predicted by the Fo¨rster model. However, the number of bonds between the Chl’s in the meta and para pathways is comparable, and the pyrene HOMO and LUMO orbital coefficients are comparable at all the positions to which Chl’s are attached.63 Given these facts, and noting that the measured EET time constants of the ortho/meta vs para pathways differ by about a factor of 50, it is unlikely that Dexter transfer is the root cause for the observed fast EET times for the ortho/meta pathways. Deviations from the predictions of the Fo¨rster model at close interchromophore distances are frequently due to limitations in the dipole-dipole approximation.64,65 At close distances, the length of the transition dipole becomes comparable to the distance between the chromophores, so that Fo¨rster theory is no longer an adequate model. However, deviations of the measured EET time constants from the predictions of Fo¨rster theory occur at all distances, even for the para pathway, where the dipole-dipole approximation is most likely valid. One possible reason for these differences may be that the Chl rotational conformations deviate from a flat distribution, which could result in stronger dipole-dipole coupling. Conclusions A series of fixed distance Chlx-py multichlorophyll arrays were synthesized, and EET time constants were determined. The three possible EET pathways within Chl4-py give rise to two observed EET times, which correlate generally with the predictions of the Fo¨rster EET model. However, deviations from this model are observed that most likely result from a breakdown of the model, rather than from significant contributions from Dexter-type energy transfer. This study shows that multiple EET pathways within complex chromophore arrays can be probed in detail using molecular models that afford control over interchromophore distances. It is also evident that further control over transition moment motions even at overall fixed distances would afford enhanced mechanistic information regarding EET. Our results indicate that EET between nonadjacent chromophores having high oscillator strengths, such as the para Chl’s in Chl4-py, is observable. Although the EET rates of nonadjacent pathways are significantly slower than those of adjacent pathways (∼50-fold slower in the case of para vs meta/ ortho EET), the ability to effectively funnel all energy to a desired location is important. By directing even the minor nonadjacent pathway energy (35% para contribution vs 65% meta/ortho contribution in the case of Chl4-py EET) toward an explicit energy trap, no unnecessary energy losses are incurred from a system’s inherent design. Therefore, the utilization of nonadjacent pathways may provide additional avenues for efficient light harvesting in future artificial photosynthetic systems.

11942

J. Phys. Chem. C, Vol. 113, No. 27, 2009

Acknowledgment. This work was supported by the Chemical Sciences, Geosciences, and Biosciences Division, Office of Basic Energy Sciences, DOE, under Grant No. DE-FG0299ER14999. Supporting Information Available: Experimental details including synthesis, fluorescence quantum yields, absorption and emission spectra, and transient absorption data. This material is available free of charge via the Internet at http://pubs.acs.org. References and Notes (1) Blankenship, R. E. Molecular Mechanisms of Photosynthesis; Blackwell Science: Oxford, 2002. (2) van Grondelle, R. Biochim. Biophys. Acta 1985, 811, 147–195. (3) Wasielewski, M. R. J. Org. Chem. 2006, 71, 5051–5066. (4) Calzaferri, G.; Lutkouskaya, K. Photochem. Photobiol. Sci. 2008, 7, 879–910. (5) Kilsa, K.; Kajanus, J.; Martensson, J.; Albinsson, B. J. Phys. Chem. B 1999, 103, 7329–7339. (6) Aratani, N.; Osuka, A.; Cho, H. S.; Kim, D. J. J. Photochem. Photobiol., C 2002, 3, 25–52. (7) Seth, J.; Palaniappan, V.; Johnson, T. E.; Prathapan, S.; Lindsey, J. S.; Bocian, D. F. J. Am. Chem. Soc. 1994, 116, 10578–10592. (8) Nakamura, Y.; Aratani, N.; Osuka, A. Chem. Soc. ReV. 2007, 36, 831–845. (9) Anderson, S.; Anderson, H. L.; Bashall, A.; McPartlin, M.; Sanders, J. K. M. Angew. Chem., Int. Ed. 1995, 34, 1096–1099. (10) Hindin, E.; Forties, R. A.; Loewe, R. S.; Ambroise, A.; Kirmaier, C.; Bocian, D. F.; Lindsey, J. S.; Holten, D.; Knox, R. S. J. Phys. Chem. B 2004, 108, 12821–12832. (11) Larsen, J.; Bruggemann, B.; Polivka, T.; Sundstrom, V.; Akesson, E.; Sly, J.; Crossley, M. J. J. Phys. Chem. A 2005, 109, 10654–10662. (12) Katz, J. J.; Shipman, L. L.; Cotton, T. M.; Janson, T. R. In The Porphyrins, Volume V, Phys. Chem. Part C; Dolphin, D., Ed.; Academic Press: New York, 1978; pp 401-458. (13) Deisenhofer, J.; Epp, O.; Miki, K.; Huber, R.; Michel, H. J. Mol. Biol. 1984, 180, 385–398. (14) Ferreira, K. N.; Iverson, T. M.; Maghlaoui, K.; Barber, J.; Iwata, S. Science 2004, 303, 1831–1838. (15) Song, H.-e.; Kirmaier, C.; Schwartz, J. K.; Hindin, E.; Yu, L.; Bocian, D. F.; Lindsey, J. S.; Holten, D. J. Phys. Chem. B 2006, 110, 19131– 19139. (16) Song, H.-e.; Kirmaier, C.; Yu, L.; Bocian, D. F.; Lindsey, J. S.; Holten, D. J. Phys. Chem. B 2006, 110, 19121–19130. (17) Taniguchi, M.; Ra, D.; Kirmaier, C.; Hindin, E.; Schwartz, J. K.; Diers, J. R.; Knox, R. S.; Bocian, D. F.; Lindsey, J. S.; Holten, D. J. Am. Chem. Soc. 2003, 125, 13461–13470. (18) Hindin, E.; Kirmaier, C.; Diers, J. R.; Tomizaki, K.-Y.; Taniguchi, M.; Lindsey, J. S.; Bocian, D. F.; Holten, D. J. Phys. Chem. B 2004, 108, 8190–8200. (19) Muthiah, C.; Kee, H. L.; Diers, J. R.; Fan, D.; Ptaszek, M.; Bocian, D. F.; Holten, D.; Lindsey, J. S. Photochem. Photobiol. 2008, 84, 786– 801. (20) van Grondelle, R.; Novoderezhkin, V. I. Phys. Chem. Chem. Phys. 2006, 8, 793–087. (21) van Grondelle, R.; Dekker, J. P.; Gillbro, T.; Sundstrom, V. Biochim. Biophys. Acta 1994, 1187, 1–65. (22) Sasaki, S.-i.; Mizutani, K.; Kunieda, M.; Tamiaki, H. Tetrahedron Lett. 2008, 49, 4113–4115. (23) Sasaki, S.-i.; Omoda, M.; Tamiaki, H. Photochem. Photobiol. A 2004, 162, 307–315. (24) Huber, V.; Sengupta, S.; Würthner, F. Chem.sEur. J. 2008, 14, 7791–7807. (25) Scholes, G. D.; Jordanides, X. J.; Fleming, G. R. J. Phys. Chem. B 2001, 105. (26) Kelley, R. F.; Goldsmith, R. H.; Wasielewski, M. R. J. Am. Chem. Soc. 2007, 129, 6384–6385. (27) Kelley, R. F.; Tauber, M. J.; Wasielewski, M. R. Angew. Chem., Int. Ed. 2006, 45, 7979–7982. (28) Kelley, R. F.; Tauber, M. J.; Wasielewski, M. R. J. Am. Chem. Soc. 2006, 128, 4779–4791.

Gunderson et al. (29) Worcester, D. L; Michalski, T. J; Katz, J. J Proc. Natl. Acad. Sci. U. S. A. 1986, 83, 3791–3795. (30) Bowman, M. K.; Michalski, T. J.; Tyson, R. L.; Worcester, D. L.; Katz, J. J. Proc. Natl. Acad. Sci. U. S. A. 1988, 85, 1498–1502. (31) Tamiaki, H.; Amakawa, M.; Holzwarth, A. R.; Schaffner, K. Photosynth. Res. 2002, 71, 59–67. (32) Prokhorenko, V. I.; Holzwarth, A. R.; Mueller, M. G.; Schaffner, K.; Miyatake, T.; Tamiaki, H. J. Phys. Chem. B 2002, 106, 5761–5768. (33) Roeger, C.; Mueller, M. G.; Lysetska, M.; Miloslavina, Y.; Holzwarth, A. R.; Wu¨rthner, F. J. Am. Chem. Soc. 2006, 128, 6542–6543. (34) Huber, V.; Katterle, M.; Lysetska, M.; Wu¨rthner, F. Angew. Chem., Int. Ed. 2005, 44, 3147–3151. (35) Fo¨rster, T. Ann. Phys. (Leipzig) 1948, 2, 55–75. (36) Fo¨rster, T. Z. Naturforsch. 1949, A4, 321–327. (37) Fo¨rster, T. In Modern Quantum Chemistry, Part III; Sinanoglu, O., Ed.; Academic Press: New York, 1965; pp 93-137. (38) Jones, D. M.; Lang, M. J.; Nagasawa, Y.; Joo, T.; Fleming, G. J. Phys. Chem. 1996, 100, 12660–12673. (39) Hwang, I.-W.; Ko, D. M.; Ahn, T. K.; Yoon, Z. S.; Kim, D.; Peng, X.; Aratani, N.; Osuka, A. J. Phys. Chem. B 2005, 109, 8643–8651. (40) Min, C.-K.; Joo, T.; Yoon, M.-C.; Kim, C. M.; Hwang, Y. H.; Kim, D.; Aratani, N.; Yoshida, N.; Osuka, A. J. Chem. Phys. 2001, 114, 6750– 6758. (41) Bruggemann, B.; Herek, J. L.; Sundstrom, V.; Pullerits, T.; May, V. J. Phys. Chem. B 2001, 105, 11391–11394. (42) Valkunas, L.; Trinkunas, G.; Liuolia, V.; Grondelle, R. v. Biophys. J. 1995, 69, 1117–1129. (43) Smith, K. M.; Goff, D. A.; Simpson, D. J. J. Am. Chem. Soc. 1985, 107, 4946–4954. (44) Kenner, G. W.; McCombie, S. W.; Smith, K. M. J. Chem. Soc., Perkin Trans. 1 1973, 2517–2523. (45) Sonogashira, K.; Tohda, Y.; Hagihara, N. Tetrahedron Lett. 1975, 50, 4467–4470. (46) Tougerti, A.; Negri, S.; Jutand, A. Chem.sEur. J. 2007, 13, 666– 676. (47) Ogino, K.; Iwashima, S.; Inokuchi, H.; Harada, Y. Bull. Chem. Soc. Jpn. 1965, 38, 473–477. (48) Lukas, A. S.; Miller, S. E.; Wasielewski, M. R. J. Phys. Chem. B 2000, 104, 931–940. (49) Pshenichnikov, M. S.; de Boerij, W. P.; Wiersma, D. A. Opt. Lett. 1994, 19, 572–575. (50) Lor, M.; De, R.; Jordens, S.; DeBlder, G.; Schweitzer, G.; Cotlet, M.; Hofkens, J.; Weil, T.; Herrmann, A.; Mullen, K.; Auweraer, M. V. D.; Schryver, F. C. D. J. Phys. Chem. A 2002, 106, 2083–2090. (51) Schweitzer, G.; Gronheid, R.; Jordens, S.; Lor, M.; Belder, G. D.; Weil, T.; Reuther, E.; Mullen, K.; Schyver, F. C. D. J. Phys. Chem. A 2003, 107, 3199–3207. (52) Metivier, R.; Kulzer, F.; Weil, T.; Mullen, K.; Basche, T. J. Am. Chem. Soc. 2004, 126, 14364–14365. (53) Hwang, I.-W.; Kamada, T.; Ahn, T. K.; Ko, D. M.; Nakamura, T.; Tsuda, A.; Osuka, A.; Kim, D. J. Am. Chem. Soc. 2004, 126, 16187–16198. (54) Trinkunas, G. J. Lumin. 2003, 102-103, 532–535. (55) Lakowicz, J. R. Principles of Fluorescence Spectroscopy; Kluwer: Dordrecht, 1999. (56) Hypercube Inc.: 1115 NW 4th Street, Florida 32601, USA, 1994. (57) Bradforth, S. E.; Jimenez, R.; van Mourik, F.; van Grondelle, R.; Fleming, G. R. J. Phys. Chem. 1995, 99, 16179–16191. (58) Dexter, D. L. J. Chem. Phys. 1953, 21, 836–850. (59) Kelley, R. F.; Lee, S. J.; Wilson, T. M.; Nakamura, Y.; Tiede, D. M.; Osuka, A.; Hupp, J. T.; Wasielewski, M. R. J. Am. Chem. Soc. 2008, 130, 4277–4284. (60) Van der Meer, B. W. ReV. Mol. Biotechnol. 2002, 82, 181–196. (61) Corry, B.; Jayatilaka, D.; Martinac, B.; Rigby, P. Biophys. J. 2006, 91, 1032–1045. (62) Du, H.; Fuh, R.-C. A.; Li, J.; Corkan, L. A.; Lindsey, J. S. Photochem. Photobiol. 1998, 68, 141–142. (63) Ruiz-Morales, Y. J. Phys. Chem. A 2002, 106, 11283–11308. (64) Braslavsky, S. E.; Fron, E.; Rodriguez, H. B.; San Roman, E.; Scholes, G. D.; Schweitzer, G.; Valeur, B.; Wirz, J. Photochem. Photobiol. Sci. 2008, 7, 1444–1448. (65) Khan, Y. R.; Dykstra, T. E.; Scholes, G. D. Chem. Phys. Lett. 2008, 461, 305–309.

JP902515P