Yuan-Chung Cheng

Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems

Photosynthetic complexes are exquisitely tuned to capture solar light efficiently, and then transmit the excitation energy to reaction centres, where long term energy storage is initiated. The energy transfer mechanism is often described by semiclassical models that invoke ‘hopping’ of excited-state populations along discrete energy levels. Two-dimensional Fourier transform electronic spectroscopy has mapped these energy levels and their coupling in the Fenna–Matthews–Olson (FMO) bacteriochlorophyll complex, which is found in green sulphur bacteria and acts as an energy ‘wire’ connecting a large peripheral light-harvesting antenna, the chlorosome, to the reaction centre. The spectroscopic data clearly document the dependence of the dominant energy transport pathways on the spatial properties of the excited-state wavefunctions of the whole bacteriochlorophyll complex. But the intricate dynamics of quantum coherence, which has no classical analogue, was largely neglected in the analyses—even though electronic energy transfer involving oscillatory populations of donors and acceptors was first discussed more than 70 years ago, and electronic quantum beats arising from quantum coherence in photosynthetic complexes have been predicted and indirectly observed. Here we extend previous two-dimensional electronic spectroscopy investigations of the FMO bacteriochlorophyll complex, and obtain direct evidence for remarkably long-lived electronic quantum coherence playing an important part in energy transfer processes within this system. The quantum coherence manifests itself in characteristic, directly observable quantum beating signals among the excitons within the Chlorobium tepidum FMO complex at 77 K. This wavelike characteristic of the energy transfer within the photosynthetic complex can explain its extreme efficiency, in that it allows the complexes to sample vast areas of phase space to find the most efficient path.

Coherence dynamics in photosynthesis: protein protection of excitonic coherence.

The role of quantum coherence in promoting the efficiency of the initial stages of photosynthesis is an open and intriguing question. We performed a two-color photon echo experiment on a bacterial reaction center that enabled direct visualization of the coherence dynamics in the reaction center. The data revealed long-lasting coherence between two electronic states that are formed by mixing of the bacteriopheophytin and accessory bacteriochlorophyll excited states. This coherence can only be explained by strong correlation between the protein-induced fluctuations in the transition energy of neighboring chromophores. Our results suggest that correlated protein environments preserve electronic coherence in photosynthetic complexes and allow the excitation to move coherently in space, enabling highly efficient energy harvesting and trapping in photosynthesis.

Dynamics of Light Harvesting in Photosynthesis

We review recent theoretical and experimental advances in the elucidation of the dynamics of light harvesting in photosynthesis, focusing on recent theoretical developments in structure-based modeling of electronic excitations in photosynthetic complexes and critically examining theoretical models for excitation energy transfer. We then briefly describe two-dimensional electronic spectroscopy and its application to the study of photosynthetic complexes, in particular the Fenna-Matthews-Olson complex from green sulfur bacteria. This review emphasizes recent experimental observations of long-lasting quantum coherence in photosynthetic systems and the implications of quantum coherence in natural photosynthesis.

ARCHITECTURE OF A CHARGE-TRANSFER STATE REGULATING LIGHT HARVESTING IN A PLANT ANTENNA PROTEIN

Energy-dependent quenching of excess absorbed light energy (qE) is a vital mechanism for regulating photosynthetic light harvesting in higher plants. All of the physiological characteristics of qE have been positively correlated with charge transfer between coupled chlorophyll and zeaxanthin molecules in the light-harvesting antenna of photosystem II (PSII). We found evidence for charge-transfer quenching in all three of the individual minor antenna complexes of PSII (CP29, CP26, and CP24), and we conclude that charge-transfer quenching in CP29 involves a delocalized state of an excitonically coupled chlorophyll dimer. We propose that reversible conformational changes in CP29 can “tune” the electronic coupling between the chlorophylls in this dimer, thereby modulating the energy of the chlorophyll-zeaxanthin charge-transfer state and switching on and off the charge-transfer quenching during qE.

Three-dimensional band structure and bandlike mobility in oligoacene single crystals: A theoretical investigation

Quantum-chemical calculations coupled with a tight binding band model are used to study the charge carrier mobilities in oligoacene crystals. The transfer integrals for all nonzero interactions in four crystalline oligoacenes (naphthalene, anthracene, tetracene, and pentacene) were calculated, and then used to construct the excess electron and hole band structures of all four oligoacene crystals in the tight binding approximation. From these band structures, thermal-averaged velocity–velocity tensors in the constant-free-time and the constant-free-path approximations for all four materials were calculated at temperatures ranging from 2 to 500 K. The bandwidths for these oligoacenes were found to be of the order of 0.1–0.5 eV. Furthermore, comparison of the thermal-averaged velocity–velocity tensors with the experimental mobility data indicates that the simple band model is applicable for temperatures only up to about 150 K. A small-polaron band model is also considered, but the exponential band narrowing ...

Quantum Coherence Enabled Determination of the Energy Landscape in Light-Harvesting Complex II

The near-unity efficiency of energy transfer in photosynthesis makes photosynthetic light-harvesting complexes a promising avenue for developing new renewable energy technologies. Knowledge of the energy landscape of these complexes is essential in understanding their function, but its experimental determination has proven elusive. Here, the observation of quantum coherence using two-dimensional electronic spectroscopy is employed to directly measure the 14 lowest electronic energy levels in light-harvesting complex II (LHCII), the most abundant antenna complex in plants containing approximately 50% of the worlds chlorophyll. We observe that the electronically excited states are relatively evenly distributed, highlighting an important design principle of photosynthetic complexes that explains the observed ultrafast intracomplex energy transfer in LHCII.

Theory of coherent resonance energy transfer

A theory of coherent resonance energy transfer is developed combining the polaron transformation and a time-local quantum master equation formulation, which is valid for arbitrary spectral densities including common modes. The theory contains inhomogeneous terms accounting for nonequilibrium initial preparation effects and elucidates how quantum coherence and nonequilibrium effects manifest themselves in the coherent energy transfer dynamics beyond the weak resonance coupling limit of the Forster and Dexter (FD) theory. Numerical tests show that quantum coherence can cause significant changes in steady state donor/acceptor populations from those predicted by the FD theory and illustrate delicate cooperation of nonequilibrium and quantum coherence effects on the transient population dynamics.

Coherence Quantum Beats in Two-Dimensional Electronic Spectroscopy

We study the coherence quantum beats in two-dimensional (2D) electronic spectroscopy of a coupled dimer system using a theoretical method based on a time-nonlocal quantum master equation and a recently proposed scheme for the evaluation of the third-order photon echo polarization [Gelin, M. F.; Egorova, D.; Domcek, W. J. Chem. Phys. 2005, 123, 164112]. The simulations show that the amplitude and peak shape beating in the 2D spectra is a result of the interplay between the rephasing and non-rephasing contributions to the 2D signals and can be used to elucidate the coherence dynamics in a multichromophoric system. In addition, the results suggest that the rephasing and non-rephasing 2D spectra contain complementary information, and a study of both of them could provide more dynamical information from 2D electronic spectroscopy.

Reversible adapting layer produces robust single-crystal electrocatalyst for oxygen evolution

Electrochemically converting water into oxygen/hydrogen gas is ideal for high-density renewable energy storage in which robust electrocatalysts for efficient oxygen evolution play crucial roles. To date, however, electrocatalysts with long-term stability have remained elusive. Here we report that single-crystal Co3O4 nanocube underlay with a thin CoO layer results in a high-performance and high-stability electrocatalyst in oxygen evolution reaction. An in situ X-ray diffraction method is developed to observe a strong correlation between the initialization of the oxygen evolution and the formation of active metal oxyhydroxide phase. The lattice of skin layer adapts to the structure of the active phase, which enables a reversible facile structural change that facilitates the chemical reactions without breaking the scaffold of the electrocatalysts. The single-crystal nanocube electrode exhibits stable, continuous oxygen evolution for >1,000 h. This robust stability is attributed to the complementary nature of defect-free single-crystal electrocatalyst and the reversible adapting layer.

A unified theory for charge-carrier transport in organic crystals

To characterize the crossover from bandlike transport to hopping transport in molecular crystals, we study a microscopic model that treats electron-phonon interactions explicitly. A finite-temperature variational method combining Merrifields transformation with Bogoliubovs theorem is developed to obtain the optimal basis for an interacting electron-phonon system, which is then used to calculate the bandlike and hopping mobilities for charge carriers. Our calculations on the one dimensional (1D) Holstein model at T=0 K and finite temperatures show that the variational basis gives results that compared favorably to other analytical methods. We also study the structures of polaron states at a broad range of parameters including different temperatures. Furthermore, we calculate the bandlike and hopping mobilities of the 1D Holstein model in different parameters and show that our theory predicts universal power-law decay at low temperatures and an almost temperature independent behavior at higher temperatures, in agreement with experimental observations. In addition, we show that as the temperature increases, hopping transport can become dominant even before the polaron state changes its character. Thus, our result indicates that the self-trapping transition studied in conventional polaron theories does not necessarily correspond to the bandlike to hopping transition in the transport properties in organic molecular crystals. Finally, a comparison of our 1D results with experiments on ultrapure naphthalene crystals suggests that the theory can describe the charge-carrier mobilities quantitatively across the whole experimental temperature range.