Letter pubs.acs.org/JPCL
Excitonic and Vibrational Coherence in the Excitation Relaxation Process of Two LH1 Complexes as Revealed by Two-Dimensional Electronic Spectroscopy Fei Ma,*,† Long-Jiang Yu,‡,§ Ruud Hendrikx,† Zheng-Yu Wang-Otomo,‡ and Rienk van Grondelle† †
Department of Physics and Astronomy, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, 1081 HV Amsterdam, The Netherlands ‡ Faculty of Science, Ibaraki University, Mito, Ibaraki 310-8512, Japan § Research Institute for Interdisciplinary Science, Okayama University, 3-1-1 Tsushima Naka, Okayama 700-8530, Japan S Supporting Information *
ABSTRACT: Ultrafast excitation relaxation within a manifold exciton state and longlived vibrational coherence are two universal characteristics of photosynthetic antenna complexes. In this work, we studied the two-dimensional electronic spectra of two core light-harvesting (LH1) complexes of Thermochromatium (Tch.) tepidum, native Ca2+LH1 and modified Ba2+-LH1. The role of the vibrational coherence in the exciton relaxation was revealed by comparing the two LH1 with similar structures but different electronic properties and by the evolution of the exciton and vibrational coherence as a function of temperature.
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chains.18 As a result, it possesses the best thermal stability among all the LH1 complexes. The lowest excited-state absorption of BChl a (Qy) is at 915 nm (Figures 1B and S1), significantly redder than most BChl a-containing LH1s of other purple bacteria. When Ba2+ substitutes for Ca2+, it binds only the α chain,19 leading to an inhomogeneity of site energies between the α- and β-BChl a. The Qy absorption is blue-shifted to 893 nm. Reversible LH1 → RC EET is the last and ratelimiting step of the overall EET processes in purple bacteria.21,22 We recently compared the trapping and detrapping rates between Ca-LH1-RC and Ba-LH1-RC by 2DES, and big differences were found: trapping is (70/64 ps)−1 at RT and (235/47 ps)−1 at 77 K, whereas detrapping is (4.0/ 2.2 ps)−1 at RT and (9.3/4.0 ps)−1 at 77 K, for Ca-/Ba-LH1, respectively.23 The Ca-LH1 and Ba-LH1 are an excellent system to compare the excitonic and vibronic coherences, considering that although the majority of the structure (such as protein matrix and primary configuration of BChl a) is conserved, there are essential difference in the electronic properties. In Ca-LH1, the 32 BChl a molecules are rather homogeneous, whereas in BaLH1 they are alternating with an energy inhomogeneity of ∼550 cm−1.23 Thus, comparing the excitonic and vibrational coherence between Ca-LH1 and Ba-LH1 will provide
wo-dimensional electronic spectroscopy (2DES) has been employed for a variety of photosynthetic pigment− protein complexes.1−11 A universal feature observed in these complexes is the oscillatory dynamics which last up to a few picoseconds. Closely packed pigments have a large coupling strength and as a result form a dense set of exciton levels with relatively small energy gaps between the different levels. Electronic/excitonic coherences usually live for a few hundred femtoseconds.6,12,13 The long-lived oscillations mainly originate from coherent nuclear vibrations.8,10−13 Specific vibrational modes may couple with exciton states, leading to electronic transitions with a strong vibronic character. More and more evidence shows that these vibrational modes contribute to sustain the electronic/excitonic coherence.7,8,13−16 Recently, vibronic coupling was revealed that can redistribute absorption strength and as a result increase the energy-transfer (EET) rate.17 In this work, we studied the excitonic and vibronic coherence of two purple bacterial core complexes of Thermochromatium (Tch.) tepidum. Their recent crystal structures show that the reaction center (RC) is enclosed by the core light-harvesting antenna (LH1), and LH1 is a closed elliptical ring containing 16 heterodimers of the αβ-subunit and 32 bacteriochlorophyll (BChl) a molecules sandwiched between the rings of α and β polypeptides (Figure 1A).18,19 The LH1 of Tch. tepidum is unique because it can bind different metal cations and alter the transition energy of BChl a.20 In its native form, a Ca2+ binds at the C-terminal of each αβ-subunit and connects the α and β © XXXX American Chemical Society
Received: April 5, 2017 Accepted: June 6, 2017 Published: June 6, 2017 2751
DOI: 10.1021/acs.jpclett.7b00824 J. Phys. Chem. Lett. 2017, 8, 2751−2756
Letter
The Journal of Physical Chemistry Letters
can be attributed to rapid downhill energy migration, reflecting excitation redistribution and building up of a new equilibrium in the exciton manifold. Full width at half maximum (fwhm) along the diagonal (inhomogeneous) provides information on the degree of static disorder. The fwhm along antidiagonal (homogeneous) is related to the dephasing rate, γ.5,24−26 As can be seen in Figure 3, the diagonal widths of both Ca-LH1 and Ba-LH1 do not
Figure 1. (A) Supramolecular architecture of the two LH1-RC complexes of Tch. tepidum.2 Display strategy: dark green (dark blue) ball, α- (β-) polypeptide; yellow (red) balls, Ca2+ (Ba2+); green, special pair (P) in RC. (B) RT linear absorption spectra of Ca-LH1-RC (red) and Ba-LH1-RC (blue), normalized with regard to the carotenoid absorption bands at 550 nm. The spectrum of the excitation pulse is shown in black, and the detection range in the experiment is limited within the gray dashed lines.
Figure 3. Evolution of the antidiagonal fwhm (A), diagonal fwhm (B), and line shape (C) as a function of the population time (T). Oneexponential fittings and time constants are also shown in panel C. Color code: Ca-LH1 at RT, orange; Ba-LH1 at RT, navy; Ca-LH1 at 77 K, red; and Ba-LH1 at 77 K, blue.
information on how the interactions between pigments and between pigment and the protein bath control the coherences and thereby the energy-transfer properties.24,25 The room-temperature (RT) 2D real (for phasing, see Figure S2) spectra are shown in Figure 2 (for 77 K spectra, see Figure S3). The most prominent difference between the two complexes is that in Ba-LH1, the ground-state bleaching (GSB) signal contains two sub-bands along the diagonal (see Figure S4 for a clear view). As discussed in a previous study,23 they are attributable to lower-energy α-BChl a and high-energy β-BChl a, respectively. In both complexes, the GSB amplitude drops significantly and the GSB shape becomes more round during the first 100 fs. Because the broadening of the GSB (especially along the antidiagonal direction) can be regarded as the growth of cross peaks, the ultrafast line shape dynamics thus
change much with the population time, reflecting a constant structure of the exciton manifold, whereas the antidiagonal widths increase significantly at early time reflecting relaxation in the exciton manifold and then remain unchanged after 200 fs. The 2D line shape is defined as the ratio of the antidiagonal to the diagonal fwhm. The evolution of this line shape was fitted with a single exponential rise, and the time constants obtained are very close: 57 and 58 fs for Ca-LH1 and 57 and 55 fs for BaLH1 at RT and 77 K, respectively. A 5% error can be estimated because of the large amplitude of oscillations superimposed on the time profile. Therefore, within the error level, the time constants for the four cases are uniform. The line shape dynamics reflects a loss of correlation among the exciton states due to the exciton−exciton and exciton−bath interactions;
Figure 2. RT 2D real spectra of Ca-LH1-RC (top) and Ba-LH1-RC (bottom) at the indicated population times (T). λτ and λt are excitation and detection wavelengths, respectively. 2752
DOI: 10.1021/acs.jpclett.7b00824 J. Phys. Chem. Lett. 2017, 8, 2751−2756
Letter
The Journal of Physical Chemistry Letters
Figure 4. 77 K population time dynamics of Ca-LH1 (A) and Ba-LH1 (B). Color code: black, diagonal GSB; green, ESA; pink, below-diagonal cross peak. See also the solid circles in Figure 2. The inset shows the oscillations obtained by subtraction exponential decay. Normalized population time dynamics (C) and the FFT spectra of their oscillations (D). Color code is the same as in Figure 3. *1 and *2 in panel D correspond to the two dominant oscillation frequencies, 110 and 190 cm−1, respectively.
nearly opposite signal signs (Figure 4A,B). This cross peak represents the excitation transfer into the lowest (k = 0) exciton state.23 Therefore, this observation may indicate that the phase changes by ∼180° from the FC to the newly formed equilibrium excited state. A ∼90° phase change found in the different positions of the LH2 cross peak was attributed to two EET pathways (from the B800 k = +1 and k = −1 states to B850) with antiphases acting in concert to optimize the transfer efficiency.6 The oscillatory pattern in the ESA signal also exhibits nearly reversed signal signs compared to that in the GSB signal. A similar phenomenon found in chlorosomes was explained by the fact that the oscillatory ESA originates from the vibrational coherences in the excited state while oscillatory GSB comes from the vibrational coherences in the ground state, and the vibrational coherences in the excited states and in the ground states are antiphase.31 These assignments can explain all our observations, as both the ESA and cross peak represent the wavepacket population in the excited state. At RT, the same phenomena are not as clear as at 77 K. The oscillations last for longer than 1 ps, both at 77 K and RT (Figures 4C). The dominant frequencies are ∼110 and ∼190 cm −1 for both complexes (Figure 4D). Similar frequencies were observed in several LH1 and LH2 complexes, via pump−probe, three-pulse photon echo, transient grating, and 2DES spectroscopies.7,32−34 In some of these measurements other frequencies such as 560 and 750 cm−1 also appeared; however, they are not clear in this work. These >1 ps coherences are much longer than that of pure exciton coherence, 177 fs, indicating that they originate from nuclear coherence. Furthermore, the amplitudes of the oscillations are high, implying that they are due to vibrations coupled to the exciton states.14 Therefore, the two modes are attributable to vibronic coherence. All the GSB, ESA, and cross peaks contain these oscillations; therefore, it is difficult to distinguish if these modes are ground- or excited-state vibrations, although groundand excited-state vibrational coherence in principle differ in dephasing rates: excited-state coherences dephase completely, while the ground state may dephase only partially.35 We
therefore, this time constant can be used to estimate the excitonic dephasing time (proportional to γ−1). This result is surprising because our previous work found that in Ba-LH1 the electronic coupling between BChl a monomers is weaker and the delocalization length is shorter than that in Ca-LH1,27 which is not beneficial for sustaining electronic/excitonic coherence, so a shorter coherence lifetime was expected for Ba-LH1. The temperature independence of LH1 is different from the case of chlorosomes, for which the time constants increases from 36 fs at 77 K to 45 fs at RT.10 The population dynamics at the GSB maximum are shown in Figure 4A. The ultrafast decay is attributable to the relaxation of the Franck−Condon (FC) excited-state population (Γ), and the picosecond-scale decay corresponds to the detrapping process.23 This ultrafast (
