Carotenoid to chlorophyll energy transfer in the peridinin-chlorophyll-a-protein complex involves an intramolecular charge transfer state

Abstract

Carotenoids are, along with chlorophylls, crucial pigments involved in light-harvesting processes in photosynthetic organisms. Details of carotenoid to chlorophyll energy transfer mechanisms and their dependence on structural variability of carotenoids are as yet poorly understood. Here, we employ femtosecond transient absorption spectroscopy to reveal energy transfer pathways in the peridinin-chlorophyll-a-protein (PCP) complex containing the highly substituted carotenoid peridinin, which includes an intramolecular charge transfer (ICT) state in its excited state manifold. Extending the transient absorption spectra toward near-infrared region (600-1800 nm) allowed us to separate contributions from different low-lying excited states of peridinin. The results demonstrate a special light-harvesting strategy in the PCP complex that uses the ICT state of peridinin to enhance energy transfer efficiency.

Fig 1.

Absorption spectra of the PCP complex (solid line), Chl-a in diethyl ether (dashed line), and peridinin in ethylene glycol (dotted line).

Fig 2.

Transient absorption spectra of the PCP complex at 0.5 ps (filled squares) and 30 ps (open circles) after the excitation at 535 nm. (Inset) Enlargement of the spectral region 800–1,800 nm.

Fig 3.

Kinetic traces of the PCP complex measured after the excitation at 535 nm. Probing wavelengths are indicated for each kinetic. Solid lines represent best fits obtained from multiexponential global fitting procedure.

Fig 4.

Scheme of energy levels and energy transfer pathways between peridinin and Chl-a in the PCP complex. Intramolecular relaxation processes are denoted by wavy arrows, whereas the dashed arrow represents the long-lived Chl-a fluorescence. Solid arrows represent energy transfer channels: (S₂→Q_x channel, 25%; S₁/ICT→Q_y channel, 63%). The dotted line represents a possible minor energy transfer channel involving higher vibrational levels of the S₁/ICT state. Excitation at 535 nm is shown as a double arrow. All processes are labeled by a corresponding time constant. See text for details.