Mechanisms underlying carotenoid absorption in oxygenic photosynthetic proteins

Abstract

The electronic properties of carotenoid molecules underlie their multiple functions throughout biology, and tuning of these properties by their in vivo locus is of vital importance in a number of cases. This is exemplified by photosynthetic carotenoids, which perform both light-harvesting and photoprotective roles essential to the photosynthetic process. However, despite a large number of scientific studies performed in this field, the mechanism(s) used to modulate the electronic properties of carotenoids remain elusive. We have chosen two specific cases, the two β-carotene molecules in photosystem II reaction centers and the two luteins in the major photosystem II light-harvesting complex, to investigate how such a tuning of their electronic structure may occur. Indeed, in each case, identical molecular species in the same protein are seen to exhibit different electronic properties (most notably, shifted absorption peaks). We assess which molecular parameters are responsible for this in vivo tuning process and attempt to assign it to specific molecular events imposed by their binding pockets.

Keywords: Carotenoid; Electronic Absorption; LHCII; Lutein; Photosynthesis; Photosystem II; Raman Spectroscopy; Spectroscopy; β-Carotene.

FIGURE 1.

Molecular structures of β-carotene and lutein.

FIGURE 2.

Correlation between the S₀→S₂ electronic transition and the frequency of the ν₁ Raman band for linear Cars with different conjugation length, N (performed in n-hexane; black line), compared with the same correlation for β-carotene (blue line) and lutein (red line) as a function of solvent polarizability. Solvents: a, tetrahydrofuran; b, n-hexane; c, cyclohexane; d, diethylether; e, toluene; f, chloroform; g, acetonitrile; h, methanol; i, pyridine; j, nitrobenzene; and k, CS₂.

FIGURE 3.

Absorption spectra of PSII-RC particles at room temperature (solid line) and 77 K (dashed line).

FIGURE 4.

RR spectra of PSII-RC recorded with 488.0- and 514.5-nm excitation at room temperature (RT; A) and 77 K (B).

FIGURE 5.

Correlation between the S₀→S₂ electronic transition and the frequency of the ν₁ Raman band for the two β-carotene molecules in PSII-RC at room temperature (RT; red triangles) and 77 K (red inverted triangles). For comparison, the relationship between Cars of different conjugation length in the same solvent (n-hexane) and the relationship expressed as a function of solvent polarizability for β-carotene are also shown (cf. Fig. 2).

FIGURE 6.

Absorption spectra of LHCII trimers at room temperature (RT; solid line) and 77 K (dashed line).

FIGURE 7.

RR spectra of LHCII trimers recorded with 496.5- and 514.5-nm excitation at room temperature (RT; A) and 77 K (B).

FIGURE 8.

Correlation between the S₀→S₂ electronic transition and the frequency of the ν₁ Raman band for the two lutein molecules in LHCII trimers (blue triangles, room temperature (RT); blue inverted triangles, 77 K). For comparison, the relationship between Cars of different conjugation length in the same solvent (n-hexane) and the relationship expressed as a function of solvent polarizability for lutein are also shown (cf. Fig. 2).

FIGURE 9.

Structural details of the carotenoid end rings in PSII-RC and LHCII, drawn using PyMOL from Protein Data Bank entries 3ARC and 1RWT, respectively. Ball-and-stick representations colored by atom except for carbons are shown for: protein-bound carotenoids (carbons in yellow); aromatic residues discussed in the text (gray); and other cofactors present (white). For PSII-RC, the DFT-calculated β-carotene structure (; cyan) has been fitted to Bcr651 (A and B) and Bcr645 (C and D). For LHCII, the latest structure containing the twist in lut2 is not yet available; in the structure shown here (E), whereas the ring orientation relative to TRP46 is correct, the position of carbon atoms immediately preceding the ring (C7–9) is not.