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 nearinfrared 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. C arotenoids are among the most abundant pigments in nature, having a wide variety of functions in living organisms. In photosynthetic organisms, besides their important regulatory role in the flow of the absorbed energy, carotenoids serve predominantly as light-harvesting pigments, efficiently covering the spectral region 450-550 nm (1). They transfer absorbed light energy to chlorophyll (Chl) or bacteriochlorophyll (BChl) molecules that funnel energy toward the reaction center where a charge separation occurs (1). The ability of the carotenoids to act both as photoprotection agents and light-harvesting pigments is a consequence of their unique photophysical properties (2). A typical carotenoid belongs to an idealized C 2h point symmetry group. In the manifold of singlet states of a carotenoid, the one-photon optical transitionϪ in C 2h group notation) is symmetry forbidden, resulting in the absence of an S 0 3S 1 absorption and in very weak fluorescence from the S 1 state (2). The well-known absorption of carotenoids in the blue-green region of the visible spectrum is caused by a strongly allowed transition from the S 0 (1A g Ϫ ) state to the S 2 (1B u ϩ ) state. Usually, fluorescence from the S 1 and S 2 states of carotenoids has a good spectral overlap with the Q y and Q x bands of Chls͞BChls, which favors energy transfer. On the other hand, the forbidden nature of the S 1 state results in a very weak transition dipole and puts substantial limits on efficient Förster mechanism of energy transfer (3). Furthermore, although the S 2 state has a strong transition dipole moment, there is a rapid internal conversion to the S 1 state in 50-300 fs (4), so that energy transfer from the S 2 state has to be extremely fast to compete with the S 2 to S 1 relaxation. Despite these apparent limitations, carotenoids are indeed efficient energy donors in various light-harvesting complexes of bacteria, algae, and higher plants, where efficiency of carotenoid to Chl͞ BChl energy transfer approaches 100% (1, 5, 6). Such high efficiencies are achieved by tight packing at van der Waals radius of pigments in light-harvesting complexes, ...

Photoprotection in a purple phototrophic bacterium mediated by oxygen-dependent alteration of carotenoid excited-state properties

“…It is worth noting that the S 2 route is significantly diminished in light-harvesting complexes of dinoflagellates or diatoms binding the carbonyl carotenoids peridinin or fucoxanthin. Then, the pathway through the S 1 ∕ICT state becomes the major pathway (20)(21)(22) reminiscent of the situation studied here in RC-LH1-PufX(spn) complexes.…”

“…In other types of light-harvesting complexes such as the peridinin-chlorophyll protein from dinoflagellates, carotenoids with a conjugated C═O group facilitate S 1 -mediated energy transfer by coupling to an intramolecular charge-transfer (ICT) state (20). This light-harvesting strategy seems common among certain genera of marine algae that utilize carbonyl carotenoids (21)(22)(23).…”

Energy Transfer, Excited-State Deactivation, and Exciplex Formation in Artificial Caroteno-Phthalocyanine Light-Harvesting Antennas

“…The carotenoid to Pc energy transfer in dyad 1 is reminiscent of several natural light-harvesting antennas where high carotenoid to chlorophyll energy transfer efficiency is obtained by employing a multiphasic Car to Chl energy transfer. 2,11,21,[31][32][33] The final EADS (magenta line) appears after 2 ns and represents the component that does not decay on the time scale of the experiment. It features the typical carotenoid triplet ESA in the 475-550 nm region as well as a bleach/band-shift-like signal in the Pc Q region.…”

Dependence of the energy transfer to graphene on the excitation energy

“…The absorption spans over the whole visible range with the main band (from 350 to 550 nm) attributed mainly to peridinin absorption. Chlorophylls absorb through the Q y band around 670 nm and the Soret band at 437 nm [20]. The emission of PCP complex is associated with fluorescence of chlorophylls and occurs at 673 nm, with a 30% quantum yield and a decay time constant of 4 ns [21].…”