Molecular factors controlling photosynthetic light harvesting by carotenoids

Abstract

Carotenoids are naturally occurring pigments that absorb light in the spectral region in which the sun irradiates maximally. These molecules transfer this energy to chlorophylls, initiating the primary photochemical events of photosynthesis. Carotenoids also regulate the flow of energy within the photosynthetic apparatus and protect it from photoinduced damage caused by excess light absorption. To carry out these functions in nature, carotenoids are bound in discrete pigment-protein complexes in the proximity of chlorophylls. A few three-dimensional structures of these carotenoid complexes have been determined by X-ray crystallography. Thus, the stage is set for attempting to correlate the structural information with the spectroscopic properties of carotenoids to understand the molecular mechanism(s) of their function in photosynthetic systems. In this Account, we summarize current spectroscopic data describing the excited state energies and ultrafast dynamics of purified carotenoids in solution and bound in light-harvesting complexes from purple bacteria, marine algae, and green plants. Many of these complexes can be modified using mutagenesis or pigment exchange which facilitates the elucidation of correlations between structure and function. We describe the structural and electronic factors controlling the function of carotenoids as energy donors. We also discuss unresolved issues related to the nature of spectroscopically dark excited states, which could play a role in light harvesting. To illustrate the interplay between structural determinations and spectroscopic investigations that exemplifies work in the field, we describe the spectroscopic properties of four light-harvesting complexes whose structures have been determined to atomic resolution. The first, the LH2 complex from the purple bacterium Rhodopseudomonas acidophila, contains the carotenoid rhodopin glucoside. The second is the LHCII trimeric complex from higher plants which uses the carotenoids lutein, neoxanthin, and violaxanthin to transfer energy to chlorophyll. The third, the peridinin-chlorophyll-protein (PCP) from the dinoflagellate Amphidinium carterae, is the only known complex in which the bound carotenoid (peridinin) pigments outnumber the chlorophylls. The last is xanthorhodopsin from the eubacterium Salinibacter ruber. This complex contains the carotenoid salinixanthin, which transfers energy to a retinal chromophore. The carotenoids in these pigment-protein complexes transfer energy with high efficiency by optimizing both the distance and orientation of the carotenoid donor and chlorophyll acceptor molecules. Importantly, the versatility and robustness of carotenoids in these light-harvesting pigment-protein complexes have led to their incorporation in the design and synthesis of nanoscale antenna systems. In these bioinspired systems, researchers are seeking to improve the light capture and use of energy from the solar emission spectrum.

Figure 1

(top left) A three-state model of carotenoid excited states consisting of S₂ (blue) and S₁ (red) states. Relaxation processes are denoted by arrows and corresponding time constants. Internal conversion processes are denoted by blue and red arrows, black arrows denote vibrational relaxation. Blurred lines denotes the other states whose role in energy transfer is less clear: ICT (red), S* (green), 1¹B_u⁻ (purple) and 3¹A_g⁻ (black). (Top right) Absorption spectra of LH2 (purple), PCP (orange) and LHCII (green). The range of energies of carotenoid S₂ and S₁ transitions are also shown by the orange and red bars beneath the spectra. Dashed line denotes the solar irradiance spectrum emphasizing the importance of carotenoids in light-harvesting. (Bottom) Molecular structures of four important carotenoids. Color coding corresponds to the absorption spectra of the light-harvesting complexes in which they are found.

Figure 2

Structures of four light-harvesting complexes exhibiting energy transfer from carotenoids. (A) LH2 complex of the purple bacterium Rhodopseudomonas acidophila having the carotenoid rhodopin glucoside (red) and BChl-a (green); (B) LHCII trimer utilizing the carotenoids lutein (red), neoxanthin (yellow) and violaxanthin (orange) in energy transfer to Chl-a (green) and Chl-b (blue); (C) Peridinin-Chl-a-protein from the dinoflagellate, Amphidinium carterae. Eight peridinin molecules (red) transfer energy to two Chl-a (green); (D) Xanthorhodopsin from the eubacteirum Salinibacter ruber. The carotenoid salinixanthin (red) transfers energy to the retinal chromophore (green).

Figure 3

Dependence of the S₁ (blue) and S₂ (red) state energies of carotenoids on their number of conjugated double bonds, N. The width of the bands corresponds either to the variability in state energy due to environment or to uncertainty in determining the energy. The green band corresponds to S₂ energies of carbonyl carotenoids. Energies of typical acceptor states are also shown.

Figure 4

Summary of pathways and efficiencies of carotenoid-mediated energy transfer in light-harvesting systems from various sources. Energy is transferred either from the S₂ state of carotenoids (orange) to the Q_x bands of (B)Chl (yellow), or from the carotenoid S₁ state (red) to Q_y bands of BChl (brown) or Chl (green). The S₁ energy of the retinal chromophore in xanthorhodopsin is shown in purple. The height of the rectangles corresponds to the variation in energy of the electronic states in complexes.