Letter pubs.acs.org/JPCL
Coherent Vibronic Coupling in Light-Harvesting Complexes from Photosynthetic Marine Algae G. H. Richards,† K. E. Wilk,‡ P. M. G. Curmi,‡ H. M. Quiney,¶ and J. A. Davis*,†,§ †
Centre for Atom Optics and Ultrafast Spectroscopy, and §ARC Centre of Excellence for Coherent X-ray Science, Swinburne University of Technology, Victoria 3122, Australia ‡ School of Physics and Centre for Applied Medical Research, St. Vincents Hospital, The University of New South Wales, Sydney, New South Wales 2052, Australia ¶ School of Physics and ARC Centre of Excellence for Coherent X-Ray Science, The University of Melbourne, Victoria 3010, Australia S Supporting Information *
ABSTRACT: Observations of long-lived coherences in photosynthetic lightharvesting complexes utilize short pulses with broad spectral bandwidths to coherently excite multiple transitions and coherent superpositions. In order to identify the role that such quantum effects might play in efficient energy transfer, however, an alternative approach is required. We have developed a technique for two-color photon echo spectroscopy to selectively excite the pathway of interest and measure its evolution in the absence of any other excitation. We use this technique to excite a coherence pathway in phycocyanin-645 from cryptophyte algae and measure the dynamics of this coherence. A decoherence time of 500 fs was measured, and clear signatures for strong coupling between the electronic states and phonon modes were observed, allowing coherent coupling between otherwise nonresonant transitions. This provides detailed experimental evidence of the long-lived coherences and the nature of the quantum mechanical interactions between electronic states and phonon modes in phycocyanin-645 from cryptophyte marine algae. SECTION: Kinetics, Spectroscopy
T
for the role of quantum effects in photosynthetic energy transfer remains elusive. The identification of long-lived coherences in photosynthetic light-harvesting systems has relied on being able to resolve beating of amplitudes and/or peak shapes in two-dimensional (2D) electronic spectroscopy. This type of multidimensional spectroscopy, with ultrashort, broad bandwidth pulses, has become an important tool for identifying dynamics of energy transfer in a range of complex systems.17−22 The use of broadband pulses, while giving this technique much of its capability, also presents some limitations. In complex systems, for example, there are often competing pathways that generate signals that are partially or completely overlapped in the 2D spectrum.23 This makes it difficult to isolate different processes and analyze the dynamics or peak shapes that provide insight into the interactions within the system. More importantly, broadband excitation can resonantly excite many different transitions within the bandwidth, which can alter the relative contributions of different interactions and relaxation pathways compared to excitation of individual states.23,24 In relation to
he role of quantum effects in photosynthesis has been a subject of great speculation since the first observations of long-lived coherences in light-harvesting complexes.1−4 The initial theoretical models showed that quantum coherence, by itself, actually reduces the efficiency of energy transfer, but by including some dephasing, the combination of quantum tunnelling and noise leads to highly efficient energy transfer.5−11 Part of the reason for this enhanced transfer efficiency is that the dephasing caused by a Markovian bath of phonon modes leads to spectral broadening, which brings otherwise nonresonant transitions into resonance.8,11 Subsequent studies looked at the effect of spatial correlations of the phonon interactions12 and non-Markovian dynamics of the system− bath interactions.13−15 The conclusions of these studies point to a regime where the separation of the system and bath is not clear, and it is necessary to include both electronic states and vibrational modes within the description of the system. The form of the interactions between vibrational and electronic states and assumptions made about the phonon spectral density have been shown to significantly alter the calculated dynamics.16 Experimental details of the interactions between electronic states and the vibrational/phonon modes of the chromophores and surrounding protein matrix remain lacking. Similarly, beyond the observation of long-lived coherent coupling between exciton states, any experimental evidence © 2012 American Chemical Society
Received: December 6, 2011 Accepted: January 6, 2012 Published: January 7, 2012 272
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Figure 1. The pathways in (a−d) show the coherence pathways primarily excited in the two-color experiment described. In this representation, each arrow represents an interaction with a laser pulse, and the labels on the interior represent the state of the system; g is the ground state, a and b are excited electronic states, and the prime represents a higher vibrational level. (a,b) Pathways involving coherences between excited states; (c,d) equally valid pathways involving vibrational coherences.
Figure 2. (a) The structure of PC645. The chromophores are represented as space-filling models with the DBVs, PCBs, and MBVs colored in blue, yellow and green, respectively. The polypeptide backbone is represented as a cartoon with the two β chains colored cyan and red while α1 and α2 are shown in magenta and green, respectively. A transparent rendering of the protein surface colored by a contact potential envelops the structure. (b) The absorption spectrum for PC645.
the incident laser pulses. This is equivalent to coherent Raman scattering, except that the third pulse may also interact with an electronic coherence instead of scattering from a vibrational coherence. The pathways responsible for generating such a signal are depicted in Figure 1. By varying the delay of the third pulse, we are then able to probe the dynamics of the coherence generated by the first two pulses. In these experiments, after the first two pulses, the system can be thought of as being in a coherent superposition of states. For the coherent third-order signal to be generated, these superpositions must remain coherent.31 The signature of coherent coupling between excited electronic states or between vibrational levels is therefore simply the presence of any signal for values of T, the delay between the second and third pulse, beyond the pulse overlap regime. We do not expect to see beating at the difference frequency, as is the case in 2D spectroscopy, because the two pulses of different wavelength come from two optical parametric amplifiers (OPAs) that are not phase-stabilized, meaning the phase of the superposition varies from shot to shot of the laser. If, however, there is coherent excitation of another superposition, either by coherence transfer or phonon-assisted excitation by a laser pulse, then beating as a function of T at the difference frequency will be present and detectable in the spectrally resolved intensity measurement. (See Supporting Information for further details.) In principle, such a process should also generate signal at a different wavelength determined by the new coherence frequency. This signal would, however, be a small contribution to an already weak signal and quadratically dependent on the amplitude of the coherence. In contrast,
photosynthesis and the role of quantum effects, exciting all transitions will naturally lead to beating at each of the difference frequencies for as long as the states remain coupled and coherent with respect to each other. While this is ideal for identifying long-lived coherent superpositions, it can hide details of the interactions within and between exciton states and vibrational modes. These coherent superpositions of excited states remain coherent for several hundred femtoseconds despite the shortlived nature, 800 fs, clearly beyond the nearly transform limited pulse duration of 80 fs. This signal directly represents the evolution of the coherence between the DBV+ and MBV states without any competing signals, interactions, or relaxation pathways resulting from the simulataneous excitation of other states. By integrating the data as a function of emission energy, ωt , and delay between the first two pulses, τ, the one-dimensional plot of the signal as a function of T, shown in Figure 3b, is obtained. This is well-fitted by a single-exponential decay to give a dephasing time of 500 ± 70 fs. There are likely two
Figure 3. Evolution of the coherence between DBV+ and MBV states. (a) The spectrally resolved intensity as a function of waiting time shows the signal extending beyond 800 fs. Oscillations of the intensity can also be seen. (b) By integrating across the spectral domain, a dephasing time of 500 ± 70 fs is obtained. The fit is a singleexponential decay, with an offset of 80 fs to account for the pulse overlap effects within this region.
contributions to this dephasing, the pure decoherence of the superposition and the dephasing due to the inhomogeneous distribution of energy differences between the excited states. Experiments in other light-harvesting complexes have measured similar values at 77 K with the influence of inhomogeneity35 and longer values where the influence of inhomogeneity is minimal.26,35 Previous experiments in PC645 have been unable to determine an accurate decoherence time.4,32 Further analysis of Figure 3 and the data recorded at different τ delays shows that there is some modulation of the signal intensity as a function of T. By Fourier transforming the complete data set with respect to T, the power spectrum as a function of ωT can be represented in a 3D plot, as shown in Figure 4a. This figure plots the power spectrum along ωT as a function of τ and ωt. In addition to the intense broad signal around ωT = 0, there are three other regions where significant amplitude is seen. By integrating over all values of τ, the location and relative intensities of these signals can be seen more clearly (Figure 4b). This reveals three peaks corresponding to energy differences of 22 ± 2, 40 ± 2, and 74 ± 8 meV. In order to verify that these peaks are real, the experiments were repeated four times over different days and slightly different conditions, as described in the Experimental Methods section. On each occasion, the same three peaks were observed, as shown in the Supporting Information. The peak at 22 meV may arise due to the simultaneous excitation of an additional state by one of the laser pulses. Its location at 22 meV is not much beyond the pulse bandwidth and, as shown in Figure 4, overlaps slightly with the signal peaked at ωT = 0. It is possible that this peak at 22 meV may be 274
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4, suggesting that both peaks are due to beating with this DBV− state. The indirect coherent excitation of this state could be due to coherence transfer mediated by a phonon or by phononassisted absorption of the laser pulses. Either process could excite the DBV− transition and generate the two beat frequencies and would involve (a) a 2.179 eV photon and the emission of a 74 meV phonon and (b) a 2.066 eV photon and the absorption of a 40 meV phonon. The indirect excitation of the DBV− transition via pathway (a) will have a definite phase relationship with the laser pulse at 2.179 eV and the DBV+ state, leading to beating as a function of T, corresponding to the energy difference between the two DBV states, ∼74 meV. Similarly, the indirect excitation of the DBV− transition via pathway (b) will have a definite phase relationship with the laser pulse at 2.066 eV and the MBV state, leading to beating between the DBV− and MBV states at ∼40 meV. In order for these processes to occur, it is essential that phonon modes with the matching energy exist. Calculated spectral densities of similar phycobiliproteins show a continuum of states up to and beyond 800 cm−1 (100 meV). This ensures that there are sufficient phonon modes to couple with the electronic transitions and indirectly excite the DBV− transition. In addition to the broad phonon bath, there are also likely to be more localized vibrational modes associated with the individual chromophores. In principle, the experiments described here could equally be exciting vibrational coherences related to these modes rather than coherences between excited electronic states. Turner et al.32 were able to compare contributions to the data from rephasing and nonrephasing pathways to show that the major contribution to the long-lived coherence in PC645 is from electronic coherences. In the present work, we are not able to make such comparisons because the increased pulse duration means that the rephasing and nonrephasing pathways are overlapped and inseparable. As a result, we cannot definitively rule out the possibility that the signals that we observe are due to vibrational coherences. In the current experiment, it is likely that involvement of vibrational coherences occurs within the excited electronic state. This is due to the lack of enforced phase stability between our excitation pulses, which excludes the possibility of beating between transitions in the coherent ground-state Raman pathway. Furthermore, the transition energies involved in generating the signals reported here are very similar to those identified previously,4,32 suggesting that we are exciting the same electronic transitions. Regardless of whether the excited states involved are purely electronic or vibronic in nature, strong coupling with the phonon modes brings nonresonant transitions into resonance and establishes coherent coupling between the two states. In the present experiments, we are unable to conclusively determine whether this coherent coupling is established by the phonon-assisted transition excited by the laser pulse or as a result of coherent tranfer from the directly excited transitions. The strong coupling with the phonon modes does, however, suggest that coherent transfer by this mechanism is possible. If the states that we observe to be coupled are different vibronic levels within the same chromophore, there would, at first glance, appear to be little significance for quantum coherent energy transfer. The strong phonon coupling to these states and subsequent coherent coupling between them does, however, provide an intrinsically quantum mechanical mechanism for exploring the manifold of vibrational levels to
Figure 4. (a) Fourier transforming the data in Figure 3 with respect to T reveals three frequency components contributing to the oscillations in the signal. (b) By integrating the data over τ, the relative amplitude of the different contributions can be seen.
due to the energy difference between the two MBV states, where one is resonant with the second pulse (2.06 eV) and the other is excited by the low-energy edge of the same pulse. Quantum chemical calculations that have been performed on the basis of different assumptions34,36,37 have determined energy differences between these two states from 6 to 50 meV, a range that includes the 24 meV seen here. It is also possibile that such a signal may arise from simultaneous coherent excitation of two vibrational modes within the bandwidth, as has been observed previously in carotenoids.38 The peaks at values of ωT equal to 40 and 74 meV are, however, far outside of the pulse bandwidth and cannot arise from a state directly excited by either of the laser pulses. The implication, therefore, is that some other transition is being coherently excited by an indirect process. For example, the absorption of a photon from either laser pulse could be combined with the emission or absorption of a phonon to drive a transition to an electronic state not directly resonant with the laser field. This could allow coherent indirect excitation of an additional state(s) shifted in energy by 40 and 74 meV from either of the directly excited states. In the work of Collini et al.,4 another state at 2.11 eV, attributed to the DBV− state, is identified between DBV+ and MBV states. The energy differences that they determine, 74 meV between DBV+ and DBV− and 39 meV between MBV and DBV−, are in remarkable agreement with the energies identified in Figure 275
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enhance the Förster spectral overlap and resonant energy transfer between the spatially separated states. Recent theoretical treatments of energy transfer in similar light-harvesting complexes indicated that the electronic and vibrational states of the chromophores and protein matrix are intrinsically linked, and for a full understanding of energy transfer in such systems, they cannot be arbitrarily separated.13−16 We have provided experimental confirmation that strong coupling between electronic excited states and phonon modes is present and can lead to coherent couping between nonresonant electronic states in the PC645 complex from cryptophyte algae. The implications of this flow directly from the theory, where the balance of quantum coupling and interactions with phonon modes can lead to efficient energy transfer due to enhanced spectral overlap and the ability to find the most efficient pathway. These observations were made possible by the coherencespecific technique described here, and extensions of this technique to study all of the different transitions across the absorption spectrum and the dependence on temperature, wavelength, and polarization will provide a detailed picture of the states involved, the nature of the vibronic coupling, and the precise mechanisms for efficient energy transfer in the lightharvesting complexes. Finally, while clear evidence of coherence transfer remains elusive, the results presented here strongly support the available theoretical modeling, which suggests that the long-lived quantum coherences observed previously are not merely a trivial phenomenon and that such quantum effects play an important role in light harvesting in cryptophyte algae.
Letter
ASSOCIATED CONTENT
S Supporting Information *
A mathematical description of the pathways responsible for generating the signal is presented, showing where beating is expected to be visible in the spectrally resolved intensity measurements without phase stability described here. The results from the each of the repeated scans are also shown to support the repeatability of these experiments and the matching features that appear each time that the experiment is repeated. This material is available free of charge via the Internet at http://pubs.acs.org.
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected].
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ACKNOWLEDGMENTS The authors wish to thank the Australian Research Council for financial support.
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REFERENCES
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EXPERIMENTAL METHODS PC645 was purified from Chroomonas sp. CCMP270, as described previously.4 The buffer solution with the lightharvesting complexes was diluted 70:30 v/v with glycerol and placed in a quartz cell with a 0.2 mm path length. The sample was cooled to 77 K using an Oxford Instruments cryostat (Optistat). The two-color transient four-wave mixing experiments were performed with the output from two OPAs pumped by the same titanium/sapphire amplifier. The first pulse, with wavevector k1 and wavelength 570 nm, came from one OPA, and the other two pulses with wavevectors k2 and k3 and wavelength 601 nm came from the other OPA. The signal emitted in the k4 = −k1 + k2 + k3 direction was passed through a spectrometer (SPEX270) and spectrally resolved on a CCD (JY3000). The data in Figure 3 were obtained by fixing the delay between the first two pulses to 0 fs and scanning the delay, T. To obtain the complete set of data as a function of τ, T, and ωt, the delay between the first two pulses, τ, was scanned from −200 to 200 fs in 10 fs steps for a fixed value of T. This was repeated for values of T from 0 to 1000 fs in 20 fs steps. The order in which the data for the different values of T were acquired was randomized to eliminate the possibility that systematic fluctuations may be responsible for the oscillations in the data as a function of T. After each scan for a given value of T, the sample was moved to prevent damage, and the signal before and after the scan were compared to ensure that no damage occurred. To ensure consistency and repeatability of the results, the complete experiment was repeated four times over three different days, with the order in which the T points were taken different each time. The data presented here is the average of these four data sets. The results from the individual scans each show the same features and are presented in the Supporting Information. 276
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