Mechanism of the Carotenoid-to-Bacteriochlorophyll Energy Transfer via the S₁ State in the LH2 Complexes from Purple Bacteria

Abstract

This investigation was motivated by a desire to get a deeper insight into the mechanism of carotenoiod-to-bacteriochlorophyll (Car-to-BChl) energy transfer proceeding via the carotenoid S1 state. (Here, we call the 2Ag - and 1Bu + states “the S1 and S2 states” according to the notation presently accepted.) To systematically examine the effect of the conjugation length of carotenoid on the rate and efficiency of the Car(S1)-to-BChl(Qy) energy transfer, we performed the following experiments. (1) Subpicosecond time-resolved absorption spectroscopy was employed to measure the S1-state lifetimes of lycopene (number of conjugated CC bonds, n = 11), spheroidene (n = 10), and neurosporene (n = 9), both free in n-hexane and bound to the LH2 complexes from Rhodospirillum molischianum (Rs. molischianum), Rhodobactor sphaeroides (Rb. sphaeroides) 2.4.1, and Rb. sphaeroides G1C, respectively. The lifetime of each free (bound) carotenoid was determined to be 4.7(3.4) ps for lycopene, 9.3(1.7) ps for spheroidene, and 21.2(1.3) ps for neurosporene. It was found that the rate and the efficiency of the Car(S1)-to-BChl(Qy) energy transfer increase systematically when the number of conjugated CC bonds decreases. (2) High-sensitivity steady-state fluorescence spectroscopy was used to measure the spectra of dual emission from the S2 and S1 states for the above carotenoids dissolved in n-hexane. The fluorescence data, combined with the above kinetic data, allowed us to evaluate the magnitudes of the transition-dipole moments associated with the Car(S1) emission. It was found that the S1 emissions of the above carotenoids carry noticeably large oscillator strengths (transition-dipole moments). In the case of the LH2 complex from Rs. molischianum, whose structural information is now available, the time constant of the Car(S1)-to-BChl(Qy) energy transfer (18.6 ps), which was predicted on the basis of a Car(S2)-to-BChl(Qy) full Coulombic coupling scaled by the ratio of the S1 vs S2 transition dipole moments, was in good agreement with the one spectroscopically determined (12.3 ps). The oscillator strength associated with the Car(S1) emission was discussed in terms of the state mixing between the carotenoid S2 and S1 states.

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

“…Multiple pathways involving S 2 and S 1 routes are common in LH2 and LH1 complexes of purple bacteria binding carotenoids with N < 11 (1,15,18). When carotenoids with a longer conjugated bond system such as lycopene (16,18,19) or spirilloxanthin (18,31) are bound to LH2 or LH1 complexes the S 1 route becomes inactive, but the S 2 pathway is functional in all purple bacterial antenna studied so far. 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.…”

“…The actual energy transfer efficiency, however, depends on the conjugation length N (the number of the conjugated C═C bonds) of the carotenoid. Whereas the S 2 -mediated energy transfer is nearly constant (∼50%) for carotenoids with N ¼ 9-11 and decreases to ∼30% only for N > 12 (1), the S 1 route reaches 90% efficiency for N ¼ 9 and drops to less than 10% for N > 11 (14)(15)(16). This strong dependence is ascribed to unfavorable spectral overlap between the carotenoid S 1 state and Q y band of BChl-a (1).…”

Femtosecond dynamics of the forbidden carotenoid S 1 state in light-harvesting complexes of purple bacteria observed after two-photon excitation

“…The electronic states of Cars often are described by analogy to polyenes (Fig. 1 (19,25,26). However, the best way to find direct evidence for Car S 1 3 BChl EET and to determine its contribution to the overall Car 3 BChl EET is to excite Car S 1 exclusively and thereby measure ET1 and ET1 directly without any convolution with S 2 state dynamics.…”

“…Despite intensive investigation of the underlying mechanisms (8,10,12,(15)(16)(17)(18)(19)(20), many aspects of the electronic energy transfer (EET) from the Cars are still poorly understood. The electronic states of Cars often are described by analogy to polyenes ( Only the S 0 7 S 2 transition is optically dipole-allowed.…”

“…However, because the S 1 3 S 0 transition is dipole-forbidden it remains a challenge to elucidate the mechanism that promotes Car S 1 to Chl EET. Neither the Förster (22,23) nor Dexter theories (24) provide satisfactory predictions (15,20 (19,25,26). However, the best way to find direct evidence for Car S 1 3 BChl EET and to determine its contribution to the overall Car 3 BChl EET is to excite Car S 1 exclusively and thereby measure ET1 and ET1 directly without any convolution with S 2 state dynamics.…”