An unusual pathway of excitation energy deactivation in carotenoids: singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna

Abstract

Carotenoids are important biomolecules that are ubiquitous in nature and find widespread application in medicine. In photosynthesis, they have a large role in light harvesting (LH) and photoprotection. They exert their LH function by donating their excited singlet state to nearby (bacterio)chlorophyll molecules. In photosynthetic bacteria, the efficiency of this energy transfer process can be as low as 30%. Here, we present evidence that an unusual pathway of excited state relaxation in carotenoids underlies this poor LH function, by which carotenoid triplet states are generated directly from carotenoid singlet states. This pathway, operative on a femtosecond and picosecond timescale, involves an intermediate state, which we identify as a new, hitherto uncharacterized carotenoid singlet excited state. In LH complex-bound carotenoids, this state is the precursor on the reaction pathway to the triplet state, whereas in extracted carotenoids in solution, this state returns to the singlet ground state without forming any triplets. We discuss the possible identity of this excited state and argue that fission of the singlet state into a pair of triplet states on individual carotenoid molecules constitutes the mechanism by which the triplets are generated. This is, to our knowledge, the first ever direct observation of a singlet-to-triplet conversion process on an ultrafast timescale in a photosynthetic antenna.

Figure 1

The absorption spectra of the R. rubrum membrane fragments at RT (solid line), purified LH1 complexes at 77 K (dashed line), and extracted Spx dissolved in n-hexane at RT (dotted line).

Figure 2

(A) SADS and associated lifetimes for Spx in n-hexane upon 475-nm excitation at RT. Note that the third SADS has been expanded by a factor of 2. (B). Target analysis by using the kinetic model shown (Inset). The arrows indicate exponential decays, with the numbers being the corresponding lifetimes, in picoseconds. The spectra represent the difference absorption of each state (S₂, S₁, and S*), normalized to a concentration of unity. The spectrum of S* was set to zero above 605 nm (see text for details).

Figure 3

SADS and lifetimes characterizing the spectral evolution of the TA induced by 540-nm excitation in membrane fragments from R. rubrum, at RT. The species generated by the laser pulse (dashed) is replaced with a time constant of 60 fs by the next one (dotted), which in turn decays in 1.45 ps into the dot-dashed spectrum. This species evolves in ≈5.3 ps into a long-lived species (solid), whose lifetime was set to 1 ns in the global analysis.

Figure 4

Global analysis results (SADS and associated lifetimes) of the TA data obtained in the visible (A) and near IR (B) after 540 nm excitation in purified LH1, at 77 K.

Figure 5

Target analysis of the TA data obtained for LH1 at 77 K. (A) The model used for target analysis. The numbers represent the reciprocals of the microscopic decay rates, in picoseconds. (B) The difference spectra associated to the Spx states S₂, S₁, and S* and T₁ from A.