Carotenoid Oxidation in Photosystem II

Abstract

The oxidation of carotenoid upon illumination at low temperature has been studied in Mn-depleted photosystem II (PSII) using EPR and electronic absorption spectroscopy. Illumination of PSII at 20 K results in carotenoid cation radical (Car+*) formation in essentially all of the centers. When a sample which was preilluminated at 20 K was warmed in darkness to 120 K, Car+* was replaced by a chlorophyll cation radical. This suggests that carotenoid functions as an electron carrier between P680, the photooxidizable chlorophyll in PSII, and ChlZ, the monomeric chlorophyll which acts as a secondary electron donor under some conditions. By correlating with the absorption spectra at different temperatures, specific EPR signals from Car+* and ChlZ+* are distinguished in terms of their g-values and widths. When cytochrome b559 (Cyt b559) is prereduced, illumination at 20 K results in the oxidation of Cyt b559 without the prior formation of a stable Car+*. Although these results can be reconciled with a linear pathway, they are more straightforwardly explained in terms of a branched electron-transfer pathway, where Car is a direct electron donor to P680(+), while Cyt b559 and ChlZ are both capable of donating electrons to Car+*, and where the ChlZ donates electrons when Cyt b559 is oxidized prior to illumination. These results have significant repercussions on the current thinking concerning the protective role of the Cyt b559/ChlZ electron-transfer pathways and on structural models of PSII.

Conductance of a biomolecular wire

“…Taking G Х 2 nS (the largest conductance measured for Car with 9 double bonds under oxidizing potential) (Fig. 3a Middle) yields k et ϭ 5.6 ϫ 10 6 s Ϫ1 or ϭ 0.18 s. Both time scales are significantly smaller than that assumed for electron transfer from Q A Ϫ to P 680 ϩ via ␤-carotene in photosystem II (200 s to 1 ms) (1,30), indicating that the electron transfer is not limited by the transfer across the Car but more likely by other steps in the photoprotection mechanism. Additionally, it is likely that electron transfer in our system involves ballistic tunneling of many electrons as opposed to consecutive oxidation and reduction for the transfer of each electron.…”

Photosystem II Peripheral Accessory Chlorophyll Mutants inChlamydomonas reinhardtii. Biochemical Characterization and Sensitivity to Photo-Inhibition,

“…As hypothesized by Schelvis et al (1994) the peripheral Chls coordinated by the D1-H118 and D2-H117 residues are sufficiently far removed (approximately 30 Å) from the Chl special pair (P680) to reduce the likelihood of their direct oxidation by P680 ϩ . Consistent with this prediction, it has been shown that Car radicals are generated under cryogenic conditions that lead to the photo-accumulation of Chl Z ϩ suggesting that Car may participate in Chl Z oxidation (Hanley et al, 1999). Chl Z ϩ subsequently is reduced by Cyt b 559 (Buser et al, 1992 Shigemori et al, 1998).…”

“…This electron transfer cycle includes plastoquinone bound at the B binding site (Q B ), Cyt b 559 , Chl Z (the redox active Chl monomer coordinated by either the D1-H118 or D2-H117 residue), possibly (Car) carotenoid, and the primary donor, P680 ϩ (Koulougliotis et al, 1994;Noguchi et al, 1994;Hanley et al, 1999;Vrettos et al, 1999). Under high-light intensities, both P680 ϩ and doubly reduced Q A may accumulate leading to damage and turnover of the D1 protein (photo-inhibition; Chen et al, 1992;Andersson and Barber, 1996;Napiwotzki et al, 1997;Gadjieva et al, 2000).…”

“…Brudvig and coworkers demonstrated that the resonance Raman spectrum of Chl Z ϩ was perturbed in a cyanobacterial D1-H118Q mutant but was unaffected in a D2-H117Q mutant. It is noted, however, that the cryogenic conditions used to trap Chl Z ϩ could lead to the photo-accumulation of Car radicals that would affect the relaxation properties of Chl Z ϩ (Noguchi et al, 1994;Hanley et al, 1999).…”

Spectroscopic and Photochemical Properties of Open-Chain Carotenoids

“…12 Carotenoids also may act as stabilizers of protein structure and facilitators of the assembly of pigment-protein complexes, [13][14][15] as regulators of energy flow, 6,[15][16][17][18][19][20][21] or as redox cofactors. [22][23][24][25] The most well-known naturally occurring carotenoid, -carotene, is a C 40 hydrocarbon with terminal isoprenoid rings and eleven π-electron conjugated carbon-carbon double bonds. Other naturally occurring carotenoids often contain functional group substitutions along the polyene chain and on the isoprenoid terminal rings.…”