Ultrafast Energy Transfer in LHC-II Revealed by Three-Pulse Photon Echo Peak Shift Measurements

Abstract

We report the results of three-pulse photon echo peak shift (3PEPS) measurements on the light-harvesting complex II (LHC-II) of the green algae Chlamydomonas reinhardtii. Experiments were performed at two different excitation wavelengths, 670 and 650 nm, corresponding to Chl-a and Chl-b excitation, respectively. The 3PEPS data are analyzed using a new theory that incorporates the effect of energy transfer on third-order response functions. Our theoretical model separates energy transfer dynamics from the solvation dynamics arising from coupling of the electronic transitions to the protein environment. We suggest that the protein fluctuations can be described by an ultrafast solvation on a sub-100 fs time scale and a long time correlation (static disorder). Decay of the 670 nm peak shift reveals spectral equilibration time scales for Chl-a molecules that range from 300 fs to 6 ps and agree well with other experiments. 3PEPS data at 650 nm (Chl-b excitation) reveal rapid Chl-b to Chl-b energy transfer (<1 ps), which suggests excitation hopping between a pair of Chls-b, and slow energy transfer from these Chls-b to Chls-a. Also, a 60 cm-1 oscillatory mode is observed for Chl-b which we attribute to the first observation of coherent nuclear dynamics in LHC-II. Calculating the energy transfer dynamics based on recently proposed assignments of chromophores by solving the master equation reveals Chl-b intra- and interband energy transfer dynamics that are in qualitative agreement with the simulation model of the peak shift data.

A comparison of the three isoforms of the light-harvesting complex II using transient absorption and time-resolved fluorescence measurements

“…This is in agreement with the absorption spectra (see Figure 2a) where, for instance, the main Chl b absorption band for Lhcb2 peaking at 650 nm is broader than that of Lhcb1 and Lhcb3 and with the steady-state fluorescence spectra of Caffarri et al and Standfuss and Ku¨hlbrandt, whose fluorescence spectrum at 77 K of Lhcb2 is the broadest (fwhm) of the three isoforms. The obtained energy transfer time constants for all the isoforms of LHC II and native complexes are very similar (see also Table 3) and in agreement with previously reported rate constants for wild-type Kwa et al 1992;Bittner et al 1994Bittner et al , 1995Du et al 1994;Visser et al 1996Visser et al , 1997Connelly et al 1997;Gradinaru et al 1998;Agarwal et al 2000). Overall, it is important to note that the pump-probe data of the complexes studied, which depend critically on mutual orientations of pigments, are virtually identical, showing that for (nearly) all the pigments the organization is the same in all preparations.…”

“…Regarding energy transfer, it has been well established for native LHC II complexes that most of the excitation energy on the Chl b molecules is transferred to the Chl a molecules with subpicosecond time constants ($150-300 and $600 fs) and only a minor fraction is transferred with a time constant of a few picoseconds (4-9 ps) (Bittner et al 1994(Bittner et al , 1995Du et al 1994;Connelly et al 1997;Agarwal et al 2000;Salverda et al 2003). For Chl a fi Chl a energy transfer slow components have been found upon blue site excitation, i.e.…”

Two-Dimensional Spectroscopy of Chlorophyll a Excited-State Equilibration in Light-Harvesting Complex II

“…13,14 However, significantly longer lifetimes, in the range of tens of picoseconds and more, have also been reported. 9,15,16 The slowest lifetimes have been assigned to one Chl a pigment absorbing in the region of 665-670 nm.…”

Principles of light harvesting from single photosynthetic complexes

“…LHCII is trimeric, and each monomer contains 14 chlorophyll (Chl), six Chl-b and eight Chl-a, and four carotenoids surrounded by a protein matrix [24]. Energy rapidly transfers to the Chl-a, and fluorescence occurs out of the Chl-a band [41][42][43][44][45][46][47]. On-going efforts are focused on characterizing the changes in the excited state manifold of LHCII under conditions that mimic high light.…”