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• W2784040638 abstract "•Method of observing spectral motions directly after femtosecond excitation•Observed synchronized fluctuations among electronic states in a protein complex•Observed correlated spectral motion between occupied and unoccupied excited states Observations of quantum coherence in photosynthetic complexes spawned a new field of quantum biology for the study of how biology exploits quantum dynamics. However, theoretical models have suggested that these signals may not arise from electronic dynamics but rather from simple molecular vibrations. The key question is whether different excited electronic states evolve in a correlated fashion after excitation. Here, we have developed two spectroscopic methods to provide experimental evidence that electronic states within a photosynthetic protein-pigment complex experience correlated fluctuations after excitation. Surprisingly, we found that the excitonic transitions in the Fenna-Matthews-Olson complex all undergo the same spectral motion after excitation despite having different degrees of delocalization and different local environments, etc. Such correlated spectral motion explains how quantum coherence among electronic states can persist for so long after femtosecond excitation. Early reports of long-lived quantum beating signals in photosynthetic pigment-protein complexes were interpreted to suggest that electronic coherence benefits from protection by the protein, but many subsequent studies have suggested instead that vibrational or vibronic contributions are responsible for the observed signals. Here, we devised two 2D-spectroscopy methods to observe how each exciton is perturbed by its nuclear environment in a photosynthetic complex. The first approach simultaneously monitors each exciton's energy fluctuations over time to obtain its time-dependent electronic-nuclear interactions. The second method isolates evidence of coupled interexcitonic environmental motions. The techniques are validated with Nile Blue A and subsequently used on the Fenna-Matthews-Olson (FMO) complex. The FMO data reveal that each exciton experiences nearly identical spectral motion after excitation and that spectral motion of one excited exciton induces similar motion on unpopulated neighboring excitonic states. These synchronized and correlated spectral dynamics prolong coherences in the FMO complex after femtosecond excitation. Early reports of long-lived quantum beating signals in photosynthetic pigment-protein complexes were interpreted to suggest that electronic coherence benefits from protection by the protein, but many subsequent studies have suggested instead that vibrational or vibronic contributions are responsible for the observed signals. Here, we devised two 2D-spectroscopy methods to observe how each exciton is perturbed by its nuclear environment in a photosynthetic complex. The first approach simultaneously monitors each exciton's energy fluctuations over time to obtain its time-dependent electronic-nuclear interactions. The second method isolates evidence of coupled interexcitonic environmental motions. The techniques are validated with Nile Blue A and subsequently used on the Fenna-Matthews-Olson (FMO) complex. The FMO data reveal that each exciton experiences nearly identical spectral motion after excitation and that spectral motion of one excited exciton induces similar motion on unpopulated neighboring excitonic states. These synchronized and correlated spectral dynamics prolong coherences in the FMO complex after femtosecond excitation. Photosynthesis depends on efficient electronic energy transfer through an array of pigment-protein complexes.1Vasmel H. van Dorssen R.J. de Vos G.J. Amesz J. Pigment organization and energy transfer in the green photosynthetic bacterium Chloroflexus aurantiacus: I. The cytoplasmic membrane.Photosynth. Res. 1986; 7: 281-294Crossref PubMed Scopus (42) Google Scholar Energy transfer requires perturbations from the environment, and the dephasing of coherent states generated within the system provides a sensitive probe of these dynamics.2Rebentrost P. Mohseni M. Kassal I. Lloyd S. Aspuru-Guzik A. Environment-assisted quantum transport.New J. Phys. 2009; 11: 033003Crossref Scopus (662) Google Scholar, 3Abramavicius D. Valkunas L. Role of coherent vibrations in energy transfer and conversion in photosynthetic pigment–protein complexes.Photosynth. Res. 2016; 127: 33-47Crossref PubMed Scopus (40) Google Scholar, 4Chenu A. Christensson N. Kauffmann H.F. Mančal T. Enhancement of vibronic and ground-state vibrational coherences in 2D spectra of photosynthetic complexes.Sci. Rep. 2013; 3https://doi.org/10.1038/srep02029Crossref PubMed Scopus (132) Google Scholar, 5Ishizaki A. Calhoun T.R. Schlau-Cohen G.S. Fleming G.R. Quantum coherence and its interplay with protein environments in photosynthetic electronic energy transfer.Phys. Chem. Chem. Phys. 2010; 12: 7319Crossref PubMed Scopus (281) Google Scholar, 6Chen X. Silbey R.J. Excitation energy transfer in a non-markovian dynamical disordered environment: localization, narrowing, and transfer efficiency.J. Phys. Chem. B. 2011; 115: 5499-5509Crossref PubMed Scopus (39) Google Scholar Dephasing occurs when a sample ensemble prepared in a coherent state is subject to random environmental perturbations.7Mukamel S. Principles of Nonlinear Optical Spectroscopy. Oxford University Press, 1995Google Scholar In general, dephasing can be slowed by reducing the temperature or physically separating the coherent states from their environments,8Ladd T.D. Jelezko F. Laflamme R. Nakamura Y. Monroe C. O’Brien J.L. Quantum computers.Nature. 2010; 464: 45-53Crossref PubMed Scopus (2264) Google Scholar but protein complexes in vivo cannot use either of these approaches. Nonetheless, some photosynthetic pigment-protein complexes display long-lived coherences, even at physiologic temperatures.9Panitchayangkoon G. Hayes D. Fransted K.A. Caram J.R. Harel E. Wen J. Blankenship R.E. Engel G.S. Long-lived quantum coherence in photosynthetic complexes at physiological temperature.Proc. Natl. Acad. Sci. USA. 2010; 107: 12766-12770Crossref PubMed Scopus (833) Google Scholar Microscopically, it has been hypothesized that correlated motions within the protein may explain this long-lived coherence.10Lee H. Cheng Y.C. Fleming G.R. Coherence dynamics in photosynthesis: protein protection of excitonic coherence.Science. 2007; 316: 1462-1465Crossref PubMed Scopus (890) Google Scholar Quantum coherences persisting on the timescale of energy transfer have been measured, leading to proposals that these systems enlist quantum dynamics to enhance their energy transport efficiencies.2Rebentrost P. Mohseni M. Kassal I. Lloyd S. Aspuru-Guzik A. Environment-assisted quantum transport.New J. Phys. 2009; 11: 033003Crossref Scopus (662) Google Scholar, 11Savikhin S. Struve W.S. Ultrafast energy transfer in FMO trimers from the green bacterium Chlorobium tepidum.Biochemistry. 1994; 33: 11200-11208Crossref PubMed Scopus (43) Google Scholar, 12Engel G.S. Calhoun T.R. Read E.L. Ahn T.-K. Mancal T.s. Cheng Y.-C. Blankenship R.E. Fleming G.R. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems.Nature. 2007; 446: 782-786Crossref PubMed Scopus (2447) Google Scholar, 13Fidler A.F. Caram J.R. Hayes D. Engel G.S. Towards a coherent picture of excitonic coherence in the Fenna–Matthews–Olson complex.J. Phys. B Mol. Opt. Phys. 2012; 45: 154013Crossref Scopus (28) Google Scholar, 14Plenio M.B. Huelga S.F. Dephasing-assisted transport: quantum networks and biomolecules.New J. Phys. 2008; 10: 113019Crossref Scopus (787) Google Scholar, 15Mohseni M. Rebentrost P. Lloyd S. Aspuru-Guzik A. Environment-assisted quantum walks in photosynthetic energy transfer.J. Chem. Phys. 2008; 129: 174106Crossref PubMed Scopus (904) Google Scholar, 16Ishizaki A. Fleming G.R. Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature.Proc. Natl. Acad. Sci. USA. 2009; 106: 17255-17260Crossref PubMed Scopus (687) Google Scholar More recent works suggest instead that the coherence signals result from the following: (1) pure vibrational states,17Tempelaar R. Jansen T.L.C. Knoester J. Vibrational beatings conceal evidence of electronic coherence in the FMO light-harvesting complex.J. Phys. Chem. B. 2014; 118: 12865-12872Crossref PubMed Scopus (61) Google Scholar, 18Plenio M.B. Almeida J. Huelga S.F. Origin of long-lived oscillations in 2D-spectra of a quantum vibronic model: electronic versus vibrational coherence.J. Chem. Phys. 2013; 139: 235102Crossref PubMed Scopus (113) Google Scholar, 19Tiwari V. Peters W.K. Jonas D.M. Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework.Proc. Natl. Acad. Sci. USA. 2013; 110: 1203-1208Crossref PubMed Scopus (407) Google Scholar (2) vibronic (mixed electronic-vibrational) states,20Christensson N. Kauffmann H.F. Pullerits T. Mančal T. Origin of long-lived coherences in light-harvesting complexes.J. Phys. Chem. B. 2012; 116: 7449-7454Crossref PubMed Scopus (341) Google Scholar, 21Caram J.R. Lewis N.H.C. Fidler A.F. Engel G.S. Signatures of correlated excitonic dynamics in two-dimensional spectroscopy of the Fenna-Matthew-Olson photosynthetic complex.J. Chem. Phys. 2012; 136: 104505Crossref PubMed Scopus (25) Google Scholar, 22Singh V.P. Westberg M. Wang C. Dahlberg P.D. Gellen T. Gardiner A.T. Cogdell R.J. Engel G.S. Towards quantification of vibronic coupling in photosynthetic antenna complexes.J. Chem. Phys. 2015; 142: 212446Crossref PubMed Scopus (24) Google Scholar or (3) pure electronic states experiencing correlated nuclear environments and/or non-Markovian vibrational perturbations.5Ishizaki A. Calhoun T.R. Schlau-Cohen G.S. Fleming G.R. Quantum coherence and its interplay with protein environments in photosynthetic electronic energy transfer.Phys. Chem. Chem. Phys. 2010; 12: 7319Crossref PubMed Scopus (281) Google Scholar, 23Hayes D. Wen J. Panitchayangkoon G. Blankenship R.E. Engel G.S. Robustness of electronic coherence in the Fenna–Matthews–Olson complex to vibronic and structural modifications.Faraday Discuss. 2011; 150: 459-469Crossref PubMed Scopus (56) Google Scholar, 24Abramavicius D. Mukamel S. Exciton dynamics in chromophore aggregates with correlated environment fluctuations.J. Chem. Phys. 2011; 134: 174504Crossref PubMed Scopus (63) Google Scholar, 25Caycedo-Soler F. Chin A.W. Almeida J. Huelga S.F. Plenio M.B. The nature of the low energy band of the Fenna-Matthews-Olson complex: vibronic signatures.J. Chem. Phys. 2012; 136: 155102Crossref PubMed Scopus (41) Google Scholar, 26Wu J. Liu F. Ma J. Silbey R.J. Cao J. Efficient energy transfer in light-harvesting systems: quantum-classical comparison, flux network, and robustness analysis.J. Chem. Phys. 2012; 137: 174111Crossref PubMed Scopus (69) Google Scholar Subtle details of these electronic-nuclear interactions govern the observed quantum dynamics. Here, we extract information from the third-order nonlinear response of the system by using two approaches: 2D single-time-domain exciton perturbation spectroscopy (2D-STEPS) and 2D time-resolved interexciton perturbation spectroscopy (2D-TRIPS). These optical, time-domain spectroscopies probe vibrational motion by examining correlated dynamics of each exciton's spectral motion. 2D-STEPS measures how excited-state nuclear motions systematically perturb individual excitonic transitions after excitation, whereas 2D-TRIPS probes how nuclear motions spawned by exciting one exciton affect other unoccupied excitonic states (Figure 1). In both approaches, three optical pulses are incident on the sample, resulting in a third-order signal. The 1–2, 2–3, and 3-signal pulse pairs are separated by the coherence (τ), waiting time (T), and rephasing time (t), respectively. The first pulse creates a quantum coherence |g〉〈ei| between the ith exciton and ground states, and also launches a wavepacket from the Franck-Condon position on the excited-state surface.27Silbey R. Electronic energy transfer in molecular crystals.Annu. Rev. Phys. Chem. 1976; 27: 203-223Crossref Google Scholar These coherences propagate according to exp(−iHgτ/h)|g〉〈ei|exp(iHeiτ/h) and the mismatch between Hei and Hg causes the system to evolve phase at the frequency ωei,g = ωei − ωg.7Mukamel S. Principles of Nonlinear Optical Spectroscopy. Oxford University Press, 1995Google Scholar The nuclear motions meanwhile perturb the corresponding excited-state transitions, causing ωei,g to fluctuate over time.27Silbey R. Electronic energy transfer in molecular crystals.Annu. Rev. Phys. Chem. 1976; 27: 203-223Crossref Google Scholar If individual complexes within the ensemble experience distinct perturbations, they will dephase. In contrast, systematic or synchronized motions of the excited-state energy gap will be detected. After this initial excitation, two subsequent pulses reverse the phase evolution of the system.7Mukamel S. Principles of Nonlinear Optical Spectroscopy. Oxford University Press, 1995Google Scholar The system once again evolves phase in the t domain, with a phase velocity determined by the difference of the states' frequencies involved in the coherences. 2D-STEPS measures the dependence of ωτ on τ to find the vibrational dynamics by using the ωt domain to sort the contributions from each exciton. This spectroscopy is sensitive only to dynamics on the excited-state surface. (For further discussion, see Figure 4 and Spectroscopy Overview.) In 2D-TRIPS, this time dependence is examined in both the τ and t domains. The nuclear motions of a chosen exciton i propagate for a duration τ′ in the τ domain, then the spectral motions of a distinct exciton j ≠ i are observed in the t domain. As τ′ advances, the effect on the spectral motion in t is observed. Dependencies observed between these two excitons indicate correlations between their nuclear environments. In this report, first the short-time Fourier-transform approach is validated with Nile Blue A as a model system. Subsequently, it is used on the Fenna-Matthews-Olson (FMO) complex of Chlorobaculum tepidum, which is known to exhibit long-lived coherences even at physiologic temperatures.9Panitchayangkoon G. Hayes D. Fransted K.A. Caram J.R. Harel E. Wen J. Blankenship R.E. Engel G.S. Long-lived quantum coherence in photosynthetic complexes at physiological temperature.Proc. Natl. Acad. Sci. USA. 2010; 107: 12766-12770Crossref PubMed Scopus (833) Google Scholar, 12Engel G.S. Calhoun T.R. Read E.L. Ahn T.-K. Mancal T.s. Cheng Y.-C. Blankenship R.E. Fleming G.R. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems.Nature. 2007; 446: 782-786Crossref PubMed Scopus (2447) Google Scholar FMO contains seven coupled bacteriochlorophyll a (BChl a) chromophores in a hydrophobic pocket, plus an eighth more weakly bound BChl a just outside the pocket, which functionally links the complex to the Chlorosome baseplate.28Tronrud D.E. Wen J. Gay L. Blankenship R.E. The structural basis for the difference in absorbance spectra for the FMO antenna protein from various green sulfur bacteria.Photosynth. Res. 2009; 100: 79-87Crossref PubMed Scopus (244) Google Scholar Coupling among these sites leads to several different excitonic states.29Hayes D. Engel G.S. Extracting the excitonic hamiltonian of the Fenna-Matthews-Olson complex using three-dimensional third-order electronic spectroscopy.Biophys. J. 2011; 100: 2043-2052Abstract Full Text Full Text PDF PubMed Scopus (66) Google Scholar Their nuclei also provide an array of vibrational modes,30Rätsep M. Freiberg A. Electron–phonon and vibronic couplings in the FMO bacteriochlorophyll a antenna complex studied by difference fluorescence line narrowing.J. Lumin. 2007; 127: 251-259Crossref Scopus (110) Google Scholar which couple to the electronic states to produce dephasing.7Mukamel S. Principles of Nonlinear Optical Spectroscopy. Oxford University Press, 1995Google Scholar The frequency evolution of the electronic state populations of FMO were analyzed by 2D-STEPS, as described in the Experimental Procedures. The signal is dominated by intense peaks near the selected ωt frequencies and evolves over τ′ (Figure 2). The distinct exciton peaks in these spectrograms exhibit synchronized spectral motions, which are reproducible in repeated experiments (Figures S6–S10). The power spectral densities of these peak motions contain frequency components at approximately 40, 120, 185, and 300 cm−1, which agree with vibrational frequencies of 46, 117, 167–202, and 284–291 cm−1, respectively, reported with fluorescence line-narrowing measurements of FMO.30Rätsep M. Freiberg A. Electron–phonon and vibronic couplings in the FMO bacteriochlorophyll a antenna complex studied by difference fluorescence line narrowing.J. Lumin. 2007; 127: 251-259Crossref Scopus (110) Google Scholar The frequency components of this spectral motion have been assigned to intramolecular vibrational modes within the chromophores, although the 40 cm−1 feature has been attributed either to phonon modes or vibrations of BChl a's acetyl tail.31Lee M.K. Coker D.F. Modeling electronic-nuclear interactions for excitation energy transfer processes in light-harvesting complexes.J. Phys. Chem. Lett. 2016; 7: 3171-3178Crossref PubMed Scopus (91) Google Scholar, 32Matsuzaki S. Zazubovich V. Rätsep M. Hayes J.M. Small G.J. Energy transfer kinetics and low energy vibrational structure of the three lowest energy qy-states of the Fenna-Matthews-Olson antenna complex.J. Phys. Chem. B. 2000; 104: 9564-9572Crossref Scopus (22) Google Scholar, 33Czarnecki K. Diers J.R. Cynwat V. Erickson J.P. Frank H.A. Bocian D.F. Characterization of the strongly coupled, low-frequency vibrational modes of the special pair of photosynthetic reaction centers via isotopic labeling of the cofactors.J. Am. Chem. Soc. 1997; 119: 415-426Crossref Scopus (68) Google Scholar, 34Schulze J. Kühn O. Explicit correlated exciton-vibrational dynamics of the FMO complex.J. Phys. Chem. B. 2015; 119: 6211-6216Crossref PubMed Scopus (34) Google Scholar Because the coherence time domain only accesses coherent superpositions of vibrational states on the excited-state surface (see the Experimental Procedure for further discussion), these frequency fluctuations are attributed to the excited-state vibrational motions. As a result of their delocalization, phonon modes may have an impact on the excitons collectively; but local vibrational motions should not. We therefore attribute the clear synchronized spectral motion to local modes acting independently on the seven BChl a chromophores to produce synchronized motions for the distinct excitons. For reference, the same treatment was applied to a Nile Blue A standard, confirming that it produces its own expected power spectral densities,35Fearey B.L. Carter T.P. Small G.J. Efficient nonphotochemical hole burning of dye molecules in polymers.J. Phys. Chem. 1983; 87: 3590-3592Crossref Scopus (41) Google Scholar, 36Miller S.K. Baiker A. Meier M. Wokaun A. Surface-enhanced Raman scattering and the preparation of copper substrates for catalytic studies.J. Chem. Soc. Faraday Trans. 1. 1984; 80: 1305-1310Crossref Google Scholar, 37Zhang Y. Hartmann S.R. Moshary F. Fluorescence-line-narrowing spectroscopy of nile blue in glass and polymer at 5 K: determination of a single-site line shape function.J. Chem. Phys. 1996; 104: 4371-4379Crossref Scopus (9) Google Scholar, 38Le Ru E.C. Schroeter L.C. Etchegoin P.G. Direct measurement of resonance Raman spectra and cross sections by a polarization difference technique.Anal. Chem. 2012; 84: 5074-5079Crossref PubMed Scopus (35) Google Scholar which are distinct from those in FMO. For a more detailed discussion of these Nile Blue A experiments, including narrower spectrogram windows and distinct waiting times, refer to Section S9 in the Supplemental Information. 2D-TRIPS uses a similar strategy to 2D-STEPS. However, 2D-TRIPS exploits multiple time domains to isolate evidence of interexcitonic vibrational motion during the coherence time and a subsequent time period. Using a time-ordered pulse sequence, we observe how propagation of one exciton's nuclear motions during the coherence time affects those of another exciton during the rephasing time. Because of its smaller time-domain range, the frequency resolution is lower in the short-time Fourier transform than in the standard Fourier transform. Therefore, exciton signals that are too close in energy overlap spectrally, and this overlap obscures their distinct contributions. We therefore focus primarily on excitons 1 and 7 for this analysis, because their energies are separated by approximately 500 cm−1 (other combinations are shown in Figure S11). Exciton 7 is selected in the τ domain and allowed to propagate for a designated duration τ′. Subsequently, the t domain spectrogram is obtained, and its exciton 1 cross-peak fluctuations are observed as a function of both τ′ and t′. This process is repeated with systematic variation of τ′, to observe any dependence of the spectral fluctuations in t′ on τ′. For uncorrelated nuclear environments, no dependence would be observed. Figure 3 displays 2D-TRIPS spectrograms for excitons 1 and 7. It resolves two peak fluctuation cycles occurring over the first 600 fs of t′. Although the first cycle fluctuates as expected when it is distinguishable (e.g., τ′ = 140 and 157.5 fs), we do not focus on it here because inhomogeneous broadening contributions, which dominate the signal at low t′,7Mukamel S. Principles of Nonlinear Optical Spectroscopy. Oxford University Press, 1995Google Scholar contaminate the upper region of the spectrograms. However, the second fluctuation is well isolated and suitable for comparison with varying τ′. When τ′ increases, the phase of the spectral motion in the rephasing domain shifts by a nearly equivalent increment, indicating that spectral motion during the coherence time advances the phase of spectral motion of a different exciton later in time. The dashed, horizontal lines in Figure 3 indicate the phase progression of this second cycle with increasing τ′. The heatmap in Figure 3 shows that the phase progression is maintained even for smaller increments of τ′. The solid black line in the heatmap indicates the peak position. A horizontal black line would have indicated no correlation of the peak energy between t and τ; however, this sloped line represents a correlation of the nuclear phase between increasing τ and decreasing t. In essence, the vibrational motion in the rephasing domain inherits vibrational phase from the coherence time domain, although different excitons were excited in these two domains. The 2D-STEPS spectrograms display synchronized spectral motion of the excitons over much of the first picosecond. Because these spectrograms report dynamics in the coherence time domain, when only single excitations are allowed, these motions indicate that the ensemble trajectory for each exciton independently undergoes very similar dynamics following its initial excitation. These similar vibrational motions occur despite the different site compositions of the excitons. The excitons are delocalized over a number of sites described by their inverse participation ratios, which span 1.28–2.54 in FMO.39Cho M. Vaswani H.M. Brixner T. Stenger J. Fleming G.R. Exciton analysis in 2D electronic spectroscopy.J. Phys. Chem. B. 2005; 109: 10542-10556Crossref PubMed Scopus (368) Google Scholar As a result, some are nearly monomeric, while others are nearly trimeric. Furthermore, previous work has shown that vibrational modes arise from intermolecular coupling between bacteriochlorophylls.19Tiwari V. Peters W.K. Jonas D.M. Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework.Proc. Natl. Acad. Sci. USA. 2013; 110: 1203-1208Crossref PubMed Scopus (407) Google Scholar Therefore, after excitation with a short laser pulse, a given exciton will exhibit synchronized nuclear motions across the ensemble;40Cina J.A. Kovac P.A. Jumper C.C. Dean J.C. Scholes G.D. Ultrafast transient absorption revisited: phase-flips, spectral fingers, and other dynamical features.J. Chem. Phys. 2016; 144: 175102-175119Crossref PubMed Scopus (43) Google Scholar but the motions of distinct excitons can diverge over time. It is therefore not a given that FMO's excited states would exhibit these synchronized vibrational oscillations over a picosecond. Nonetheless, the 2D-STEPS results indicate that the excitons experience synchronized nuclear perturbations over this duration. Therefore, even before invoking particular effects, such as correlated nuclear environments, non-Markovian fluctuations, or vibronic states, when a coherent superposition of excited states is generated in 2D spectroscopy,9Panitchayangkoon G. Hayes D. Fransted K.A. Caram J.R. Harel E. Wen J. Blankenship R.E. Engel G.S. Long-lived quantum coherence in photosynthetic complexes at physiological temperature.Proc. Natl. Acad. Sci. USA. 2010; 107: 12766-12770Crossref PubMed Scopus (833) Google Scholar, 12Engel G.S. Calhoun T.R. Read E.L. Ahn T.-K. Mancal T.s. Cheng Y.-C. Blankenship R.E. Fleming G.R. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems.Nature. 2007; 446: 782-786Crossref PubMed Scopus (2447) Google Scholar the excitons' spectral motion will remain synchronized over approximately the first picosecond because of their independently similar vibrational motions. Thus, in an ultrafast 2D experiment, electronic coherences may be prolonged in FMO as a result of synchronized nuclear fluctuations, even without invoking correlated nuclear environments, for suitably broadband coherent light capable of generating superpositions of electronic and vibrational excited states in FMO. This duration coincides with the relevant timescale for energy transfer in FMO,9Panitchayangkoon G. Hayes D. Fransted K.A. Caram J.R. Harel E. Wen J. Blankenship R.E. Engel G.S. Long-lived quantum coherence in photosynthetic complexes at physiological temperature.Proc. Natl. Acad. Sci. USA. 2010; 107: 12766-12770Crossref PubMed Scopus (833) Google Scholar, 11Savikhin S. Struve W.S. Ultrafast energy transfer in FMO trimers from the green bacterium Chlorobium tepidum.Biochemistry. 1994; 33: 11200-11208Crossref PubMed Scopus (43) Google Scholar and prolonged coherences have been reported to enhance transport efficiencies.14Plenio M.B. Huelga S.F. Dephasing-assisted transport: quantum networks and biomolecules.New J. Phys. 2008; 10: 113019Crossref Scopus (787) Google Scholar, 15Mohseni M. Rebentrost P. Lloyd S. Aspuru-Guzik A. Environment-assisted quantum walks in photosynthetic energy transfer.J. Chem. Phys. 2008; 129: 174106Crossref PubMed Scopus (904) Google Scholar In addition to this effect, the results from 2D-TRIPS indicate coupling between the nuclear motions of distinct excitons, suggesting an additional mechanism to enhance coherence lifetimes. These correlated interexcitonic nuclear environments increase the critical temperature for the transition of coherent-to-incoherent energy transport.41Nazir A. Correlation-dependent coherent to incoherent transitions in resonant energy transfer dynamics.Phys. Rev. Lett. 2009; 103: 146404Crossref PubMed Scopus (157) Google Scholar Coherences lasting hundreds of femtoseconds in FMO at room temperature have been observed previously,9Panitchayangkoon G. Hayes D. Fransted K.A. Caram J.R. Harel E. Wen J. Blankenship R.E. Engel G.S. Long-lived quantum coherence in photosynthetic complexes at physiological temperature.Proc. Natl. Acad. Sci. USA. 2010; 107: 12766-12770Crossref PubMed Scopus (833) Google Scholar which is consistent with this additional explanation. In terms of Redfield theory,3Abramavicius D. Valkunas L. Role of coherent vibrations in energy transfer and conversion in photosynthetic pigment–protein complexes.Photosynth. Res. 2016; 127: 33-47Crossref PubMed Scopus (40) Google Scholar these correlated motions will reduce the nuclear damping. Coupling between numerous harmonic oscillators can also induce synchrony, so exploring whether this mechanism applies to the vibrational modes in FMO represents a promising future direction.42Kuramoto Y. Chemical Oscillations, Waves, and Turbulence. Springer, 1984Crossref Google Scholar, 43Strogatz S.H. From Kuramoto to Crawford: exploring the onset of synchronization in populations of coupled oscillators.Physica D. 2000; 143: 1-20Crossref Scopus (2055) Google Scholar After femtosecond excitation, the FMO complex exhibits both synchronized and correlated excitonic nuclear environments. 2D-STEPS reveals similar spectral motion for each exciton after femtosecond excitation so that, even before considering interexcitonic vibrational correlations, superpositions of these excitons propagate in common for at least 1 ps at 77 K. Furthermore, 2D-TRIPS provides direct evidence that one exciton's spectral motion affects a distinct exciton's nuclear dynamics. These properties result from embedding multiple identical chromophores, with the same intramolecular vibrational modes, in close proximity within the protein scaffold. Taken together, these data provide three key insights into the origins of long-lived coherence in photosynthetic systems: first, the common response of the chromophores ensures that the excited state spectral motions will be synchronized after femtosecond excitation; second, estimating the spectral diffusion without subtracting the synchronized motion dramatically overestimates the system-bath coupling; third, nuclear motions on one exciton do affect the energy gap of other excitons, which will favor coherent energy-transfer mechanisms.16Ish" @default.
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• W2784040638 title "Correlated Protein Environments Drive Quantum Coherence Lifetimes in Photosynthetic Pigment-Protein Complexes" @default.
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