Long-lived quantum coherence in photosynthetic complexes at physiological temperature

Abstract

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-MatthewsOlson 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.biophysics | photosynthesis | quantum beating | ultrafast spectroscopy | quantum biology E nergy transfer through photosynthetic pigment-protein complexes operates with exceptionally high quantum efficiency (1). Recent studies have demonstrated that energy moves through antennae using not only a classical hopping mechanism but also a manifestly quantum mechanical wave-like mechanism at cryogenic temperatures (2-5). Theoretical studies of this process within the Fenna-Matthews-Olson antenna complex (FMO) show that this quantum transport mechanism requires a balance between unitary (oscillatory) and dissipative (dephasing) dynamics; further, this balance appears to be optimized near room temperature and contributes to the robustness of the process (6-9). This theory demands that quantum coherence persist long enough to affect transport, but quantum beating has never been observed in FMO at physiological temperature.The FMO pigment-protein complex from Chlorobium tepidum serves as a model system for photosynthetic energy transfer processes (2, 10-13). This complex conducts energy from the larger light-harvesting chlorosome to the reaction center in green sulfur bacteria (14, 15). Each noninteracting FMO monomer contains seven coupled bacteriochlorophyll-a chromophores arranged asymmetrically, yielding seven nondegenerate, delocalized molecular excited states called excitons (11,16). The small number of distinct states makes this particular complex attractive for theoretical studies o...

Laser-Limited Signatures of Quantum Coherence

“…The signatures of vibronic coupling in multidimensional spectroscopy have drawn great interest lately, in particular to interpret oscillatory transients observed for light-harvesting complexes [3,[8][9][10] that persist much longer than predicted electronic dephasing times [11].…”

“…For FMO, the oscillations were found to persist for hundreds of femtoseconds at ambient temperatures and even up to a few picoseconds at 77 K [10]. In contrast, the measured spectral linewidths predict electronic dephasing times at 77 K hardly exceeding 100 fs [11], owing to rapid, stochastic variations in the environment, and coherences between excitons are expected to decay roughly on this timescale.…”

Quantum Wave Information of Life Revealed: An Algorithm for Electromagnetic Frequencies that Create Stability of Biological Order, With Implications for Brain Function and Consciousness

“…Quantum coherence in electron transfer in photosynthesis lasts for a long time (600 fs) in the pigment-protein complex (Engel, 2007;Ishizaki, 2010). But it is not yet fully known how this coherence is brought about in living tissue, although it has been shown that environmental noise increases energy delivery efficiency (Panitchayangkoona, 2010;Collini, 2010). The inferred algorithm of the present study shows that this coherence may be embedded in both higher and lower frequency bands.…”

Scalable High-Performance Algorithm for the Simulation of Exciton Dynamics. Application to the Light-Harvesting Complex II in the Presence of Resonant Vibrational Modes

“…4 On top of the relaxation process, oscillatory components prevail in 2d-spectra which contain signatures of electronic coherences and specific vibrational modes. 6,[8][9][10] The coupling to the environment determines the transfer efficiency in LHCs 11,12 through the bath-correlation time of the phonon bath, [13][14][15] the shape of the continuum part of the spectral density, 9,16 and specific structures within the spectral density. 9,17 For the FMO complex, the superohmic character of the spectral density results in long-lasting electronic coherences despite a strong coupling to the environment.…”