The role of the individual Lhcas in photosystem I excitation energy trapping

Abstract

In this work, we have investigated the role of the individual antenna complexes and of the low-energy forms in excitation energy transfer and trapping in Photosystem I of higher plants. To this aim, a series of Photosystem I (sub)complexes with different antenna size/composition/absorption have been studied by picosecond fluorescence spectroscopy. The data show that Lhca3 and Lhca4, which harbor the most red forms, have similar emission spectra (λ(max) = 715-720 nm) and transfer excitation energy to the core with a relative slow rate of ∼25/ns. Differently, the energy transfer from Lhca1 and Lhca2, the "blue" antenna complexes, occurs about four times faster. In contrast to what is often assumed, it is shown that energy transfer from the Lhca1/4 and the Lhca2/3 dimer to the core occurs on a faster timescale than energy equilibration within these dimers. Furthermore, it is shown that all four monomers contribute almost equally to the transfer to the core and that the red forms slow down the overall trapping rate by about two times. Combining all the data allows the construction of a comprehensive picture of the excitation-energy transfer routes and rates in Photosystem I.

Figure 1

77 K fluorescence emission of PSI (sub)complexes upon 475 nm excitation.

Figure 2

Streak-camera time-resolved fluorescence measurements. (A) Cartoons of the investigated complexes were prepared with PyMOL (DeLano, W. L. The PyMOL Molecular Graphics System (2002) on http://www.pymol.org) from the structural data of PSI-LHCI (57) (and LHCII (21) for Lhca1/4) (Protein Data Bank codes: 2O01 and 1RWT). (B) Streak images showing 140 ps along the y axis and 650–780 nm along the x axis. Color represents fluorescence intensity with black no fluorescence, red highest intensity. Excitation was at 475 nm. (C) DAS estimated from the streak data, shown in B. (D) Average lifetime calculated according to τ_av = ΣA_i^∗τ_i, with A the relative area under the DAS and τ the corresponding lifetime, the transfer component was not taken into account.

Figure 3

TCSPC DAS of PSI core (A), PSI-Lhca1/4 (B), and PSI-WT (C), excitation was at 440 (solid) and 475 nm (dashed). DAS are normalized to each other based on the area under the red-shifted DAS.

Figure 4

RT absorption (A), 77 K emission (B), and TCSPC DAS (C) of PSI-Lhca5. For comparison the absorption spectrum of PSI-WT is also shown (A). Spectra are normalized to the number of Chls in the Q_y region (A), or the red maximum (B and C).

Figure 5

Target analysis of PSI-LHCI kinetics. (A) Compartmental model of PSI-LHCI, with EET rates in /ns. (B) Species associated spectra of the compartments.

Figure 6

Schematic presentations of energy transfer and trapping in PSI-LHCI. Thickness of the arrows indicates the rates. The transfer rate between Lhca2 and Lhca4 could not be estimated from our target analysis, but, based on structural data, it has been suggested to be similar to the intradimer transfer rates (1,58).