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Mimicking Photosynthetic Two-Step Energy Transfer in Cyanine Triads Assembled into Capsules Zhifei Dai, Lars Da¨hne,* Edwin Donath, and Helmuth Mo¨hwald Max-Planck Institute of Colloids and Interfaces, D-14424 Golm, Germany Received January 11, 2002 A two-step energy transfer cascade was constructed in the wall of hollow microcapsules by means of defined assembly of three cyanine dyes, thiacyanine (antenna), thiacarbocyanine (receiver and antenna), and indodicarbocyanine (receiver), in the wall plane and perpendicular to it. The efficiency of the energy transfer steps has been measured by fluorescence spectroscopy. The unidirectional energy transfer perpendicular to the surface was smaller than for the lateral one. The antenna dyes on the outer surface of the capsules harvest the light energy and conduct it downhill by Fo¨rster resonance energy transfer to the capsule interior in analogy to chloroplasts in nature. However, the obtained efficiency is much smaller, though some improvement was reached by using J-aggregate-forming dyes.
Biomimetic systems’ blueprint has inspired the conception of artificial light-harvesting antenna systems for applications in solar energy conversion, optoelectronics, photonics, sensor design, and other areas of nanotechnology based on biological paradigms.1 The strategy employed by nature is to capture sunlight over a wide spectral range in chromophore arrays and then funnel the energy unidirectionally through several dye aggregates to the photosynthetic reaction center.2 The juxtaposition of chromophores tunes their electronic interactions, which govern both their absorptive/emissive properties and the kinetics of energy transfer.3 One approach to mimic this type of behavior involves covalent linkage of chromophores, but the synthesis becomes very demanding for increasing complexity of such systems.3 The approach of nature, to use self-organization of chromophores to aggregates in protein matrixes, promises more success.4 Similar but simpler self-organization processes are used in the layer-by-layer self-assembly (LbL) technique of oppositely charged polyelectrolytes. It permits the construction of nanoscale devices and semibiological hybrids.5 Recently, we have demonstrated that dyes can be introduced into polyelectrolyte capsules as noncovalently linked guest molecules by a variation of the LbL technique.6 Such capsules are produced by alternating deposition of 10 layers of poly(styrenesulfonate, sodium salt) (PSS, Mw ) 70 000 g/mol) and poly(allylamine hydrochloride) (PAH, Mw ) 60 000 g/mol, Aldrich) on spherical melamine formaldehyde resin particles (Microparticles GmbH), followed by removal of the templating cores. The capsules (1) (a) Gust, D.; Moore, T. A.; Moore, A. L. Acc. Chem. Res. 2001, 34, 40. (b) Wasielewski, M. R. Chem. Rev. 1992, 92, 435. (c) Bach, U.; Lupo, D.; Comte, P.; Moser, J. E.; Weisso¨, F.; Salbeck, J.; Spreitzer, H.; Gra¨tzel, M. Nature 1998, 395, 583. (2) McDermott, G.; Prince, S. M.; Freer, A. A.; HawthornthwaiteLawless, A. M.; Papiz, M. Z.; Cogdell, R. J.; Isaacs, N. W.; et al. Nature 1995, 374, 517. (3) (a) Kaschak, D. M.; Lean, J. T.; Waraksa, C. C.; Saupe, G. B.; Usami, H.; Mallouk, T. E. J. Am. Chem. Soc. 1999, 121, 3435. (b) Scholes, G. D.; Jordanides, X. J.; Fleming, G. R. J. Phys. Chem. B 2001, 105, 1640. (4) (a) Fossum, R. D.; Fox, M. A. J. Am. Chem. Soc. 1997, 119, 1197. (b) Balzani, V.; Campagna, S.; Denti, G.; Juris, A.; Serroni, S.; Venturi, M. Acc. Chem. Res. 1998, 31, 26. (d) Borja, M.; Dutta, P. K. Nature 1993, 362, 43. (5) (a) Decher, G. Science 1997, 277, 1232. (b) Donath, E.; Sukhorukov, G. B.; Caruso, F.; Davis, S. A.; Mo¨hwald, H. Angew. Chem., Int. Ed. 1998, 37, 2202. (c) Caruso, F.; Caruso, R.; Mo¨hwald, H. Science 1998, 282, 1111. (6) (a) Dai, Z. F.; Voigt, A.; Leporatti, S.; Donath, E.; Da¨hne, L.; Mo¨hwald, H. Adv. Mater. 2001, 13, 1339.
Scheme 1. Molecular Structure of the Cyanine Dyes TC, TCC, and IDCC and Energy Transfer Pathways for the Antenna System
have a wall thickness of 15-20 nm, a diameter of 1 µm, and a positive surface charge.7 Different components can be assembled within one layer or along the radial direction.5,6 One-step energy transfer has been demonstrated several times in these systems.8 In a pioneering work, an energy transfer cascade was prepared in flat LbL films using chromophore-labeled polyelectrolytes.3 However, for final applications as light-harvesting antenna systems, spherical devices with a large photosensitive surface area and a redox-active core have to be used in analogy to chloroplasts in photosynthesis. The polyelectrolyte capsules have the potential for the construction of such advanced microspheres. We prepared noncovalently linked multichromophoric assemblies in the walls of polyelectrolyte capsules for the demonstration of lateral and unidirectional radial two-step Fo¨rster resonance energy transfer (FRET). The model system studied here involves an energy transfer cascade consisting of three negatively charged cyanine dyes (Scheme 1), electrostatically associated with the capsule surface.5,6 Cyanines are chosen as model systems because they have high absorption coefficients and fluorescence quantum yields. Noncovalently linked cyanine triads, which consist of thiacyanine (TC, antenna), (7) Leporatti, S.; Voigt, A.; Mitlo¨hner, R.; Sukhorukov, G. B.; Donath, E.; Mo¨hwald, H. Langmuir 2000, 16, 4059. (8) Gao, C. Y.; Moya, S.; Lichtenfeld, H.; Casoli, A.; Fiedler, H.; Donath, E.; Mo¨hwald, H. Macromol. Mater. Eng. 2001, 286, 355.
10.1021/la0255222 CCC: $22.00 © 2002 American Chemical Society Published on Web 05/09/2002
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Langmuir, Vol. 18, No. 12, 2002
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Table 1. Fluorescence Intensities (in au ) photons per second/10 000, λexc ) 410 nm) of TC, TCC, and IDCC in Different Assemblies, Lateral and Radial, in the Capsule Walla fluorescence lateral
fluorescence radial
system
λ ) 485 nm
λ ) 590 nm
λ ) 675 nm
λ ) 485 nm
λ ) 590 nm
λ ) 675 nm
TC TCC + IDCC TC + TCC TC + IDCC TC + TCC + IDCC
340 0 117 108 37
0 0 342 0 64
0 0 0 7 50
340 0 98 95 30
0 0 236 0 52
0 0 0 3 5
a
Concentrations of each dye were kept constant: 5 × 10-5 M for TC, 6 × 10-7 M for IDCC, and 6 × 10-7 M for TCC (ref 12).
Figure 1. Fluorescence spectra (λexc ) 410 nm) of the cyanine triads of TC, TCC, and IDCC coadsorbed on the surface of hollow capsules: (a) TC concentration was varied from 0 to 1 × 10-4 M, while the concentrations of TCC and IDCC were kept constant at 6 × 10-7 M; (b) the TCC concentration was varied from 0 to 2.4 × 10-6 M, while the concentrations of TC and IDCC were kept constant at 5 × 10-5 M and 6 × 10-7 M, respectively. The insets show the fluorescence intensities as functions of the TC and TCC concentrations, respectively: dotted line, 480 nm; dashed line, 590 nm; solid line, 675 nm.
thiacarbocyanine (TCC, receiver and antenna), and indodicarbocyanine (IDCC, receiver), are assembled on the surface capsules in order to achieve lateral energy transfer inside the layer. For an energy transfer across the capsule wall, the dyes were stepwise assembled with PAH into a sandwich structure along the radial direction of the capsules. TC forms J-aggregates upon adsorption on PAH (λabs ) 465 nm),9 whereas TCC and IDCC are adsorbed as monomers. The absorption maxima of TC, TCC, and IDCC are completely separated from one another, permitting selective excitation of each dye (410 or 465 nm for TC, 565 nm for TCC, and 645 nm for IDCC). The fluorescence spectra of TC at 485 nm and TCC at 590 nm (Figure 1a) have some overlap with the absorption spectra of TCC and IDCC. This is the prerequisite for an efficient FRET.3 Thus, the fluorescence from IDCC at 675 nm can result from either direct excitation of IDCC in the red, from excitation of TCC in the green followed by energy transfer step 2 to IDCC, or from excitation of TC in the blue and direct energy transfer 3 to IDCC or via TCC (1 + 2, Scheme 1). The formation of a J-aggregate of the donor, in which very fast coherent energy transfer takes place,10 and the rather long singlet excited-state lifetime of the acceptor (τIDCC ∼ 232 ps) should make the TC-TCC-IDCC energy transfer cascade very efficient. (9) Kometani, N.; Nakajima, H.; Asami, K.; Yonezawa, Y.; Kajimoto, O. J. Phys. Chem. B 2000, 104, 9630.
For all experiments, an excitation wavelength of 410 nm was used. Only TC shows a strong J-aggregate fluorescence, while TCC and IDCC are only very weakly excited. Quantitative fluorescence data for different dye combinations are given in the table. The FRET steps 1 and 2 were investigated separately by varying the concentration of the two participating dyes. The energy transfer from TCC to IDCC 2 shows the usual efficiency given by the dye ratio and the overlap integral between donor fluorescence and acceptor absorption. However, FRET step 1 from TC to TCC proceeds very efficiently. Even at a high excess of TC, the fluorescence of its J-aggregates is quenched strongly by 70% and a high TCC fluorescence is observed. The reason may be the extraordinary property of J-aggregates to conduct energy rapidly and coherently via up to 60 molecules to an acceptor.10 Also, nature uses such aggregates in the antenna systems.4 To prove the two-step (1 + 2) energy transfer, two dyes were adsorbed on the surface of the capsules and titrated with the third dye. For example, the concentrations of TCC and IDCC were kept constant at 6 × 10-7 M while the TC concentration was varied from 0 to 1 × 10-4 M (Figure 1a).12 In absence of TC, the sum of direct excitation of TCC and FRET 2 to IDCC as well as direct excitation of IDCC yielded negligible fluorescence. Addition of TC leads to a characteristic triple-peaked fluorescence demonstrating efficient FRET from TC to TCC and IDCC. Maximal fluorescence was observed for IDCC at 3.75 × 10-5 M TC and for TC and TCC at 6.25 × 10-5 M TC (Figure 1a, inset). Addition of IDCC to a constant ratio of TC and TCC yielded optimal FRET at 6 × 10-7 M IDCC. A higher concentration results in self-quenching of IDCC. In the third experiment, the TCC concentration was varied from 0 to 2.4 × 10-6 M while optimal concentrations of TC (5 × 10-5 M) and IDCC (6 × 10-7 M) were taken (Figure 1b). In the absence of TCC, IDCC is excited to a small extent showing that direct FRET 3 takes place (Table 1). Nevertheless, increasing TCC concentration results in 7-fold enhanced IDCC fluorescence and extensively quenched TC fluorescence up to the optimal concentration of TCC (6 × 10-7 M). This proves clearly the two-step energy transfer 1 + 2. In addition, the strong quenching of the TCC fluorescence, induced by FRET 1, in the presence of IDCC confirms this result very well. Hence, the main contribution of the IDCC fluorescence comes from the two-step FRET pathway. As shown, lateral two-step energy transfer occurs efficiently when cyanine triads are deposited in a single (10) Fidder, H.; Knoester, J.; Wiersma, D. A. J. Phys. Chem. 1991, 95, 7880. (11) Da¨hne, L.; Leporatti, S.; Donath, E.; Mo¨hwald, H. J. Am. Chem. Soc. 2001, 123, 5431. (12) The concentration values are given for a constant volume of dye solutions added to a constant amount of capsules. After adsorption, the capsules were washed with water and the loss of dye molecules was controlled. The dyes were almost completely adsorbed. Only very high TC concentrations lead to a saturation of adsorption and a loss of dyes.
Letters
PAH layer of capsules. For unidirectional FRET across the capsule wall, we assembled the cyanine triads separately sandwiched into PAH layers along the radial direction of capsules with different dye concentrations and different distances between the dye layers, but the efficiency of the lateral energy transfer could not be reached (Table 1). Generally, the smaller dimensionality of the FRET in the radial arrangement reduces the efficiency remarkably. A further reason might be difficulties in controlling the concentration ratio between the dyes. To avoid interpenetration or diffusion of the dyes through the separating layers as a reason for the FRET, the experiments were repeated with dyes covalently linked to the polyelectrolytes. The quite similar results point to the real downhill energy transfer perpendicular across the wall of capsules. Two-step energy transfer downhill was demonstrated for the first time in polyelectrolyte capsules. Although the advantage of the LbL method, to adjust the distances between chromophores according to the requirements of FRET, has been exploited, the efficiency of the desired FRET through the wall was much smaller than for the
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lateral one. Nevertheless, the antenna dyes on the surface of the capsules harvest the light energy and transfer it across the wall to the capsule center. One can envisage that optimized capsules of this type can funnel light energy from the outside to the interior, where photochemical initiators11 or semiconductor nanoparticles can induce chemical reactions in these micrometer-sized cages. The utilization of biology-based ideas to design artificial photosynthetic nanostructures opens the door to research and possible applications in both biotechnology and information technology. Future efforts will be directed toward optimizing the energy transfer efficiencies by finetuning the layer distances and polarity as well as by varying the actual layer constituents. Taking the lightharvesting system of nature as a model, the formation of J-aggregates of all three dyes may improve the FRET further. Acknowledgment. We thank BASF and the Fonds der Chemischen Industrie for financial support. LA0255222
