Dugan Hayes

Long-lived quantum coherence in photosynthetic complexes at physiological temperature

Photosynthetic antenna complexes capture and concentrate solar radiation by transferring the excitation to the reaction center that stores energy from the photon in chemical bonds. This process occurs with near-perfect quantum efficiency. Recent experiments at cryogenic temperatures have revealed that coherent energy transfer—a wave-like transfer mechanism—occurs in many photosynthetic pigment-protein complexes. Using the Fenna–Matthews–Olson antenna complex (FMO) as a model system, theoretical studies incorporating both incoherent and coherent transfer as well as thermal dephasing predict that environmentally assisted quantum transfer efficiency peaks near physiological temperature; these studies also show that this mechanism simultaneously improves the robustness of the energy transfer process. This theory requires long-lived quantum coherence at room temperature, which never has been observed in FMO. Here we present evidence that quantum coherence survives in FMO at physiological temperature for at least 300 fs, long enough to impact biological energy transport. These data prove that the wave-like energy transfer process discovered at 77 K is directly relevant to biological function. Microscopically, we attribute this long coherence lifetime to correlated motions within the protein matrix encapsulating the chromophores, and we find that the degree of protection afforded by the protein appears constant between 77 K and 277 K. The protein shapes the energy landscape and mediates an efficient energy transfer despite thermal fluctuations.

Engineering Coherence Among Excited States in Synthetic Heterodimer Systems

Coherence in Photosynthesis It is unclear how energy absorbed by pigments in antenna proteins is transferred to the central site of chemical catalysis during photosynthesis. Hildner et al. (p. 1448) observed coherence—prolonged persistence of a quantum mechanical phase relationship—at the single-molecule level in light-harvesting complexes from purple bacteria. The results bolster conclusions from past ensemble measurements that coherence plays a pivotal role in photosynthetic energy transfer. Hayes et al. (p. 1431, published online 18 April) examined a series of small molecules comprised of bridged chromophores that also manifest prolonged coherence. Small molecules comprising bridged chromophores manifest a quantum mechanical effect observed in light-harvesting proteins. The design principles that support persistent electronic coherence in biological light-harvesting systems are obscured by the complexity of such systems. Some electronic coherences in these systems survive for hundreds of femtoseconds at physiological temperatures, suggesting that coherent dynamics may play a role in photosynthetic energy transfer. Coherent effects may increase energy transfer efficiency relative to strictly incoherent transfer mechanisms. Simple, tractable, manipulable model systems are required in order to probe the fundamental physics underlying these persistent electronic coherences, but to date, these quantum effects have not been observed in small molecules. We have engineered a series of rigid synthetic heterodimers that can serve as such a model system and observed quantum beating signals in their two-dimensional electronic spectra consistent with the presence of persistent electronic coherences.

Extracting the Excitonic Hamiltonian of the Fenna-Matthews-Olson Complex Using Three-Dimensional Third-Order Electronic Spectroscopy

We extend traditional two-dimensional (2D) electronic spectroscopy into a third Fourier dimension without the use of additional optical interactions. By acquiring a set of 2D spectra evenly spaced in waiting time and dividing the area of the spectra into voxels, we can eliminate population dynamics from the data and transform the waiting time dimension into frequency space. The resultant 3D spectrum resolves quantum beating signals arising from excitonic coherences along the waiting frequency dimension, thereby yielding up to 2n-fold redundancy in the set of frequencies necessary to construct a complete set of n excitonic transition energies. Using this technique, we have obtained, to our knowledge, the first fully experimental set of electronic eigenstates for the Fenna-Matthews-Olson (FMO) antenna complex, which can be used to improve theoretical simulations of energy transfer within this protein. Whereas the strong diagonal peaks in the 2D rephasing spectrum of the FMO complex obscure all but one of the crosspeaks at 77 K, extending into the third dimension resolves 19 individual peaks. Analysis of the independently collected nonrephasing data provides the same information, thereby verifying the calculated excitonic transition energies. These results enable one to calculate the Hamiltonian of the FMO complex in the site basis by fitting to the experimental linear absorption spectrum.

Dynamics of electronic dephasing in the Fenna–Matthews–Olson complex

Electronic coherence has been shown to persist in the Fenna?Matthews?Olson (FMO) antenna complex from green sulfur bacteria at 77?K for at least 660?fs, several times longer than the typical lifetime of a coherence in a dynamic environment at this temperature. Such long-lived coherence was proposed to improve energy transfer efficiency in photosynthetic systems by allowing an excitation to follow a quantum random walk as it approaches the reaction centre. Here we present a model for bath-induced electronic transitions, demonstrating that the protein matrix protects coherences by globally correlating fluctuations in transition energies. We also quantify the dephasing rates for two particular electronic coherences in the FMO complex at 77?K using two-dimensional Fourier transform electronic spectroscopy and find that the lifetimes of individual coherences are distinct. Within the framework of noise-assisted transport, this result suggests that the FMO complex has been locally tuned by natural selection to optimize transfer efficiency by exploiting quantum coherence.

Two-dimensional electronic spectroscopy of bacteriochlorophyll a in solution: Elucidating the coherence dynamics of the Fenna-Matthews-Olson complex using its chromophore as a control

Following the observation of long-lived coherences in the two-dimensional (2D) electronic spectra of the Fenna-Matthews-Olson (FMO) complex, many theoretical works suggest that coherences between excitons may play a role in the efficient energy transfer that occurs in photosynthetic antennae. This interpretation of the dynamics depends on the assignment of quantum beating signals to superpositions of excitons, which is complicated by the possibility of observing both electronic and vibrational coherences in 2D spectra. Here, we explore 2D spectra of bacteriochlorophyll a (BChla) in solution in an attempt to isolate vibrational beating signals in the absence of excitonic signals to identify the origin of the quantum beats in 2D spectra of FMO. Even at high laser power, our BChla spectra show strong beating only from the nonresonant response of the solvent. The beating signals that we can conclusively assign to vibrational modes of BChla are only slightly above the noise and at higher frequencies than those previously observed in spectra of FMO. Our results suggest that the beating observed in spectra of FMO is of a radically different character than the signals observed here and can therefore be attributed to electronic coherences or intermolecular degrees of freedom.

Robustness of electronic coherence in the Fenna–Matthews–Olson complex to vibronic and structural modifications

We present the first two-dimensional electronic spectra of photosynthetic antenna complexes bearing modifications to the protein and the chromophores. The vibronic structure of the Fenna-Matthews-Olson complex was altered by near-complete substitution of 13C for naturally abundant carbon and separately by randomly distributed partial deuteration. The structure and arrangement of the bacteriochlorophyll a chromophores were modified by deletion of the gene encoding the enzyme responsible for reducing the isoprenoid tail of the bacteriochlorophylls. Analysis of the time-dependent amplitude of the crosspeak corresponding to excitons 1 and 2 indicates that these modifications do not affect the frequency or dephasing of the beating observed in this particular peak. This result leads us to conclude that this beating indeed arises from electronic coherence and not vibrational wavepacket motion. We further conclude that the protection of zero-quantum coherences afforded by the protein matrix of this photosynthetic complex is not the result of a finely-tuned series of system-bath interactions perfected by billions of years of evolution but rather a simple downstream property of a close arrangement of chromophores within a phonon bath. We conclude with a brief discussion of the outstanding questions and possible applications of this phenomenon.

Towards a coherent picture of excitonic coherence in the Fenna?Matthews?Olson complex

Observations of long-lived coherence between excited states in several photosynthetic antenna complexes has motivated interest in developing a more detailed understanding of the role of the protein matrix in guiding the underlying dynamics of the system. These experiments suggest that classical rate laws may not provide an adequate description of the energy transfer process and that quantum effects must be taken into account to describe the near unity transfer efficiency in these systems. Recently, it has been shown that coherences between different pairs of excitons dephase at different rates. These details should provide some insight about the underlying electronic structure of the complex and its coupling to the protein bath. Here we show that a simple model can account for the different dephasing rates as well as the most current available experimental evidence of excitonic coherences in the Fenna–Matthews–Olson complex. The differences in dephasing rates can be understood as arising largely from differences in the delocalization and shared character between the underlying electronic states. We also suggest that the anomalously low dephasing rate of the exciton 1–2 coherence is enhanced by non-secular effects.

Scalable Ligand-Mediated Transport Synthesis of Organic–Inorganic Hybrid Perovskite Nanocrystals with Resolved Electronic Structure and Ultrafast Dynamics

Colloidal perovskite nanocrystals support bright, narrow PL tunable over the visible spectrum. However, bandgap tuning of these materials remains limited to laboratory-scale syntheses. In this work, we present a polar-solvent-free ligand-mediated transport synthesis of high-quality organic-inorganic perovskite nanocrystals under ambient conditions with photoluminescence quantum yields up to 97%. Our synthesis employs a ligand-mediated transport mechanism that circumvents the need for exquisite external control (e.g., temperature control, inert-gas protection, dropwise addition of reagents) required by other methods due to extremely fast reaction kinetics. In the ligand-mediated transport mechanism, multiple equilibria cooperatively dictate reaction rates and enable precise control over NC size. These small nanocrystals exhibit high photoluminescence quantum yields due to quantum confinement. Nanosecond transient absorption spectroscopy experiments reveal a fluence-independent PL decay originating from exciton recombination. Two-dimensional electronic spectroscopy resolves multiple spectral features reflecting the electronic structure of the nanocrystals. The resolved features exhibit size-dependent spectral positions, further indicating the synthesized nanocrystals are quantum-confined.

Peak shape analysis of diagonal and off-diagonal features in the two-dimensional electronic spectra of the Fenna-Matthews-Olson complex.

We have recorded a series of two-dimensional electronic spectra of the Fenna–Matthews–Olson (FMO) complex from Prosthecochloris aestuarii, with several crosspeaks sufficiently resolved to permit a quantitative analysis of both the amplitude and the two-dimensional peak shape. The exponential growth and/or decay of peaks on and off the main diagonal provides information on population transfer rates between pairs of excitons. Quantum beats observed in the amplitudes and shapes of these peaks persist throughout the relaxation process, indicating that energy transfer in FMO involves both incoherent and coherent dynamics. By comparing the oscillations in the amplitude and shape of crosspeaks, we confirm theoretical predictions regarding their correlation and identify previously indistinguishable combinations of nonlinear response pathways that contribute to the signal at particular positions in the spectra. Such analysis is crucial to understanding the enormous amount of information contained in two-dimensional electronic spectra and offers a new route to uncovering a complete description of the energy transfer kinetics in photosynthetic antennae.

Response to Comment on “Engineering coherence among excited states in synthetic heterodimer systems”

Halpin, Johnson, and Miller contest our assignment of quantum beating signals observed in the two-dimensional electronic spectra of a series of fluorescein heterodimers to electronic coherences. Here, we present resonance Raman spectra, statistical analysis on multiple data sets, and an explanation of differences between the family of molecules described in our Report and the homodimer examined by the commenters. We contend that these results all support our assignment of the beating signals to electronic coherences.