Hidden Vibronic and Excitonic Structure and Vibronic Coherence Transfer in the Bacterial Reaction Center
Veronica R. Policht, Andrew Niedringhaus, Rhiannon Willow, Philip D. Laible, David F. Bocian, Christine Kirmaier, Dewey Holten, Tomáš Mančal, Jennifer P. Ogilvie
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23 pages, 5 figures, submitted to Nature Communications
We report two-dimensional electronic spectroscopy (2DES) experiments on the bacterial reaction center (BRC) from purple bacteria, revealing hidden excitonic and vibronic structure. Through analysis of the coherent dynamics of the BRC we resolve specific coherent signatures that allow us to definitively assign the upper exciton energy of the "special pair." This assignment is supported by simulations of coherent dynamics of a reduced excitonic model of the BRC. The simulations also identify nonsecular vibronic coherence transfer processes neglected in standard models of photosynthetic energy transfer and charge separation. In addition, the coherent dynamics reveal multiple quasi-resonances between key intramolecular pigment vibrations and excited state energy gaps in the BRC. The functional significance of such electronic-vibrational resonances for photosynthetic energy transfer and charge separation remains an open question.
We recently proposed effective normal modes for excitonically coupled aggregates which exactly transform the energy transfer Hamiltonian into a sum of one-dimensional Hamiltonians along the effective normal modes. Identifying physically meaningful vibrational motions which maximally promote vibronic mixing suggested an interesting possibility of leveraging vibrational-electronic resonance for mediating selective energy transfer. Here we expand on the effective mode approach elucidating its iterative nature for successively larger aggregates, and extend the idea of mediated energy transfer to l…
Photosynthetic proteins have evolved over billions of years so as to undergo optimal energy transfer to the sites of charge separation. Based on spectroscopically detected quantum coherences, it has been suggested that this energy transfer is partially wavelike. This conclusion critically depends on assignment of the coherences to the evolution of excitonic superpositions. Here we demonstrate for a bacterial reaction centre protein that long-lived coherent spectroscopic oscillations, which bear canonical signatures of excitonic superpositions, are essentially vibrational excited state coherenc…
Nonlinear spectroscopy has revealed long-lasting oscillations in the optical response of a variety of photosynthetic complexes. Different theoretical models which involve the coherent coupling of electronic (excitonic) or electronic-vibrational (vibronic) degrees of freedom have been put forward to explain these observations. The ensuing debate concerning the relevance of either one or the other mechanism may have obscured their potential synergy. To illustrate this synergy, we quantify how the excitonic delocalization in the LH2 unit of Rhodopseudomonas Acidophila purple bacterium, leads to c…
The dynamical properties of exciton transfer coupled to polarization vibrations in a two site system are investigated in detail. A fixed point analysis of the full system of Bloch - oscillator equations representing the coupled excitonic - vibronic flow is performed. For overcritical polarization a bifurcation converting the stable bonding ground state to a hyperbolic unstable state which is basic to the dynamical properties of the model is obtained. The phase space of the system is generally of a mixed type: Above bifurcation chaos develops starting from the region of the hyperbolic state and…
The prevalence of long-lasting oscillatory signals in the 2d echo-spectroscopy of light-harvesting complexes has led to a search for possible mechanisms. We investigate how two causes of oscillatory signals are intertwined: (i) electronic coherences supporting delocalized wave-like motion, and (ii) narrow bands in the vibronic spectral density. To disentangle the vibronic and electronic contributions we introduce a time-windowed Fourier transform of the signal amplitude. We find that 2d spectra can be dominated by excitations of pathways which are absent in excitonic energy transport. This lea…
Until recently it was believed that photosynthesis, a fundamental process for life on earth, could be fully understood with semi-classical models. However, puzzling quantum phenomena have been observed in several photosynthetic pigment-protein complexes, prompting questions regarding the nature and role of these effects. Recent attention has focused on discrete vibrational modes that are resonant or quasi-resonant with excitonic energy splittings and strongly coupled to these excitonic states. Here we unambiguously identify excited state coherent superpositions in photosynthetic light-harvesti…
We demonstrate that the coupling of excitonic and vibrational motion in biological complexes can provide mechanisms to explain the long-lived oscillations that have been obtained in non linear spectroscopic signals of different photosynthetic pigment protein complexes and we discuss the contributions of excitonic versus purely vibrational components to these oscillatory features. Considering a dimer model coupled to a structured spectral density we exemplify the fundamental aspects of the electron-phonon dynamics, and by analyzing separately the different contributions to the non linear signal…
We introduce a heterodimer model in which multiple mechanisms of vibronic coupling and their impact on energy transfer can be explicitly studied. We consider vibronic coupling that arises through either Franck-Condon activity in which each site in the heterodimer has a local electron-phonon coupling and as Herzberg-Teller activity in which the transition dipole moment coupling the sites has an explicit vibrational mode-dependence. We have computed two-dimensional electronic-vibrational (2DEV) spectra for this model while varying the magnitude of these two effects and find that 2DEV spectra con…
In this work, we study the effects of non-Condon vibronic coupling on the quantum coherence of excitation energy transfer, via the exact dissipaton-equation-of-motion (DEOM) evaluations on excitonic model systems. Field-triggered excitation energy transfer dynamics and two dimensional coherent spectroscopy are simulated for both Condon and non-Condon vibronic couplings. Our results clearly demonstrate that the non-Condon vibronic coupling intensifies the dynamical electronic-vibrational energy transfer and enhances the total system-and-bath quantum coherence. Moreover, the hybrid bath dynamics…
A general theory of electronic excitations in aggregates of molecules coupled to intramolecular vibrations and the harmonic environment is developed for simulation of the third-order nonlinear spectroscopy signals. The model is applied in studies of the time-resolved two-dimensional coherent spectra of four characteristic model systems: weakly / strongly vibronically coupled molecular dimers coupled to high / low frequency intramolecular vibrations. The results allow us to classify the typical spectroscopic features as well as to define the limiting cases, when the long-lived quantum coherence…
Long-lived oscillations in 2D spectra of chlorophylls are at the heart of an ongoing debate. Their physical origin is either a multi-pigment effect, such as excitonic coherence, or primarily stems from localized vibrations. In the present work, we analyze distinguishing characteristics of relative phase difference measured between diagonal- and cross-peak oscillations. While direct discrimination between the two scenarios is obscured when peaks overlap, their sensitivity to temperature provides a stronger argument. We show that vibrational (vibronic) oscillations change relative phase with tem…
The primary steps of photosynthesis rely on the generation, transport, and trapping of excitons in pigment-protein complexes (PPCs). Generically, PPCs possess highly structured vibrational spectra, combining many discrete intra-pigment modes and a quasi-continuous of protein modes, with vibrational and electronic couplings of comparable strength. The intricacy of the resulting vibronic dynamics poses significant challenges in establishing a quantitative connection between spectroscopic data and underlying microscopic models. Here we show how to address this challenge using numerically exact si…
We present a study on the evolution of the Fenna-Matthews-Olson bacterial photosynthetic pigment-protein complex. This protein complex functions as an antenna. It transports absorbed photons - excitons - to a reaction center where photosynthetic reactions initiate. The efficiency of exciton transport is therefore fundamental for the photosynthetic bacterium's survival. We have reconstructed an ancestor of the complex to establish whether coherence in the exciton transport was selected for or optimized over time. We have also investigated on the role of optimizing free energy variation upon fol…
Vibronic Landscape of Excitons in Photosynthetic Antenna
Institute of Integrative Biology of the Cell, CEA, CNRS, Université Paris Saclay（细胞整合生物学研究所）；Laboratoire d’ingénierie des systèmes moléculaires, CNRS, Aix-Marseille University（分子系统工程实验室）；Department of Molecular Compound Physics, Centre for Physical Sciences and Technology（物理化学中心）
The idea that excitonic state (electronic) coherences are of fundamental importance to natural photosynthesis gained popularity when, a decade ago, slowly dephasing quantum beats were observed in the two-dimensional electronic spectra of the Fenna-Matthews-Olson complex at 77 K. These were assigned to quantum superpositions of excitonic states; a controversial interpretation, as the spectral linewidths suggested fast dephasing arising from strong interactions with the environment. While it has been pointed out that vibrational motion produces similar spectral signatures, concrete assignment of…
A vibronic-exciton model is applied to investigate the mechanism of enhancement of coherent oscillations due to mixing of electronic and nuclear degrees of freedom recently proposed as the origin of the long-lived oscillations in 2D spectra of the FMO complex [Christensson et al. J. Phys. Chem. B 116 (2012) 7449]. We reduce the problem to a model BChl dimer to elucidate the role of resonance coupling, site energies, nuclear mode and energy disorder in the enhancement of vibronic-exciton and ground-state vibrational coherences, and to identify regimes where this enhancement is significant. For …
Owing to both electronic and dielectric confinement effects, two-dimensional organic-inorganic hybrid perovskites sustain strongly bound excitons at room temperature. Here, we demonstrate that there are non-negligible contributions to the excitonic correlations that are specific to the lattice structure and its polar fluctuations, both of which are controlled via the chemical nature of the organic counter-cation. We present a phenomenological, yet quantitative framework to simulate excitonic absorption lineshapes in single-layer organic-inorganic hybrid perovskites, based on the two-dimensiona…
We report a family of two-dimensional hybrid perovskites (2DHPs) based on phenethylammonium lead iodide ((PEA)$_2$PbI$_4$) that show complex structure in their low-temperature excitonic absorption and photoluminescence (PL) spectra as well as hot exciton PL. We replace the 2-position (ortho) H on the phenyl group of the PEA cation with F, Cl, or Br to systematically increase the cation's cross-sectional area and mass and study changes in the excitonic structure. These single atom substitutions substantially change the observable number of and spacing between discrete resonances in the excitoni…
Roles of individual pigments in ultrafast excitation dynamics of light-harvesting phycobiliproteins revealed by recombinant techniques and two-dimensional electronic spectroscopy
Kansai Institute for Photon Science, National Institutes for Quantum Science and Technology (QST)（量子科学技术研究院光子科学关西研究所）；Institute for Quantum Life Science, National Institutes for Quantum Science and Technology (QST)（量子科学技术研究院量子生命科学研究所）
In this paper we consider dynamics of a molecular system subjected to external pumping by a light source. Within a completely quantum mechanical treatment, we derive a general formula, which enables to asses effects of different light properties on the photo-induced dynamics of a molecular system. We show that once the properties of light are known in terms of certain two-point correlation function, the only information needed to reconstruct the system dynamics is the reduced evolution superoperator. The later quantity is in principle accessible through ultrafast non-linear spectroscopy. Consi…
In purple bacteria, the fundamental charge-separation step that drives the conversion of radiation energy into chemical energy proceeds along one branch - the A branch - of a heterodimeric pigment-protein complex, the reaction center. Here, we use first principles time-dependent density functional theory (TDDFT) with an optimally-tuned range-separated hybrid functional to investigate the electronic and excited-state structure of the primary six pigments in the reaction center of \textit{Rhodobacter sphaeroides}. By explicitly including amino-acid residues surrounding these six pigments in our …
Environmental Control Extends Beyond Quantum Dephasing in Exciton Energy Transfer
Ningbo University（宁波大学）；SLAC National Accelerator Laboratory（斯坦福直线加速器中心）；Hangzhou Dianzi University（杭州电子科技大学）；University of Toronto（多伦多大学）；Rosalind Franklin Institute（罗莎琳德·富兰克林研究所）；University of Oxford（牛津大学）
