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J. Phys. Chem. B 2000, 104, 1088-1096
Exciton Relaxation and Polaron Formation in LH2 at Low Temperature Toma´ sˇ Polı´vka, To˜ nu Pullerits, Jennifer L. Herek, and Villy Sundstro1 m* Chemical Physics, Lund UniVersity, P.O. Box 124, S-221 00 Lund, Sweden ReceiVed: May 18, 1999; In Final Form: NoVember 18, 1999
Excited state dynamics of antenna complexes in an LH2-only mutant of the purple bacterium Rb. sphaeroides have been investigated by means of two-color femtosecond spectroscopy combined with computer simulations. Measurements of transient absorption spectra revealed a new spectral band in the stimulated emission region around 880 nm at 6 K. To simulate this new dynamic feature that appears within the first 2 ps after light absorption, we have used a simplified polaron model via a decoupled red pigment within the B850 ring. Comparison of simulations and experiment suggests the following kinetic scheme: (1) initial ultrafast (∼100 fs) dynamics correspond to exciton relaxation to the lowest exciton state; (2) mixing of the lowest exciton state with charge-transfer states results in a relaxation to these states in about 600 fs; (3) picosecond dielectric relaxation in the charge-transfer states corresponding to polaron formation follows.
1. Introduction The primary photosynthetic machinery consists of lightharvesting (LH) antenna complexes and a so-called reaction center (RC). In the antenna, electronic excitations of pigment molecules are created by light absorption. A very fast excitation transfer follows. Within ∼100 ps, the excitation is trapped by the RC, where the energy is used to carry electrons from one side of the membrane to the other via a sequence of specially arranged pigment molecules.1 The progress made in dynamic and structural studies of these systems and processes has provided a general understanding of the underlying principles of natural light harvesting. At the same time, the detailed molecular level understanding of structure-function relationships in primary photosynthesis still suffers from a number of unresolved issues. In this article, we address one of these questions, the nature of the electronic excited states and their dynamics and coupling to the nuclear degrees of freedom in antennae of photosynthetic purple bacteria. All photosynthetic purple bacteria have a core antenna (LH1), which is believed to form a ring around the reaction center and absorbs light at about 870-880 nm. Species such as Rhodobacter (Rb.) sphaeroides, Rhodopseudomonas (Rps.) acidophila, and Rhodospirillum (Rs.) molischianum in addition have a peripheral antenna, LH2, characterized by two absorption bands. The corresponding pigments are called B800 and B850 according to their characteristic bacteriochlorophyll-a (BChl-a) Qy transition wavelengths. The high-resolution structures of LH2 from Rps. acidophila2 and Rs. molischianum3 have been obtained by X-ray crystallography. On the basis of the homology of the protein sequences of a variety of purple bacteria, it is generally believed that they all exhibit a very similar basic structure. The elementary building blocks of these antennae are Rβ-polypeptide pairs that bind two B850 and one B800 BChl molecules. In addition to those, there are one or two (depending on species) carotenoid molecules. In Rps. acidophila, these units form a nonamer ring, whereas LH2 of Rs. molischianum is an octamer. B800 and B850 BChl molecules of LH2 form two * Corresponding author. E-mail:
[email protected]. Fax: +46-46-2224119.
pigment rings. One of the most striking features of the structure is the dense packing of the B850 BChls, leading to a significant coupling between the transitions of molecular electronic states.4 During recent years, the nature of elementary excitations in the B850 ring has been a subject of extensive studies. Pullerits et al.5 simulated the isotropic and anisotropic decays in a ring of N ) 18 BChl molecules with spectral disorder as in B850. They found that for incoherent Fo¨rster energy transfer at room temperature, the anisotropy decay has to be at least 3 times longer than the isotropic decay when measured in the middle of the absorption band. Yet, the experimentally measured decays did not show the predicted dependence, strongly suggesting that the dynamics cannot be characterized as an excitation hopping among monomeric BChl molecules but rather reflects the behavior of a collective state of a number of pigment molecules. By analyzing the room-temperature transient absorption spectrum (TAS) 2 ps after excitation, Pullerits et al.5 concluded that the excitation is delocalized over four BChl molecules. In a subsequent study, it was found that the delocalization length Ne does not change substantially with temperature.6 In contrast, when the amount of photobleaching and induced absorption per absorbed photon has been used as a measure of the exciton delocalization length, much larger numbers close to the full ring size have been reported.7,8 On the other hand, when Monshouwer and co-workers9 measured the amount of B850 bleaching relative to the bleaching in the LH1 dimeric subunit B820, they concluded that the observed bleaching in LH2 corresponds to that expected for an exciton delocalized over 4 BChls. Also Kennis et al.10 compared the stimulated emission band of B850 with the optical signal of B800 and suggested that the exciton states are partly localized. A third and probably the most direct way of measuring the exciton delocalization length is the superradiance. Because of the collective nature of delocalized states, the square of the emitting dipole moments and consequently the radiative rates can be related to the delocalization length.11 Here, we point out that in the case of ring structures such as LH2, the superradiance does not give a unique answer to the extent of exciton delocalization since both Ne and N - Ne lead to the same radiative rate. Monshouwer et al.11 measured the intensity of
10.1021/jp9915984 CCC: $19.00 © 2000 American Chemical Society Published on Web 01/19/2000
Exciton Relaxation and Polaron Formation in LH2 superradiance from various samples and found that in B850 the radiative rate is 2.8 times larger than the rate in the B820 dimer. From the temperature dependence of the radiative rates and Monte Carlo simulations, they concluded that the delocalization length in B850 is about 3-4 pigments at room temperature. Thus, despite the lack of a general agreement, strong evidence is accumulating showing that the excited states in B850, at least at room temperature, have a rather localized character. Another interesting feature of the B850 band is its strong Stark effect, characterized mainly by a large change in polarizability.12 At the same time, Stark hole-burning measurements have shown that the dipole moment changes of the red wing of B850 is about the same as for monomeric BChl.13 The former observation has been thought to originate from mixing of charge transfer states with conventional exciton states, while the latter result may be due to a cancellation effect because of the headto-head arrangement of BChl molecules in B850. Simulations performed by Somsen et al. have also suggested that chargetransfer states may play an important role in the LH2 dynamics.14 The mismatch between calculated and experimental Stark spectra was explained by the presence of an additional state with charge-transfer character. A more rigorous explanation is yet to be developed. At low temperature, a new dynamic feature in the B850 TAS was observed by Chachisvilis et al.6 The stimulated emission/ bleaching band broadens and splits into two bands in about 3 ps. The new band is initially located at about 870 nm and moves further to the red and broadens on the time scale of tens of picoseconds. It was suggested to originate from stimulated emission from the lowest exciton state. Interestingly enough, in LH1 the effect is much less pronounced, if present at all. Early 4.2 K steady-state fluorescence measurements of a LH1less mutant of Rb. sphaeroides showed an unusually large Stokes' shift, which was explained by emission from a minor long-wavelength component of B850.15 On the other hand, from recent transient absorption data, it was suggested that the slower phases of this red-band B850 SE dynamics are due to energy transfer among the lowest exciton states of inhomogeneously distributed rings.16 The zero phonon hole action spectra have also been interpreted as to position the lowest exciton component of B850 at 870 nm.17 Exciton dynamics in LH2 antenna complexes of purple bacteria have been the subject of a number of recent works. There is general agreement that the initial relaxation within the B850 exciton band occurs in about 70-140 fs at both room and cryogenic temperatures. Such values were observed in LH2 complexes of both Rb. sphaeriodes6,16,18,19 and Rps. acidophila.20 Using 25 fs excitation pulses in a one-color pump-probe experiment Nagarajan et al.18 concluded that the initial phases of exciton dynamics can be as fast as 20-30 fs, based on anisotropy decays within the B850 band. These extremely fast processes were ascribed to a dephasing between the two most strongly allowed exciton states of B850. In addition, slower phases (>0.5 ps) of exciton dynamics within the LH2 complex have been observed at low temperatures. A ∼0.7 ps component observed by Vulto et al.20 in both isotropic and anisotropic decays in isolated LH2 complexes of Rps. acidophila at 7 K has been explained as due to the relaxation between exciton states of B850. On the other hand, a few slow components (0.8150 ps) observed in isotropic decays in LH2 complexes of Rb. sphaeroides have been assigned to inter-ring energy transfer.16 In this work, we address the origin of the slower relaxation processes (>0.5 ps) and the red emission in the LH2 antenna complexes. First we describe our experimental procedures and
J. Phys. Chem. B, Vol. 104, No. 5, 2000 1089 present a set of the most characteristic results. Subsequently, we outline our method of modeling the observed signals and compare the results of simulations with experiments. Finally, we discuss the discrepancies between experiment and simulations and draw conclusions. A preliminary account of this work has been published in the Proceedings of the EleVenth International Photosynthesis Congress.21 2. Materials and Methods Membranes of the LH2-only mutant DD13 of Rb. sphaeroides lacking the core complex were prepared according to ref 22 and dissolved in buffer solution (50 mM Tris, pH 8). The excited-state dynamics of the B850 band were studied by means of a two-color pump-probe technique. The experimental setup for these measurements is a femtosecond transient absorption spectrometer based on a mode-locked Ti:sapphire laser (Tsunami, Spectra Physics) operating at a repetition rate of 82 MHz and pumped by a CW argon ion laser (Spectra Physics). The ∼60 fs output pulses of this laser were directed to a regenerative Ti:sapphire amplifier (Spitfire, Spectra Physics) pumped by the second harmonic of a Q-switched Nd:YLF laser (Merlin, Spectra Physics) operating at a repetition rate of 5 kHz. The amplified pulses of ∼100 fs duration and approximately 300 µJ energy were divided into two paths: one to pump an optical parametric amplifier (TOPAS, Light Conversion) for generation of tunable pump pulses over a wide spectral range, and the other to produce white-light continuum probe pulses in a 1 cm sapphire plate. The resulting cross-correlation measured at the sample position was ∼100 fs, and the spectral width of the excitation pulses was about 150 cm-1. A detection system based on a three-diode arrangement in combination with a single grating monochromator was used as described in more detail in refs 6 and 23. The pump pulses were attenuated using neutral density filters to achieve excitation intensities of
