Ultrafast time-resolved absorption spectroscopy of geometric isomers of carotenoids

Abstract

The structures of a number of stereoisomers of carotenoids have been revealed in three-dimensional X-ray crystallographic investigations of pigment-protein complexes from photosynthetic organisms. Despite these structural elucidations, the reason for the presence of stereoisomers in these systems is not well understood. An important unresolved issue is whether the natural selection of geometric isomers of carotenoids in photosynthetic pigment-protein complexes is determined by the structure of the protein binding site or by the need for the organism to accomplish a specific physiological task. The association of cis isomers of a carotenoid with reaction centers and trans isomers of the same carotenoid with light-harvesting pigment-protein complexes has led to the hypothesis that the stereoisomers play distinctly different physiological roles. A systematic investigation of the photophysics and photochemistry of purified, stable geometric isomers of carotenoids is needed to understand if a relationship between stereochemistry and biological function exists. In this work we present a comparative study of the spectroscopy and excited state dynamics of cis and trans isomers of three different open-chain carotenoids in solution. The molecules are neurosporene (n=9), spheroidene (n=10), and spirilloxanthin (n=13), where n is the number of conjugated π-electron double bonds. The spectroscopic experiments were carried out on geometric isomers of the carotenoids purified by high performance liquid chromatography (HPLC) and then frozen to 77 K to inhibit isomerization. The spectral data taken at 77 K provide a high resolution view of the spectroscopic differences between geometric isomers. The kinetic data reveal that the lifetime of the lowest excited singlet state of a cis-isomer is consistently shorter than that of its corresponding all-trans counterpart despite the fact that the excited state energy of the cis molecule is typically higher than that of the trans molecule. Quantum theoretical calculations on an n=9 linear polyene were carried out to examine this process. The calculations indicate that the electronic coupling terms are significantly higher for the cis isomer, and when combined with the Franck-Condon factors, predict internal conversion rates roughly double those of the all-trans species. The electronic effects more than offset the decrease in coupling efficiencies associated with the higher system origin energies and explain the observed shorter cis isomer lifetimes.

Triplet excited state spectra and dynamics of carotenoids from the thermophilic purple photosynthetic bacterium Thermochromatium tepidum

“…Interestingly, Spx also has preferred excited state properties to be a direct quencher of the BChl excited singlet state in that complex. The S 1 state energy of Spx is 11,500 cm -1 (Niedzwiedzki et al 2009;Papagiannakis et al 2003), which lies right below the BChl B850 band (11,765 cm -1 ) and fits perfectly with the B850 fluorescence that appears at 877 nm (11,460 cm -1 ).…”

Ultrafast time-resolved spectroscopy of the light-harvesting complex 2 (LH2) from the photosynthetic bacterium Thermochromatium tepidum

“…S 2 (1 1 B u ? ) transition (Niedzwiedzki et al 2009Polivka et al 2001). Figure 2b shows global fitting results of the TA data taken in the VIS range.…”

“…state represents decay of the state immediately after excitation (Macpherson and Gillbro 1998) that decays to populate the S 1 (2 1 A g -). Decay of the transition associated with the ESA from the S 1 (2 1 A g -) state is represented by the second EADS with lifetime of 1.4 ps (Niedzwiedzki et al 2009;Okamoto et al 1998). The last and very weak EADS with lifetime of 8 ps is associated with the transition from the so-called S* state.…”

Spectroscopic Investigation of Carotenoids Involved in Non-Photochemical Fluorescence Quenching

“…While S 0 →S 2 transition of a cis isomer is blue-shifted versus that of the all-trans carotenoid, the S 1 →S n transition is shifted in the opposite direction, i.e., whereas isomerization increases the energy of the S 0 →S 2 transition, it decreases the energy of the S 1 -S n transition (Niedzwiedzki et al 2009(Niedzwiedzki et al , 2010. Decreasing S 1 →S n transition energy upon isomerization to a cis confi guration can be demonstrated by measurements of the S 1 energies of cis isomers that are systematically higher than the corresponding S 1 energies of the corresponding all-trans carotenoids.…”

“…The S 3 state is of A g + symmetry, and while A g − to A g + transition is spectroscopically forbidden for all-trans carotenoids, the reduction in symmetry induced by isomerization of the molecule from an all-trans to a cis confi guration renders the transition allowed. The cis-peak is readily discerned in the spectral region between 300 and 350 nm, with an intensity as high as 50 % of the maximum of the S 0 →S 2 transition Niedzwiedzki et al 2009Niedzwiedzki et al , 2010. As for the major band, the position of the cis peak depends on conjugation length; the maximum of the cis-peak occurs at 340 nm for zeaxanthin (N eff = 10) and at 320 nm for neoxanthin (N eff = 8.5) (Niedzwiedzki et al 2010 ).…”