Annihilation of Excess Excitations along Phycocyanin Rods Precedes Downhill Flow to Allophycocyanin Cores in the Phycobilisome of Synechococcus elongatus PCC 7942.

Cyanobacterial phycobilisome complexes absorb visible sunlight and funnel photogenerated excitons to the photosystems where charge separation occurs. In the phycobilisome complex of Synechococcus elongatus PCC 7942, phycocyanin protein rods that absorb bluer wavelengths are assembled on allophycocyanin cores that absorb redder wavelengths. This arrangement creates a natural energy gradient toward the reaction centers of the photosystems. Here, we employ broadband pump-probe spectroscopy to observe the fate of excess excitations in the phycobilisome complex of this organism. We show that excess excitons are quenched through exciton-exciton annihilation along the phycocyanin rods prior to transfer to the allophycocyanin cores. Our observations are especially relevant in comparison to other antenna proteins, where exciton annihilation primarily occurs in the lowest-energy chlorophylls. The observed effect could play a limited photoprotective role in physiological light fluences. The exciton decay dynamics is faster in the intact phycobilisome than in isolated C-phycocyanin trimers studied in earlier work, confirming that this effect is an emergent property of the complex assembly. Using the obtained annihilation data, we calculate exciton hopping times of 2.2-6.4 ps in the phycocyanin rods. This value agrees with earlier FRET calculations of exciton hopping times along phycocyanin hexamers by Sauer and Scheer.

Redox conditions correlated with vibronic coupling modulate quantum beats in photosynthetic pigment-protein complexes.

Quantum coherences, observed as time-dependent beats in ultrafast spectroscopic experiments, arise when light-matter interactions prepare systems in superpositions of states with differing energy and fixed phase across the ensemble. Such coherences have been observed in photosynthetic systems following ultrafast laser excitation, but what these coherences imply about the underlying energy transfer dynamics remains subject to debate. Recent work showed that redox conditions tune vibronic coupling in the Fenna-Matthews-Olson (FMO) pigment-protein complex in green sulfur bacteria, raising the question of whether redox conditions may also affect the long-lived (>100 fs) quantum coherences observed in this complex. In this work, we perform ultrafast two-dimensional electronic spectroscopy measurements on the FMO complex under both oxidizing and reducing conditions. We observe that many excited-state coherences are exclusively present in reducing conditions and are absent or attenuated in oxidizing conditions. Reducing conditions mimic the natural conditions of the complex more closely. Further, the presence of these coherences correlates with the vibronic coupling that produces faster, more efficient energy transfer through the complex under reducing conditions. The growth of coherences across the waiting time and the number of beating frequencies across hundreds of wavenumbers in the power spectra suggest that the beats are excited-state coherences with a mostly vibrational character whose phase relationship is maintained through the energy transfer process. Our results suggest that excitonic energy transfer proceeds through a coherent mechanism in this complex and that the coherences may provide a tool to disentangle coherent relaxation from energy transfer driven by stochastic environmental fluctuations.

Sub-10 fs Intervalley Exciton Coupling in Monolayer MoS2 Revealed by Helicity-Resolved Two-Dimensional Electronic Spectroscopy.

The valley pseudospin at the K and K' high-symmetry points in monolayer transition metal dichalcogenides (TMDs) has potential as an optically addressable degree of freedom in next-generation optoelectronics. However, intervalley scattering and relaxation of charge carriers leads to valley depolarization and limits practical applications. In addition, enhanced Coulomb interactions lead to pronounced excitonic effects that dominate the optical response and initial valley depolarization dynamics but complicate the interpretation of ultrafast spectroscopic experiments at short time delays. Employing broadband helicity-resolved two-dimensional electronic spectroscopy (2DES), we observe ultrafast (∼10 fs) intervalley coupling between all A and B valley exciton states that results in a complete breakdown of the valley index in large-area monolayer MoS2 films. These couplings and subsequent dynamics exhibit minimal excitation fluence or temperature dependence and are robust toward changes in sample grain size and inherent strain. Our observations strongly suggest that this direct intervalley coupling on the time scale of optical excitation is an inherent property of large-area MoS2 distinct from dynamic carrier or exciton scattering, phonon-driven processes, and multiexciton effects. This ultrafast intervalley coupling poses a fundamental challenge for exciton-based valleytronics in monolayer TMDs and must be overcome to fully realize large-area valleytronic devices.

Photosynthesis tunes quantum-mechanical mixing of electronic and vibrational states to steer exciton energy transfer.

Photosynthetic species evolved to protect their light-harvesting apparatus from photoxidative damage driven by intracellular redox conditions or environmental conditions. The Fenna-Matthews-Olson (FMO) pigment-protein complex from green sulfur bacteria exhibits redox-dependent quenching behavior partially due to two internal cysteine residues. Here, we show evidence that a photosynthetic complex exploits the quantum mechanics of vibronic mixing to activate an oxidative photoprotective mechanism. We use two-dimensional electronic spectroscopy (2DES) to capture energy transfer dynamics in wild-type and cysteine-deficient FMO mutant proteins under both reducing and oxidizing conditions. Under reducing conditions, we find equal energy transfer through the exciton 4-1 and 4-2-1 pathways because the exciton 4-1 energy gap is vibronically coupled with a bacteriochlorophyll-a vibrational mode. Under oxidizing conditions, however, the resonance of the exciton 4-1 energy gap is detuned from the vibrational mode, causing excitons to preferentially steer through the indirect 4-2-1 pathway to increase the likelihood of exciton quenching. We use a Redfield model to show that the complex achieves this effect by tuning the site III energy via the redox state of its internal cysteine residues. This result shows how pigment-protein complexes exploit the quantum mechanics of vibronic coupling to steer energy transfer.

Evidence for the Dominance of Carrier-Induced Band Gap Renormalization over Biexciton Formation in Cryogenic Ultrafast Experiments on MoS2 Monolayers.

Transition-metal dichalcogenides (TMDs) such as MoS2 display promising electrical and optical properties in the monolayer limit. Due to strong quantum confinement, TMDs provide an ideal environment for exploring excitonic physics using ultrafast spectroscopy. However, the interplay between collective excitation effects on single excitons such as band gap renormalization/exciton binding energy (BGR/EBE) change and multiexciton effects such biexciton formation remains poorly understood. Using two-dimensional electronic spectroscopy, we observe the dominance of single-exciton BGR/EBE signals over optically induced biexciton formation. We make this determination based on a lack of strong PIA features at T = 0 fs in the cryogenic spectra. By means of nodal line slope analysis, we determine that spectral diffusion occurs faster than BGR/EBE change, indicative of distinct processes. These results indicate that at higher sub-Mott limit fluences, collective effects on single excitons dominate biexciton formation.

Orientational Dynamics of Transition Dipoles and Exciton Relaxation in LH2 from Ultrafast Two-Dimensional Anisotropy.

Light-harvesting complexes in photosynthetic organisms display fast and efficient energy transfer dynamics, which depend critically on the electronic structure of the coupled chromophores within the complexes and their interactions with their environment. We present ultrafast anisotropy dynamics, resolved in both time and frequency, of the transmembrane light-harvesting complex LH2 from Rhodobacter sphaeroides in its native membrane environment using polarization-controlled two-dimensional electronic spectroscopy. Time-dependent anisotropy obtained from both experiment and modified Redfield simulation reveals an orientational preference for excited state absorption and an ultrafast equilibration within the B850 band in LH2. This ultrafast equilibration is favorable for subsequent energy transfer toward the reaction center. Our results also show a dynamic difference in excited state absorption anisotropy between the directly excited B850 population and the population that is initially excited at 800 nm, suggesting absorption from B850 states to higher-lying excited states following energy transfer from B850*. These results give insight into the ultrafast dynamics of bacterial light harvesting and the excited state energy landscape of LH2 in the native membrane environment.

Redox Conditions Affect Ultrafast Exciton Transport in Photosynthetic Pigment-Protein Complexes.

Pigment-protein complexes in photosynthetic antennae can suffer oxidative damage from reactive oxygen species generated during solar light harvesting. How the redox environment of a pigment-protein complex affects energy transport on the ultrafast light-harvesting time scale remains poorly understood. Using two-dimensional electronic spectroscopy, we observe differences in femtosecond energy-transfer processes in the Fenna-Matthews-Olson (FMO) antenna complex under different redox conditions. We attribute these differences in the ultrafast dynamics to changes to the system-bath coupling around specific chromophores, and we identify a highly conserved tyrosine/tryptophan chain near the chromophores showing the largest changes. We discuss how the mechanism of tyrosine/tryptophan chain oxidation may contribute to these differences in ultrafast dynamics that can moderate energy transfer to downstream complexes where reactive oxygen species are formed. These results highlight the importance of redox conditions on the ultrafast transport of energy in photosynthesis. Tailoring the redox environment may enable energy transport engineering in synthetic light-harvesting systems.

Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo.

In photosynthetic organisms, the pigment-protein complexes that comprise the light-harvesting antenna exhibit complex electronic structures and ultrafast dynamics due to the coupling among the chromophores. Here, we present absorptive two-dimensional (2D) electronic spectra from living cultures of the purple bacterium, Rhodobacter sphaeroides, acquired using gradient assisted photon echo spectroscopy. Diagonal slices through the 2D lineshape of the LH1 stimulated emission/ground state bleach feature reveal a resolvable higher energy population within the B875 manifold. The waiting time evolution of diagonal, horizontal, and vertical slices through the 2D lineshape shows a sub-100 fs intra-complex relaxation as this higher energy population red shifts. The absorption (855 nm) of this higher lying sub-population of B875 before it has red shifted optimizes spectral overlap between the LH1 B875 band and the B850 band of LH2. Access to an energetically broad distribution of excitonic states within B875 offers a mechanism for efficient energy transfer from LH2 to LH1 during photosynthesis while limiting back transfer. Two-dimensional lineshapes reveal a rapid decay in the ground-state bleach/stimulated emission of B875. This signal, identified as a decrease in the dipole strength of a strong transition in LH1 on the red side of the B875 band, is assigned to the rapid localization of an initially delocalized exciton state, a dephasing process that frustrates back transfer from LH1 to LH2.

Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells.

Photosynthesis transfers energy efficiently through a series of antenna complexes to the reaction center where charge separation occurs. Energy transfer in vivo is primarily monitored by measuring fluorescence signals from the small fraction of excitations that fail to result in charge separation. Here, we use two-dimensional electronic spectroscopy to follow the entire energy transfer process in a thriving culture of the purple bacteria, Rhodobacter sphaeroides. By removing contributions from scattered light, we extract the dynamics of energy transfer through the dense network of antenna complexes and into the reaction center. Simulations demonstrate that these dynamics constrain the membrane organization into small pools of core antenna complexes that rapidly trap energy absorbed by surrounding peripheral antenna complexes. The rapid trapping and limited back transfer of these excitations lead to transfer efficiencies of 83% and a small functional light-harvesting unit.During photosynthesis, energy is transferred from photosynthetic antenna to reaction centers via ultrafast energy transfer. Here the authors track energy transfer in photosynthetic bacteria using two-dimensional electronic spectroscopy and show that these transfer dynamics constrain antenna complex organization.

Electronic Structure and Dynamics of Higher-Lying Excited States in Light Harvesting Complex 1 from Rhodobacter sphaeroides.

Light harvesting in photosynthetic organisms involves efficient transfer of energy from peripheral antenna complexes to core antenna complexes, and ultimately to the reaction center where charge separation drives downstream photosynthetic processes. Antenna complexes contain many strongly coupled chromophores, which complicates analysis of their electronic structure. Two-dimensional electronic spectroscopy (2DES) provides information on energetic coupling and ultrafast energy transfer dynamics, making the technique well suited for the study of photosynthetic antennae. Here, we present 2DES results on excited state properties and dynamics of a core antenna complex, light harvesting complex 1 (LH1), embedded in the photosynthetic membrane of Rhodobacter sphaeroides. The experiment reveals weakly allowed higher-lying excited states in LH1 at 770 nm, which transfer energy to the strongly allowed states at 875 nm with a lifetime of 40 fs. The presence of higher-lying excited states is in agreement with effective Hamiltonians constructed using parameters from crystal structures and atomic force microscopy (AFM) studies. The energy transfer dynamics between the higher- and lower-lying excited states agree with Redfield theory calculations.