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 A.; Moore, Ana L.; Batista, Victor S.; Robert, Bruno

doi:10.1073/pnas.1614857114

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

Journal Article · Mon Jun 26 00:00:00 EDT 2017 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1614857114· OSTI ID:1366576

Ho, Junming; Kish, Elizabeth; Méndez-Hernández, Dalvin D.; WongCarter, Katherine; Pillai, Smitha; Kodis, Gerdenis; Niklas, Jens; Poluektov, Oleg G.; Gust, Devens; Moore, Thomas A.; Moore, Ana L.; Batista, Victor S.;

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.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE; 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

Grant/Contract Number:: FG02-03ER15393; SC0001059; AC02-06CH11357

OSTI ID:: 1366576

Alternate ID(s):: OSTI ID: 1374200

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 23 works

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References (50)

Time-resolved resonance Raman spectroscopy of carotenoids in Triton X-100 micellar solution Conn, P. F.; Haley, J.; Lambert, C. R. Journal of the Chemical Society, Faraday Transactions, Vol. 89, Issue 11 https://doi.org/10.1039/ft9938901753	journal	January 1993
Excited State Properties of 3′-Hydroxyechinenone in Solvents and in the Orange Carotenoid Protein from Synechocystis sp. PCC 6803 Niedzwiedzki, Dariusz M.; Liu, Haijun; Blankenship, Robert E. The Journal of Physical Chemistry B, Vol. 118, Issue 23 https://doi.org/10.1021/jp5041794	journal	May 2014
Unravelling electronic and structural requisites of triplet–triplet energy transfer by advanced electron paramagnetic resonance and density functional theory Di Valentin, M.; Salvadori, E.; Barone, V. Molecular Physics, Vol. 111, Issue 18-19 https://doi.org/10.1080/00268976.2013.807368	journal	May 2013
Microwave and optical spectroscopy of carotenoid triplets in light-harvesting complex LHC II of spinach by absorbance-detected magnetic resonance van der Vos, R.; Carbonera, D.; Hoff, A. J. Applied Magnetic Resonance, Vol. 2, Issue 2 https://doi.org/10.1007/BF03166035	journal	June 1991
The Electronic Structure of the Photoexcited Triplet State of Free-Base (Tetraphenyl)porphyrin by Time-Resolved Electron−Nuclear Double Resonance and Density Functional Theory Kay, Christopher W. M. Journal of the American Chemical Society, Vol. 125, Issue 45 https://doi.org/10.1021/ja036278j	journal	November 2003
The electronic structure of the lutein triplet state in plant light-harvesting complex II Salvadori, Enrico; Di Valentin, Marilena; Kay, Christopher W. M. Physical Chemistry Chemical Physics, Vol. 14, Issue 35 https://doi.org/10.1039/c2cp40877e	journal	January 2012
S1 and T1 species of .beta.-carotene generated by direct photoexcitation from the all-trans, 9-cis, 13-cis, and 15-cis isomers as revealed by picosecond transient absorption and transient Raman spectroscopies Hashimoto, Hideki; Koyama, Yasushi; Hirata, Yoshinori The Journal of Physical Chemistry, Vol. 95, Issue 8 https://doi.org/10.1021/j100161a022	journal	April 1991
Universal Solvation Model Based on Solute Electron Density and on a Continuum Model of the Solvent Defined by the Bulk Dielectric Constant and Atomic Surface Tensions Marenich, Aleksandr V.; Cramer, Christopher J.; Truhlar, Donald G. The Journal of Physical Chemistry B, Vol. 113, Issue 18, p. 6378-6396 https://doi.org/10.1021/jp810292n	journal	May 2009
Ab Inito Study on Triplet Excitation Energy Transfer in Photosynthetic Light-Harvesting Complexes You, Zhi-Qiang; Hsu, Chao-Ping The Journal of Physical Chemistry A, Vol. 115, Issue 16 https://doi.org/10.1021/jp200200x	journal	April 2011
Unravelling the Origin of Intermolecular Interactions Using Absolutely Localized Molecular Orbitals Khaliullin, Rustam Z.; Cobar, Erika A.; Lochan, Rohini C. The Journal of Physical Chemistry A, Vol. 111, Issue 36 https://doi.org/10.1021/jp073685z	journal	September 2007
Identification of the Sites of Chlorophyll Triplet Quenching in Relation to the Structure of LHC-II from Higher Plants. Evidence from EPR Spectroscopy Di Valentin, Marilena; Biasibetti, Federico; Ceola, Stefano The Journal of Physical Chemistry B, Vol. 113, Issue 39 https://doi.org/10.1021/jp904012j	journal	October 2009
EPR Investigation of Photoinduced Radical Pair Formation and Decay to a Triplet State in a Carotene−Porphyrin−Fullerene Triad Carbonera, Donatella; Di Valentin, Marilena; Corvaja, Carlo Journal of the American Chemical Society, Vol. 120, Issue 18 https://doi.org/10.1021/ja9712074	journal	May 1998
Tuning the Spectroscopic Properties of Aryl Carotenoids by Slight Changes in Structure Fuciman, Marcel; Keşan, Gürkan; LaFountain, Amy M. The Journal of Physical Chemistry B, Vol. 119, Issue 4 https://doi.org/10.1021/jp512354r	journal	January 2015
Quantum organic photochemistry. I. Intramolecular potential energy surfaces for the lowest 3.pi..pi. state of polyenes Baird, N. Colin; West, Richard M. Journal of the American Chemical Society, Vol. 93, Issue 18 https://doi.org/10.1021/ja00747a015	journal	September 1971
Stereodynamics of intramolecular triplet energy transfer in carotenoporphyrins Gust, Devens; Moore, Thomas A.; Bensasson, Rene V. Journal of the American Chemical Society, Vol. 107, Issue 12 https://doi.org/10.1021/ja00298a038	journal	June 1985
Electronic Absorption and Ground State Structure of Carotenoid Molecules Mendes-Pinto, Maria M.; Sansiaume, Elodie; Hashimoto, Hideki The Journal of Physical Chemistry B, Vol. 117, Issue 38 https://doi.org/10.1021/jp309908r	journal	January 2013
The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals Zhao, Yan; Truhlar, Donald G. Theoretical Chemistry Accounts, Vol. 120, Issue 1-3 https://doi.org/10.1007/s00214-007-0310-x	journal	July 2007
Resonance Raman Spectra of Carotenoid Molecules: Influence of Methyl Substitutions Macernis, Mindaugas; Galzerano, Denise; Sulskus, Juozas The Journal of Physical Chemistry A, Vol. 119, Issue 1 https://doi.org/10.1021/jp510426m	journal	December 2014
Development and testing of a general amber force field Wang, Junmei; Wolf, Romain M.; Caldwell, James W. Journal of Computational Chemistry, Vol. 25, Issue 9 https://doi.org/10.1002/jcc.20035	journal	January 2004
Redesigning photosynthesis to sustainably meet global food and bioenergy demand Ort, Donald R.; Merchant, Sabeeha S.; Alric, Jean Proceedings of the National Academy of Sciences, Vol. 112, Issue 28 https://doi.org/10.1073/pnas.1424031112	journal	June 2015
Optical and optically detected magnetic resonance investigation on purple photosynthetic bacterial antenna complexes Angerhofer, A.; Bornhäuser, F.; Gall, A. Chemical Physics, Vol. 194, Issue 2-3 https://doi.org/10.1016/0301-0104(95)00022-G	journal	May 1995
The energies and kinetics of triplet carotenoids in the LH2 antenna complexes as determined by phosphorescence spectroscopy Rondonuwu, Ferdy S.; Taguchi, Tokio; Fujii, Ritsuko Chemical Physics Letters, Vol. 384, Issue 4-6 https://doi.org/10.1016/j.cplett.2003.12.024	journal	January 2004
Crystal structure of spinach major light-harvesting complex at 2.72 Å resolution Liu, Zhenfeng; Yan, Hanchi; Wang, Kebin Nature, Vol. 428, Issue 6980 https://doi.org/10.1038/nature02373	journal	March 2004
Long-range corrected hybrid density functionals with damped atom–atom dispersion corrections Chai, Jeng-Da; Head-Gordon, Martin Physical Chemistry Chemical Physics, Vol. 10, Issue 44 https://doi.org/10.1039/b810189b	journal	January 2008
The structures of S0 spheroidene in the light-harvesting (LH2) complex and S0 and T1 spheroidene in the reaction center of Rhodobacter sphaeroides 2.4.1 as revealed by Raman spectroscopy Ohashi, Naoto; Ko-Chi, Naomi; Kuki, Michitaka Biospectroscopy, Vol. 2, Issue 1 https://doi.org/10.1002/(SICI)1520-6343(1996)2:1<59::AID-BSPY6>3.0.CO;2-N	journal	January 1996
Vibrational frequency scaling factors for correlation consistent basis sets and the methods CC2 and MP2 and their spin-scaled SCS and SOS variants Friese, Daniel H.; Törk, Lisa; Hättig, Christof The Journal of Chemical Physics, Vol. 141, Issue 19 https://doi.org/10.1063/1.4901725	journal	November 2014
Mimicry of antenna and photo-protective carotenoid functions by a synthetic carotenoporphyrin Bensasson, René V.; Land, Edward J.; Moore, Ana L. Nature, Vol. 290, Issue 5804 https://doi.org/10.1038/290329a0	journal	March 1981
Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants Peterman, E. J.; Dukker, F. M.; van Grondelle, R. Biophysical Journal, Vol. 69, Issue 6 https://doi.org/10.1016/S0006-3495(95)80138-4	journal	December 1995
Transient EPR and Absorption Studies of Carotenoid Triplet Formation in Purple Bacterial Antenna Complexes Bittl, Robert; Schlodder, Eberhard; Geisenheimer, Irene The Journal of Physical Chemistry B, Vol. 105, Issue 23 https://doi.org/10.1021/jp0033014	journal	June 2001
Apoprotein structure in the LH2 complex from Rhodopseudomonas acidophila strain 10050: modular assembly and protein pigment interactions 1 1Edited by R. Huber Prince, S. M.; Papiz, M. Z.; Freer, A. A. Journal of Molecular Biology, Vol. 268, Issue 2 https://doi.org/10.1006/jmbi.1997.0966	journal	May 1997
Changes in Molecular Structure upon Triplet Excitation of All- trans -Spheroidene in n -Hexane Solution and 15- cis -Spheroidene Bound to the Photo-Reaction Center from Rhodobacter s phaeroides As Revealed by Resonance-Raman Spectroscopy and Normal-Coordinate Analysis ^† Mukai-Kuroda, Yumiko; Fujii, Ritsuko; Ko-chi, Naomi The Journal of Physical Chemistry A, Vol. 106, Issue 14 https://doi.org/10.1021/jp0130822	journal	April 2002
The fragment spin difference scheme for triplet-triplet energy transfer coupling You, Zhi-Qiang; Hsu, Chao-Ping The Journal of Chemical Physics, Vol. 133, Issue 7 https://doi.org/10.1063/1.3467882	journal	August 2010
Charge separation and energy transfer in carotenopyropheophorbide-quinone triads Liddell, Paul A.; Barrett, Donna.; Makings, Lewis R. Journal of the American Chemical Society, Vol. 108, Issue 17 https://doi.org/10.1021/ja00277a053	journal	August 1986
Triplet states of bacteriochlorophyll and carotenoids in chromatophores of photosynthetic bacteria Monger, Teresa G.; Cogdell, Richard J.; Parson, William W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 449, Issue 1 https://doi.org/10.1016/0005-2728(76)90013-X	journal	October 1976
Combining Quantum Mechanics Methods with Molecular Mechanics Methods in ONIOM Vreven, Thom; Byun, K. Suzie; Komáromi, István Journal of Chemical Theory and Computation, Vol. 2, Issue 3 https://doi.org/10.1021/ct050289g	journal	May 2006
Triplet-triplet energy transfer in B800–850 light-harvesting complexes of photosynthetic bacteria and synthetic carotenoporphyrin molecules investigated by electron spin resonance Frank, Harry A.; Chadwick, Barry W.; Jin Oh, Jung Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 892, Issue 3 https://doi.org/10.1016/0005-2728(87)90229-5	journal	July 1987
Application of the pople-santry-segal CNDO method to the cyclopropylcarbinyl and cyclobutyl cation and to bicyclobutane Wiberg, K. B. Tetrahedron, Vol. 24, Issue 3 https://doi.org/10.1016/0040-4020(68)88057-3	journal	January 1968
Carotenoid triplet detection by time-resolved EPR spectroscopy in carotenopyropheophorbide dyads Carbonera, Donatella; di Valentin, Marilena; Corvaja, Carlo Journal of Photochemistry and Photobiology A: Chemistry, Vol. 105, Issue 2-3 https://doi.org/10.1016/S1010-6030(96)04571-6	journal	May 1997
Energy Transfer from Carotenoid Polyenes to Porphyrins: a Light-Harvesting Antenna Moore, Ana L.; Dirks, Gary; Gust, Devens Photochemistry and Photobiology, Vol. 32, Issue 5 https://doi.org/10.1111/j.1751-1097.1980.tb04041.x	journal	November 1980
Molecular Adaptation of Photoprotection: Triplet States in Light-Harvesting Proteins Gall, Andrew; Berera, Rudi; Alexandre, Maxime T. A. Biophysical Journal, Vol. 101, Issue 4 https://doi.org/10.1016/j.bpj.2011.05.057	journal	August 2011
Light Absorption and Energy Transfer in Polyene-Porphyrin Esters Dirks, Gary; Moore, Ana L.; Moore, Thomas A. Photochemistry and Photobiology, Vol. 32, Issue 2 https://doi.org/10.1111/j.1751-1097.1980.tb04022.x	journal	August 1980
Raman and infrared spectra of the all-trans, 7-cis, 9-cis, 13-cis and 15-cis isomers of β-carotene: Key bands distinguishing stretched or terminal-bent configurations form central-bent configurations Koyama, Yasushi; Takatsuka, Ichiro; Nakata, Munetaka Journal of Raman Spectroscopy, Vol. 19, Issue 1 https://doi.org/10.1002/jrs.1250190107	journal	February 1988
EasySpin, a comprehensive software package for spectral simulation and analysis in EPR Stoll, Stefan; Schweiger, Arthur Journal of Magnetic Resonance, Vol. 178, Issue 1, p. 42-55 https://doi.org/10.1016/j.jmr.2005.08.013	journal	January 2006
Resonance Raman Spectra and Electronic Transitions in Carotenoids: A Density Functional Theory Study Macernis, Mindaugas; Sulskus, Juozas; Malickaja, Svetlana The Journal of Physical Chemistry A, Vol. 118, Issue 10 https://doi.org/10.1021/jp406449c	journal	February 2014
Photodriven charge separation in a carotenoporphyrin–quinone triad Moore, Thomas A.; Gust, Devens; Mathis, Paul Nature, Vol. 307, Issue 5952 https://doi.org/10.1038/307630a0	journal	February 1984
Photoisomerization of polyenes: Potential energy surfaces and normal mode analysis Ohmine, Iwao; Morokuma, Keiji The Journal of Chemical Physics, Vol. 73, Issue 4 https://doi.org/10.1063/1.440326	journal	August 1980
Global and target analysis of time-resolved spectra van Stokkum, Ivo H. M.; Larsen, Delmar S.; van Grondelle, Rienk Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1657, Issue 2-3 https://doi.org/10.1016/j.bbabio.2004.04.011	journal	July 2004
A Protein Dynamics Study of Photosystem II: The Effects of Protein Conformation on Reaction Center Function Vasil’ev, Sergej; Bruce, Doug Biophysical Journal, Vol. 90, Issue 9 https://doi.org/10.1529/biophysj.105.076075	journal	May 2006
Time-resolved resonance Raman spectroscopy of triplet .beta.-carotene produced from all-trans, 7-cis, 9-cis, 13-cis, and 15-cis isomers and high-pressure liquid chromatography analyses of photoisomerization via the triplet state Hashimoto, Hideki; Koyama, Yasushi The Journal of Physical Chemistry, Vol. 92, Issue 8 https://doi.org/10.1021/j100319a004	journal	April 1988
Energy transfer and fine structure axes determination in a hybrid porphyrin dimer oriented in a liquid crystal. Time resolved triplet EPR spectroscopy Gonen, Oded; Levanon, Haim The Journal of Chemical Physics, Vol. 84, Issue 8 https://doi.org/10.1063/1.450083	journal	April 1986

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

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