Bidirectional Energy Flow in the Photosystem II Supercomplex

The water-splitting capability of Photosystem II (PSII) of plants and green algae requires the system to balance efficient light harvesting along with effective photoprotection against excitation in excess of the photosynthetic capacity, particularly under the naturally fluctuating sunlight intensity. The comparatively flat energy landscape of the multicomponent structure, inferred from the spectra of the individual pigment–protein complexes and the rather narrow and featureless absorption spectrum, is well known. However, how the combination of the required functions emerges from the interactions among the multiple components of the PSII supercomplex (PSII-SC) cannot be inferred from the individual pigment–protein complexes. In this work, we investigate the energy transfer dynamics of the C2S2-type PSII-SC with a combined spectroscopic and modeling approach. Specifically, two-dimensional electronic-vibrational (2DEV) spectroscopy provides enhanced spectral resolution and the ability to map energy evolution in real space, while the quantum dynamical simulation allows complete kinetic modeling of the 210 chromophores. We demonstrate that additional pathways emerge within the supercomplex. In particular, we show that excitation energy can leave the vicinity of the charge separation components, the reaction center (RC), faster than it can transfer to it. This enables activatable quenching centers in the periphery of the PSII-SC to be effective in removing excessive energy in cases of overexcitation. Overall, we provide a quantitative description of how the seemingly contradictory functions of PSII-SC arise from the combination of its individual components. This provides a fundamental understanding that will allow further improvement of artificial solar energy devices and bioengineering processes for increasing crop yield.

and SI section 3).(d) Exponential fit of the simulated population evolution of CP43 for three different excitation frequencies (fit parameters are reported in Table S3)  A detailed discussion on the origin of the improved spectral resolution of 2DEV spectroscopy 3 can be found in ref. 4 Briefly, in pigment-protein complexes, the pigment electronic degrees (Figure 2c).On the other hand,the ESA band at 15,300 cm -1 and 15,600 cm -1 (Figure 2a) share more resemblance with the same ESA band of LHCII at the two excitation frequencies 23 (Figure 2b), particularly the peak at 1,657 cm -1 .
2 Spectral Density Definitions

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The spectral density parameters are listed in Table S1  For the PSII-CC components, the spectral density is defined 8,9 as where S 0 , s 1 , s 2 , ω 1 , and ω 2 are the parameters listed in Table S2.

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For the minor antennae and LHCII, the spectral density is defined 8,10 as where λ 0 and Γ 0 are the parameters listed in Table S2.Additionally, vibronic coupling with 32 individual modes are also included for the peripheral antennae, which contributes to the 33 spectral density as 8,10 where S j , ω j , and Γ vib are the parameters for each vibration modes.The values of these parameters can be found in ref 8 and ref.
where f (t) is the excitation population evolution (traces) of individual PSII-SC subunits, and Table S3: Exponential fit of simulated population evolution of the PSII-SC subunits.A detailed description can be found in Supporting Information Section 3).

Figure S1 :
Figure S1: Experimental spectra.Normalized absorption spectrum and visible excitation pump spectra for the 2DEV measurements on the (a) PSII-SC and (b) isolated LHCII trimer.(c) Infrared probe spectrum used for all 2DEV measurements.2DEV maps at different time delays for the PSII-SC: (d) 120 fs, (e) 400 fs, (f ) 5 ps and (g) 10 ps.The excitation at 15,200 cm -1 marks the separation between the two PSII-SC measurements (see panel (a) and Experimental).

Figure S2 :
Figure S2: Example of cross-checking of LDA analysis results.LDM for the simulated population evolution of CP43 in the PSII-SC for hyper-parameter α of (a) 0.1, (b) 3 and (c) 10.With increasing α the negative amplitude around 1 ps disappears.The corresponding growth is not observed via exponential fitting of the simulated population evolution of CP43 at different excitation frequencies (see TableS3and SI section 3).(d) Exponential fit of the simulated population evolution of CP43 for three different excitation frequencies (fit parameters are reported in TableS3)

Figure S3 :
FigureS3: Simulated quenching probability in the peripheral antennae of the PSII-SC at 300 K and 77 K. Probability that the excitation energy is quenched before reaching the RC, with quenching sites (the Chls near carotenoids) being in (a, f ) LHCII-A (G/g), (b, g) LHCII-B (N/n), (c, h) LHCII-C (Y/y), (d, i) CP26 and (e, j) CP29 at 300 K (a-e) and 77 K (f-j).The EET rate from Chls to carotenoid is universally set to (200 fs) -1 and the exact quenching sites (red: C602-C603; blue: C610-C612) are selected based on literature.1,2Detailed description can be found in Experimental.

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of freedom are influenced by the electronic couplings with other pigments, while the pigment 5 nuclear degrees of freedom, particularly the highly localized modes, are influenced by the 6 interactions with the local protein residues.This indicates that, in 2DEV spectroscopy, 7 the factors shifting the spectral responses of a pigment on the excitation axis and on the 8 detection axis have little to no correlation.Therefore, the chances of observing a peak at a 9 specific position of a 2DEV spectrum depends on the conditional probability P (ω exc , ω det ), 10 where ω exc is the excitation frequency and ω det is the detection frequency.In other words, the 11 chances of having overlapping spectral responses from multiple pigments are lower compared 12 to 2D electronic spectroscopy, where the two axes are correlated, and visible pump-IR probe 13 spectroscopy, which does not have resolution of excitation frequency.14 The improved spectral resolution of 2DEV spectroscopy has been demonstrated by the 15 studies of smaller subunits of PSII, 5-7 where different IR structures can be clearly seen at 16 different excitation frequencies.Figure 2 also shows some demonstrations, including the 17 2DEV spectral slices at different of excitation frequencies for the PSII-SC.For example, 18 the ESA region between 1630 cm -1 and 1660 cm -1 for the PSII-SC show clear excitation 19 frequency dependence.The ESA band at 14,700 cm -1 and 15,000 cm -1 (Figure 2a) have 20 similar structure to the same ESA band of the PSII-CC at the two excitation frequencies 21 1,2Detailed description can be found in Experimental.Figure S4: An example of IR structure evolution at 15400 cm -1 excitation.The evolution does not show a global decay, but rather fine structural changes.This shows that annihilation is not a complicating factor in our experiment as we would expect to see a universal decay for annihilation dynamics.31Improved Spectral Resolution of 2DEV Spectroscopy and S2.Two different spectral den-

Table S2 :
Spectral density parameters (detailed description can be found in Supporting Information Section 2).This row indicates whether under-damped Brownian oscillators were included in the spectral density. a