Nature does not rely on long-lived electronic quantum coherence for photosynthetic energy transfer

Abstract

During the first steps of photosynthesis, the energy of impinging solar photons is transformed into electronic excitation energy of the light-harvesting biomolecular complexes. The subsequent energy transfer to the reaction center is commonly rationalized in terms of excitons moving on a grid of biomolecular chromophores on typical timescales [Formula: see text]100 fs. Today's understanding of the energy transfer includes the fact that the excitons are delocalized over a few neighboring sites, but the role of quantum coherence is considered as irrelevant for the transfer dynamics because it typically decays within a few tens of femtoseconds. This orthodox picture of incoherent energy transfer between clusters of a few pigments sharing delocalized excitons has been challenged by ultrafast optical spectroscopy experiments with the Fenna-Matthews-Olson protein, in which interference oscillatory signals up to 1.5 ps were reported and interpreted as direct evidence of exceptionally long-lived electronic quantum coherence. Here, we show that the optical 2D photon echo spectra of this complex at ambient temperature in aqueous solution do not provide evidence of any long-lived electronic quantum coherence, but confirm the orthodox view of rapidly decaying electronic quantum coherence on a timescale of 60 fs. Our results can be considered as generic and give no hint that electronic quantum coherence plays any biofunctional role in real photoactive biomolecular complexes. Because in this structurally well-defined protein the distances between bacteriochlorophylls are comparable to those of other light-harvesting complexes, we anticipate that this finding is general and directly applies to even larger photoactive biomolecular complexes.

Keywords: 2D spectroscopy; Fenna–Matthews–Olson protein; exciton; photosynthesis; quantum coherence.

Fig. 1.

(A) The 2D photon echo spectra for different waiting times $T$ taken at $296$ K. Shown is the real part. A, Left shows the experimental results, while A, Right displays the theoretically calculated spectra using the parameters obtained from the fits shown in C and D. The black solid line marks the antidiagonal along which the spectral signal is shown in B. It is used as a consistence check for the electronic dephasing time. The blue and red squares in the top right spectrum marks the spectral positions at which we evaluate the cross-peak time evolution shown in Fig. 3 A and B. In A, Left, the black cross in the second spectrum from the top marks the spectral position evaluated in Fig. 3C. (B) Spectral profile along the antidiagonal as extracted from the experimental data shown in A. We note that the negative amplitude part in the profile shows a mixed signal from the solvent and the excited state absorption at $T=0$ fs, which leads to a slight underestimation of the homogeneous line width. (C) Linear absorption spectrum at $296$ K. Black symbols indicate the measured data, and the red solid line marks the theoretically calculated result. The blue bars show the calculated stick spectrum. (D) Circular dichroism (CD) spectrum at $296$ K. Black symbols mark the measured data. The red solid lines show the theoretical result calculated with the same parameters as in C. a.u., arbitrary units.

Fig. 2.

(A) The 2DDAS. A, Left shows the experimental results, and A, Right shows the theoretically calculated spectra. The four resulting associated decay times ${\tau }_{1,\mathrm{\dots },4}$ are indicated in the spectra. (B) The 2D correlation map of residuals obtained from the series of experimental spectra after subtracting the kinetics by the global fitting procedure. The red line on top is the measured absorption spectrum of the FMO trimer, and the blue bars mark the stick spectrum of the FMO model. The white dashed lines mark the exciton energies, which are used to overlap with the correlation map.

Fig. 3.

(A and B) Time evolution of the real part of the calculated 2D photon echo signal at the spectral positions ${\omega }_{\tau }=\mathrm{12,300}$ cm⁻¹, ${\omega }_t=\mathrm{12,600}$ cm⁻¹ marked by a red square in Fig. 1A (A) and for ${\omega }_{\tau }=\mathrm{12,600}$ cm⁻¹, ${\omega }_t=\mathrm{12,300}$ cm⁻¹ marked by a blue square in Fig. 1A (B). It is apparent that a minimal amount of electronic coherence only survives up to $\sim 60$ fs. (C) The real (black) and imaginary (blue) part of the experimentally measured time trace at the same spectral position (black cross in Fig. 1A) ${\omega }_{\tau }=\mathrm{12,350}$ cm⁻¹, ${\omega }_t=\mathrm{12,200}$ cm⁻¹ as measured in ref. , however, measured here at $296$ K. The error bars indicate the SD obtained after averaging four datasets. The imaginary part is vertically shifted by $0.035$ for clarity. a.u., arbitrary units.