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Excitation energy transfer and vibronic coherence in intact phycobilisomes

Abstract

The phycobilisome is an oligomeric chromoprotein complex that serves as the principal mid-visible light-harvesting system in cyanobacteria. Here we report the observation of excitation-energy-transfer pathways involving delocalized optical excitations of the bilin (linear tetrapyrrole) chromophores in intact phycobilisomes isolated from Fremyella diplosiphon. By using broadband multidimensional electronic spectroscopy with 6.7-fs laser pulses, we are able to follow the progress of excitation energy from the phycoerythrin disks at the ends of the phycobilisome’s rods to the C-phycocyanin disks along their length in <600 fs. Oscillation maps show that coherent wavepacket motions prominently involving the hydrogen out-of-plane vibrations of the bilins mediate non-adiabatic relaxation of a manifold of vibronic exciton states. However, the charge-transfer character of the bilins in the allophycocyanin-containing segments localizes the excitations in the core of the phycobilisome, yielding a kinetic bottleneck that enables photoregulatory mechanisms to operate efficiently on the >10-ps timescale.

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Fig. 1: Structure and linear spectroscopy of the phycobilisome from Fremyella diplosiphon.
Fig. 2: 2DES spectra from intact phycobilisomes isolated from F. diplosiphon with delays T selected over the 10 fs–100 ps range.
Fig. 3: Global and target model for the 550–580-nm region of the excitation axis of the 2DES spectrum.
Fig. 4: Rapidly damped amplitude oscillations above and below the diagonal of the 2DES spectra.
Fig. 5: Fourier amplitude spectra and oscillation maps.
Fig. 6: Energy level and potential energy diagrams for the bilin chromophores in the phycobilisomes from F. diplosiphon.

Data availability

The datasets generated during and/or analysed during the current study are available at https://doi.org/10.5281/zenodo.6743715 (ref. 75). Source data are provided with this paper.

Code availability

The MATLAB and Julia scripts employed for analysis of data during the current study are available at https://doi.org/10.5281/zenodo.6743715 (ref. 75).

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Acknowledgements

Work in the laboratory of W.F.B. was principally supported by grant award no. DE-SC0010847 from the Photosynthetic Systems Program of the Office of Basic Energy Sciences, US Department of Energy. Work in the laboratory of C.A.K. was supported by grant award no. DE-SC0020606 from the Photosynthetic Systems Program of the Office of Basic Energy Sciences, US Department of Energy. We thank D. Sheppard, S. Lechno-Yossef and H. Bao in the Kerfeld laboratory for their assistance with the cyanobacterial cultures and with the isolation of the phycobilisome samples.

Author information

Authors and Affiliations

Authors

Contributions

S.S., R.W.T., C.A.K. and W.F.B. conceived the study and organized the project, with C.A.K. and W.F.B. providing overall supervision. S.S., M.A.D.-M. and W.L. set up the cyanobacterial cultures and the growth conditions and isolated the phycobilisome samples. S.S., R.W.T., N.M.T.M. and W.F.B. designed the multidimensional spectroscopy experiments, with S.S. and N.M.T.M. responsible for setting up the experiments and recording the datasets presented in the study. S.S., N.M.T.M. and C.H.L. analysed the datasets and produced the plotted results. S.S., R.W.T. and N.M.T.M. performed the global analysis. S.S. and J.B.R. performed the fluorescence experiments and analysed the results. S.S., N.M.T.M., C.H.L. and W.F.B. contributed the overall interpretation of the experimental results. The draft manuscript was written by S.S. and W.F.B., with contributions from N.M.T.M. and C.A.K. The revised manuscripts were written by S.S. and W.F.B.

Corresponding author

Correspondence to Warren F. Beck.

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Extended data

Extended Data Fig. 1 Continuous fluorescence excitation–emission spectra from phycobilisome preparations from Fremyella diplosiphon.

a, for broken phycobilisomes, which were produced by suspension of the isolated intact phycobilisomes in a 80 mM phosphate buffer solution at pH 7; b, for intact phycobilisomes, as suspended in a 0.8 M phosphate buffer solution at pH 7.

Extended Data Fig. 2 Global and target model for the integral of the 15150–15500 cm−1 (645–660-nm) region of the excitation axis of the 2DES spectrum.

a, Four-compartment kinetic scheme, with the initial fractional excitations (in each box) and time constants. b, Time evolution of the populations. c, Evolution-associated difference spectra (EADS). d, Amplitude transients at five detection wavelengths, with the fitted global model (black curve) superimposed; the confidence intervals for each data point are indicated by bars. The T axis used in b and d is semilogarithmic, with the linear–log split at 100 fs. In d, the instrument-response function is shown for the 640-nm transient as a 12-fs Gaussian (gray dotted curve) centered at T = 0 fs.

Source data

Extended Data Fig. 3 Decay of excited-state absorption (ESA) and diagonal ground-state bleaching (GSB) in the 2DES spectra.

a, 2DES spectrum at T = 10 ps. b, Amplitude transients sampled at the marked coordinates in the 2DES spectrum with a transient fitted over the T > 40 fs range (solid black curve) composed of two exponential components, A(T) = a0 + ∑i ai exp(−Ti), convoluted with a 12-fs Gaussian instrument-response function. For the diagonal (16.5,16.5) transient: a0 = −0.24, a1 = 4.9, τ1 = 1.4 ps, a2 = 9.8, τ2 = 38 ps; for the ESA transient (16.5,14.9): a0 = 3.2, a1 = −6.6, τ1 = 180 fs, a2 = −16, τ2 = 23 ps. The bars indicate 95% confidence intervals for the amplitudes. The delay T axis is semilogarithmic, with the linear/log split at 100 fs.

Source data

Extended Data Fig. 4 Oscillation maps for the Hann-windowed T = 50–500 fs range for the principal modulation components at 520, 830, 1300, and 1670 cm−1.

The non-oscillatory part of the 2DES signal was removed by subtracting an overdetermined 2D global model. Dashed lines in the oscillation maps are drawn evenly spaced from the diagonal of the spectrum by the selected modulation frequency. The black horizontal line along the detection axis marks the peak of the fluorescence oscillator-strength spectrum (Fig. 1f).

Extended Data Fig. 5 Oscillation maps for the Hann-windowed T = 50–500 fs range at 110, 270, 650, and 1050 cm−1.

The non-oscillatory part of the 2DES signal was removed by subtracting an overdetermined 2D global model. Dashed lines in the oscillation maps are drawn evenly spaced from the diagonal of the spectrum by the selected modulation frequency. The black horizontal line along the detection axis marks the peak of the fluorescence oscillator-strength spectrum (Fig. 1f).

Supplementary information

Supplementary Information

Supplementary Figs. 1–3.

Supplementary Video 1

Video of the 2DES dataset.

Source data

Source Data Fig. 1

Fig. 1f: Model for linear absorption spectrum of phycobilisomes from Fremyella diplosiphon using component phycobiliprotein absorption spectra.

Source Data Fig. 3

Fig. 3c: Evolution associated difference spectra (EADS) from the global model for the 550–580 nm excitation region of the 2DES spectra.

Source Data Fig. 4

Fig. 4c: Oscillatory transients above and below the diagonal of the 2DES spectrum.

Source Data Fig. 5

Fig. 5a: FT spectra for transients shown in Fig. 3d after subtraction of the global model.

Source Data Fig. 6

Fig. 6d: Model energy levels for the phycobilisome.

Source Data Extended Data Fig. 2

Extended Data Fig. 2c: Evolution associated difference spectra (EADS) from the global model for the 646–660 nm excitation region of the 2DES spectra.

Source Data Extended Data Fig. 3

Extended Data Fig. 3b: Amplitude transients for the diagonal and ESA coordinates.

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Sil, S., Tilluck, R.W., Mohan T. M., N. et al. Excitation energy transfer and vibronic coherence in intact phycobilisomes. Nat. Chem. 14, 1286–1294 (2022). https://doi.org/10.1038/s41557-022-01026-8

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