TY - JOUR
T1 - Triplet-triplet energy transfer in artificial and natural photosynthetic antennas
AU - Ho, Junming
AU - Kish, Elizabeth
AU - Méndez-Hernández, Dalvin D.
AU - WongCarter, Katherine
AU - Pillai, Smitha
AU - Kodis, Gerdenis
AU - Niklas, Jens
AU - Poluektov, Oleg G.
AU - Gust, Devens
AU - Moore, Thomas
AU - Moore, Ana
AU - Batista, Victor S.
AU - Robert, Bruno
AU - Gray, Harry B.
N1 - Funding Information:
This work was supported by the European Research Council funding agency (PHOTPROT project) and by Agence Nationale de la Recherche (ANR) (Cyanoprotect Project). This work was supported by the French Infrastructure for Integrated Structural Biology (FRISBI) ANR-10-INSB-05-01. The synthesis and transient absorption spectroscopy were funded by the Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Energy Biosciences, Department of Energy, under Contract DE-FG02-03ER15393. Computational work was funded by the Singapore Agency for Science, Technology and Research (J.H.). V.S.B. acknowledges support from NIH Grant GM106121 and high-performance computing facilities from the National Energy Research Scientific Computing Center (NERSC). EPR experiments were supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Biosciences, under Contract DE-AC02-06CH11357 at Argonne National Laboratory (to J.N. and O.G.P.).
PY - 2017/7/11
Y1 - 2017/7/11
N2 - 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.
AB - 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.
KW - Artificial photosynthesis
KW - DFT calculations
KW - Photoprotection
KW - Resonance Raman
KW - Triplet-triplet energy transfer
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U2 - 10.1073/pnas.1614857114
DO - 10.1073/pnas.1614857114
M3 - Article
C2 - 28652359
AN - SCOPUS:85023201423
SN - 0027-8424
VL - 114
SP - E5513-E5521
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 28
ER -