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Title: Triplet–triplet energy transfer in artificial and natural photosynthetic antennas

In photosynthetic organisms, protection against photo-oxidative 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, while it is ultrafast in the oxygen-rich chloroplasts of oxygen evolving photosynthetic organisms. In order 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 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 frommore » oxygenic (LHCII) and anoxygenic organisms (LH2). In conclusion, both DFT and EPR analysis further indicates that upon T-TET, the triplet wave function is localized on the carotenoid in both dyads.« less
Authors:
 [1] ;  [2] ;  [3] ;  [4] ;  [4] ;  [4] ;  [5] ;  [5] ;  [4] ;  [4] ;  [4] ;  [6] ; ORCiD logo [2]
  1. Yale Univ., New Haven, CT (United States); Institute of High Performance Computing (Singapore)
  2. Univ. Paris Sud, Gif sur Yvette (France)
  3. Yale Univ., New Haven, CT (United States); Univ. de Puerto Rico en Cayey, Cayey (Puerto Rico)
  4. Arizona State Univ., Tempe, AZ (United States)
  5. Argonne National Lab. (ANL), Argonne, IL (United States)
  6. Yale Univ., New Haven, CT (United States)
Publication Date:
Grant/Contract Number:
AC02-06CH11357; FG02-03ER15393; SC0001059
Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 114; Journal Issue: 28; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org:
European Research Council (ERC); Agence Nationale de la recherche (ANR); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22), Chemical Sciences, Geosciences, and Biosciences Division; USDOE
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; 59 BASIC BIOLOGICAL SCIENCES; artificial photosynthesis; DFT; EPR; QM/MM; carotenoid; natural bond orbital analysis; photoprotection; phthalocyanine; resonance Raman; transient absorption spectroscopy; triplet-triplet coupling; triplet-triplet energy transfer
OSTI Identifier:
1366576
Alternate Identifier(s):
OSTI ID: 1374200

Ho, Junming, Kish, Elizabeth, Méndez-Hernandez, Dalvin D., WongCarter, Katherine, Pillai, Smitha, Kodis, Gerdenis, Niklas, Jens, Poluektov, Oleg G., Gust, Devens, Moore, Thomas A., Moore, Ana L., Batista, Victor S., and Robert, Bruno. Triplet–triplet energy transfer in artificial and natural photosynthetic antennas. United States: N. p., Web. doi:10.1073/pnas.1614857114.
Ho, Junming, Kish, Elizabeth, Méndez-Hernandez, Dalvin D., WongCarter, Katherine, Pillai, Smitha, Kodis, Gerdenis, Niklas, Jens, Poluektov, Oleg G., Gust, Devens, Moore, Thomas A., Moore, Ana L., Batista, Victor S., & Robert, Bruno. Triplet–triplet energy transfer in artificial and natural photosynthetic antennas. United States. doi:10.1073/pnas.1614857114.
Ho, Junming, Kish, Elizabeth, Méndez-Hernandez, Dalvin D., WongCarter, Katherine, Pillai, Smitha, Kodis, Gerdenis, Niklas, Jens, Poluektov, Oleg G., Gust, Devens, Moore, Thomas A., Moore, Ana L., Batista, Victor S., and Robert, Bruno. 2017. "Triplet–triplet energy transfer in artificial and natural photosynthetic antennas". United States. doi:10.1073/pnas.1614857114.
@article{osti_1366576,
title = {Triplet–triplet energy transfer in artificial and natural photosynthetic antennas},
author = {Ho, Junming and Kish, Elizabeth and Méndez-Hernandez, Dalvin D. and WongCarter, Katherine and Pillai, Smitha and Kodis, Gerdenis and Niklas, Jens and Poluektov, Oleg G. and Gust, Devens and Moore, Thomas A. and Moore, Ana L. and Batista, Victor S. and Robert, Bruno},
abstractNote = {In photosynthetic organisms, protection against photo-oxidative 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, while it is ultrafast in the oxygen-rich chloroplasts of oxygen evolving photosynthetic organisms. In order 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 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). In conclusion, both DFT and EPR analysis further indicates that upon T-TET, the triplet wave function is localized on the carotenoid in both dyads.},
doi = {10.1073/pnas.1614857114},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 28,
volume = 114,
place = {United States},
year = {2017},
month = {6}
}

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