Ultrafast Dynamics and Excited State Spectra of Open-Chain Carotenoids at Room and Low Temperatures

Abstract

Many of the spectroscopic features and photophysical properties of carotenoids are explained using a three-state model in which the strong visible absorption of the molecules is associated with an S0 (1(1)Ag-) --> S2 (1(1)Bu+) transition, and the lowest lying singlet state, S1 (2(1)Ag-), is a state into which absorption from the ground state is forbidden by symmetry. However, semiempirical and ab initio quantum calculations have suggested additional excited singlet states may lie either between or in the vicinity of S1 (2(1)Ag-) and S2 (1(1)Bu+), and some ultrafast spectroscopic studies have reported evidence for these states. One such state, denoted S*, has been implicated as an intermediate in the depopulation of S2 (1(1)Bu+) and as a pathway for the formation of carotenoid triplet states in light-harvesting complexes. In this work, we present the results of an ultrafast, time-resolved spectroscopic investigation of a series of open-chain carotenoids derived from photosynthetic bacteria and systematically increasing in their number of pi-electron carbon-carbon double bonds (n). The molecules are neurosporene (n = 9), spheroidene (n = 10), rhodopin glucoside (n = 11), rhodovibrin (n = 12), and spirilloxanthin (n = 13). The molecules were studied in acetone and CS2 solvents at room temperature. These experiments explore the effect of solvent polarity and polarizability on the spectroscopic and kinetic behavior of the molecules. The molecules were also studied in ether/isopentane/ethanol (EPA) glasses at 77 K, in which the spectral resolution is greatly enhanced. Analysis of the data using global fitting techniques has revealed the ultrafast dynamics of the excited states and spectral changes associated with their decay, including spectroscopic features not previously reported. The data are consistent with S* being identified with a twisted conformational structure, the yield of which is increased in molecules having longer pi-electron conjugations. In particular, for the longest molecule in the series, spirilloxanthin, the experiments and a detailed quantum computational analysis reveal the presence of two S* states associated with relaxed S1 (2(1)Ag-) conformations involving nearly planar 6-s-cis and 6-s-trans geometries. We propose that in polar solvents, the ground state of spirilloxanthin takes on a corkscrew conformation that generates a net solute dipole moment while decreasing the cavity formation energy. Upon excitation and relaxation into the S1 (2(1)Ag-) state, the polyene unravels and flattens into a more planar geometry with comparable populations of 6-s-trans and 6-s-cis conformations.

Spectral heterogeneity and carotenoid-to-bacteriochlorophyll energy transfer in LH2 light-harvesting complexes from Allochromatium vinosum

“…6 Photosynth Res internal conversion. The shape of the strong positive visible band in this third DADS contains features that can be attributed to N = 11 (rhodopin) and N = 12 (rhodovibrin or anhydrorhodovibrin) carotenoid chromophores which are known from previous work (Niedzwiedzki et al 2007(Niedzwiedzki et al , 2011a to have room temperature S 1 lifetimes of *4.3 ps (N = 11) and *2.2 ps (N = 12) which are within the experimental error of the lifetimes obtained from the present kinetic analysis. The fourth and fifth DADS components in the visible region (green and black dashed traces in the panels labeled VIS in Fig.…”

“…6), the 605 nm band is dominant. Based on the red-shift expected when the N value of an open-chain carotenoid is increased by one (Niedzwiedzki et al 2007(Niedzwiedzki et al , 2011a, the 605 nm feature can be assigned to an N = 12 carotenoid, which in the present case would be a combination of rhodovibrin and anhydrorhodovibrin, both of which are present in substantial amounts in these complexes (Table 1; Fig. 2).…”

“…The effect of having the S 1 energies of these longer carotenoids lies near or below the S 1 state of BChl a would inhibit the rate of carotenoid-to-BChl excitation energy transfer by reducing the amount of spectral overlap between the carotenoid donor emission bands and the BChl a acceptor absorption features which would have the result of lowering the energy transfer efficiency (Cong et al 2008). Another factor to be considered is that the intrinsic S 2 lifetime of carotenoids gets shorter with increasing N (Kosumi et al 2009;Niedzwiedzki et al 2007). Therefore, as a carotenoid chromophore gets longer, energy transfer from the S 2 state must compete with its shorter intrinsic S 2 lifetime.…”

Controlling the efficiency of an artificial light-harvesting complex

“…A mechanism based on the periodic excitation pulse enhancing the vibrational coherence of low-frequency wave packets via the ISRS process is most likely responsible for the control, analogous to that proposed earlier for the control in LH2 (22). However, in the dyad, the observed effect is smaller, perhaps illustrating the fact that the dyad in solution has more degrees of freedom and possible conformations in the ground and/or excited states (39,40). The low-frequency mode that is involved is not restricted by the environment and may gain energy attributable to intramolecular vibrational redistribution freely, hence leaving the effect of the selective excitation smaller than in the LH2 complex, in which such a mode is probably more inhibited.…”

Coherent control of biomolecules

“…A mechanism based on the periodic excitation pulse enhancing the vibrational coherence of low-frequency wavepackets via ISRS process is most likely responsible for the control, analogous to that proposed earlier for the control in LH2 [44]. However, in the dyad the observed effect is smaller, perhaps illustrating the fact that the dyad in solution has more degrees of freedom and possible conformations in the ground and/or excited states [122,123]. The low-frequency mode that is involved is not restricted by the environment and may gain energy due to intramolecular vibrational redistribution freely, hence leaving the effect of the selective excitation smaller than in LH2 complex, where such a mode is probably more inhibited.…”