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-
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.
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- Award ID(s):
- 1900359
- NSF-PAR ID:
- 10438128
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 118
- Issue:
- 49
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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. -
For over a decade there has been some significant excitement and speculation that quantum effects may be important in the excitation energy transport process in the light harvesting complexes of certain bacteria and algae, in particular via the Fenna–Matthews–Olsen (FMO) complex. Whilst the excitement may have waned somewhat with the realisation that the observed long-lived oscillations in two-dimensional electronic spectra of FMO are probably due to vibronic coherences, it remains a question whether these coherences may play any important role. We review our recent work showing how important the site-to-site variation in coupling between chloroplasts in FMO and their protein scaffold environment is for energy transport in FMO and investigate the role of vibronic modes in this transport. Whilst the effects of vibronic excitations seem modest for FMO, we show that for bilin-based pigment–protein complexes of marine algae, in particular PC645, the site-dependent vibronic excitations seem essential for robust excitation energy transport, which may again open the door for important quantum effects to be important in these photosynthetic complexes.more » « less
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Abstract The complex choreography of electronic, vibrational, and vibronic couplings used by photoexcited molecules to transfer energy efficiently is remarkable, but an unambiguous description of the temporally evolving vibronic states governing these processes has proven experimentally elusive. We use multidimensional electronic-vibrational spectroscopy to identify specific time-dependent excited state vibronic couplings involving multiple electronic states, high-frequency vibrations, and low-frequency vibrations which participate in ultrafast intersystem crossing and subsequent relaxation of a photoexcited transition metal complex. We discover an excited state vibronic mechanism driving long-lived charge separation consisting of an initial electronically-localized vibrational wavepacket which triggers delocalization onto two charge transfer states after propagating for ~600 femtoseconds. Electronic delocalization consequently occurs through nonadiabatic internal conversion driven by a 50 cm−1coupling resulting in vibronic coherence transfer lasting for ~1 picosecond. This study showcases the power of multidimensional electronic-vibrational spectroscopy to elucidate complex, non-equilibrium energy and charge transfer mechanisms involving multiple molecular coordinates.
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Sodium hydride (NaH) in the gas phase presents a seemingly simple electronic structure making it a potentially tractable system for the detailed investigation of nonadiabatic molecular dynamics from both computational and experimental standpoints. The single vibrational degree of freedom, as well as the strong nonadiabatic coupling that arises from the excited electronic states taking on considerable ionic character, provides a realistic chemical system to test the accuracy of quasi-classical methods to model population dynamics where the results are directly comparable against quantum mechanical benchmarks. Using a simulated pump–probe type experiment, this work presents computational predictions of population transfer through the avoided crossings of NaH via symmetric quasi-classical Meyer–Miller (SQC/MM), Ehrenfest, and exact quantum dynamics on realistic, ab initio potential energy surfaces. The main driving force for population transfer arises from the ground vibrational level of the D 1 Σ + adiabatic state that is embedded in the manifold of near-dissociation C 1 Σ + vibrational states. When coupled through a sharply localized first-order derivative coupling most of the population transfers between t = 15 and t = 30 fs depending on the initially excited vibronic wavepacket. While quantum mechanical effects are expected due to the reduced mass of NaH, predictions of the population dynamics from both the SQC/MM and Ehrenfest models perform remarkably well against the quantum dynamics benchmark. Additionally, an analysis of the vibronic structure in the nonadiabatically coupled regime is presented using a variational eigensolver methodology.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2112817118
