Triplet–triplet energy transfer in artificial and natural photosynthetic antennas

Abstract

In photosynthetic organisms, protection against photooxidative stress due to singlet oxygen is provided by carotenoid molecules, which quench chlorophyll triplet species before they can sensitize singlet oxygen formation. In anoxygenic photosynthetic organisms, in which exposure to oxygen is low, chlorophyll-to-carotenoid triplet-triplet energy transfer (T-TET) is slow, in the tens of nanoseconds range, whereas it is ultrafast in the oxygen-rich chloroplasts of oxygen-evolving photosynthetic organisms. To better understand the structural features and resulting electronic coupling that leads to T-TET dynamics adapted to ambient oxygen activity, we have carried out experimental and theoretical studies of two isomeric carotenoporphyrin molecular dyads having different conformations and therefore different interchromophore electronic interactions. This pair of dyads reproduces the characteristics of fast and slow T-TET, including a resonance Raman-based spectroscopic marker of strong electronic coupling and fast T-TET that has been observed in photosynthesis. As identified by density functional theory (DFT) calculations, the spectroscopic marker associated with fast T-TET is due primarily to a geometrical perturbation of the carotenoid backbone in the triplet state induced by the interchromophore interaction. This is also the case for the natural systems, as demonstrated by the hybrid quantum mechanics/molecular mechanics (QM/MM) simulations of light-harvesting proteins from oxygenic (LHCII) and anoxygenic organisms (LH2). Both DFT and electron paramagnetic resonance (EPR) analyses further indicate that, upon T-TET, the triplet wave function is localized on the carotenoid in both dyads.artificial photosynthesis | photoprotection | DFT calculations | triplet-triplet energy transfer | resonance Raman P hotoprotection is central to the maintenance of photosynthesis. Under certain circumstances, chlorophyll excited triplet states may form from intersystem crossing and from electron-hole recombination reactions in reaction centers. Chlorophyll triplet species can sensitize the formation of singlet oxygen, a deleterious reactive oxygen species (1). In photosynthetic complexes, this sensitization reaction is precluded by sufficiently rapid transfer of the triplet excited state from chlorophyll (Chl) or bacteriochlorophyll (BChl) to carotenoid molecules. The triplet states of carotenoids involved in photoprotection are well below the energy of singlet oxygen and therefore do not sensitize singlet oxygen. This quenching reaction reduces the lifetime of the Chl or BChl triplet state by many orders of magnitude (1) and renders it kinetically incompetent to sensitize singlet oxygen. Moreover, carotenoids can quench singlet oxygen directly in the event that it is inadvertently formed.In the light-harvesting (LH) proteins from most (anoxygenic) purple bacteria, triplet-triplet energy transfer (T-TET) from BChl to carotenoid molecules occurs on the nanosecond timescale (2, 3). By contrast, in light-harvesting complexes (LHCs) from...

Carotenoid composition and conformation in retinal oil droplets of the domestic chicken*

“…It is possible that significant inter-molecular interactions occur between carotenoid molecules, particularly given the high carotenoid concentration in the droplets. Such packing interactions may result in constraints in their conformation, as previously described for inter-chromophore interactions in caroteno-porphyrin dyads [19]. However, given the mixture of carotenoids present in each droplet, and with no obvious mechanism for controlling these interactions, it is hard to imagine how they could be homogeneous enough for each carotenoid species to give the ν 4 structure observed here.…”

Optical Properties of Isolated and Covalent Organic Framework-Embedded Ruthenium Complexes

“…This mechanism requires the excitation of both the catalyst and substrate to a spin-triplet state and has been the subject of both theoretical 27 and application-oriented investigations. 28 The Ru(2,2′-bipyridine) 3 2+ has been exploited in a number of C–C making and breaking transformations, such as trans/cis stilbene isomerization, 29 anthracene dimerization, 30 cycloadditions, 31 and trifluoromethylations of styrene substrates 32 via the TTET mechanism.…”

Electronic Structure and Triplet–Triplet Energy Transfer in Artificial Photosynthetic Antennas

“…Such fast T‐T transfer has not only been measured in plant LHCII, but also in the peridinin‐chlorophyll protein and fucoxanthin‐chlorophyll protein of algae suggesting that it is conserved in oxygenic photosynthesis. It has been postulated that such ultrafast quenching of the triplet state of chlorophylls is an example of a molecular photoprotective adaptation that took place during the evolution of oxygenic photosynthesis .…”