Triplet-triplet energy transfer in artificial and natural photosynthetic antennas

Junming Ho, Elizabeth Kish, Dalvin D. Méndez-Hernández, Katherine WongCarter, Smitha Pillai, Gerdenis Kodis, Jens Niklas, Oleg G. Poluektov, Devens Gust, Thomas Moore, Ana Moore, Victor S. Batista, Bruno Robert, Harry B. Gray

Research output: Contribution to journalArticle

6 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)E5513-E5521
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number28
DOIs
StatePublished - Jul 11 2017

Fingerprint

Energy Transfer
Carotenoids
Oxygen
Singlet Oxygen
Chlorophyll
Mechanics
Electron Spin Resonance Spectroscopy
Photosynthesis
Chloroplasts
Theoretical Models
Light
Proteins

Keywords

  • Artificial photosynthesis
  • DFT calculations
  • Photoprotection
  • Resonance Raman
  • Triplet-triplet energy transfer

ASJC Scopus subject areas

  • General

Cite this

Triplet-triplet energy transfer in artificial and natural photosynthetic antennas. / Ho, Junming; Kish, Elizabeth; Méndez-Hernández, Dalvin D.; WongCarter, Katherine; Pillai, Smitha; Kodis, Gerdenis; Niklas, Jens; Poluektov, Oleg G.; Gust, Devens; Moore, Thomas; Moore, Ana; Batista, Victor S.; Robert, Bruno; Gray, Harry B.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 28, 11.07.2017, p. E5513-E5521.

Research output: Contribution to journalArticle

Ho, J, Kish, E, Méndez-Hernández, DD, WongCarter, K, Pillai, S, Kodis, G, Niklas, J, Poluektov, OG, Gust, D, Moore, T, Moore, A, Batista, VS, Robert, B & Gray, HB 2017, 'Triplet-triplet energy transfer in artificial and natural photosynthetic antennas', Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 28, pp. E5513-E5521. https://doi.org/10.1073/pnas.1614857114
Ho, Junming ; Kish, Elizabeth ; Méndez-Hernández, Dalvin D. ; WongCarter, Katherine ; Pillai, Smitha ; Kodis, Gerdenis ; Niklas, Jens ; Poluektov, Oleg G. ; Gust, Devens ; Moore, Thomas ; Moore, Ana ; Batista, Victor S. ; Robert, Bruno ; Gray, Harry B. / Triplet-triplet energy transfer in artificial and natural photosynthetic antennas. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 28. pp. E5513-E5521.
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AU - Kodis, Gerdenis

AU - Niklas, Jens

AU - Poluektov, Oleg G.

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