Photoprotection Mechanism of Light-Harvesting Antenna Complex from Purple Bacteria

Kosumi, Daisuke; Horibe, Tomoko; Sugisaki, Mitsuru; Cogdell, Richard J.; Hashimoto, Hideki

doi:10.1021/acs.jpcb.6b00121

Photoprotection Mechanism of Light-Harvesting Antenna Complex from Purple Bacteria

Journal Article · Fri Jan 22 00:00:00 EST 2016 · Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry

DOI:https://doi.org/10.1021/acs.jpcb.6b00121· OSTI ID:1387525

Kosumi, Daisuke ^[1]; Horibe, Tomoko ^[2]; Sugisaki, Mitsuru ^[3]; Cogdell, Richard J. ^[4]; Hashimoto, Hideki ^[2]

Kumamoto Univ., Kumamoto (Japan). Inst. of Pulsed Power Science
Kwansei Gakuin Univ., Gakuen (Japan)
Osaka City Univ., Osaka (Japan)
Univ. of Glasgow, Scotland (United Kingdom). Glasgow Biomedical Research Centre

Photosynthetic light-harvesting apparatus efficiently capture sunlight and transfer the energy to reaction centers, while they safely dissipate excess energy to surrounding environments for a protection of their organisms. Here in this study, we performed pump–probe spectroscopic measurements with a temporal window ranging from femtosecond to submillisecond on the purple bacterial antenna complex LH2 from Rhodobacter sphaeroides 2.4.1 to clarify its photoprotection functions. The observed excited state dynamics in the time range from subnanosecond to microsecond exhibits that the triplet–triplet excitation energy transfer from bacteriochlorophyll a to carotenoid takes place with a time constant of 16.7 ns. Furthermore, ultrafast spectroscopic data suggests that a molecular assembly of bacteriochlorophyll $$\alpha$$ in LH2 efficiently suppresses a generation of triple bacteriochlorophyll $$\alpha$$ .

View Accepted Manuscript (DOE)

Research Organization:: Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC); Washington Univ., St. Louis, MO (United States)

Sponsoring Organization:: Japan Society for the Promotion of Science; USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

Grant/Contract Number:: SC0001035

OSTI ID:: 1387525

Journal Information:: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry, Journal Name: Journal of Physical Chemistry. B, Condensed Matter, Materials, Surfaces, Interfaces and Biophysical Chemistry Journal Issue: 5 Vol. 120; ISSN 1520-6106

Publisher:: American Chemical SocietyCopyright Statement

Country of Publication:: United States

Language:: English

References (43)

Ultrafast Energy-Transfer Pathway in a Purple-Bacterial Photosynthetic Core Antenna, as Revealed by Femtosecond Time-Resolved Spectroscopy Kosumi, Daisuke; Maruta, Satoshi; Horibe, Tomoko Angewandte Chemie International Edition, Vol. 50, Issue 5 https://doi.org/10.1002/anie.201003771	journal	December 2010
Excited-State Dynamics of Pentacene Derivatives with Stable Radical Substituents Ito, Akitaka; Shimizu, Akihiro; Kishida, Noriaki Angewandte Chemie International Edition, Vol. 53, Issue 26 https://doi.org/10.1002/anie.201310291	journal	April 2014
The dependence of excitation energy transfer pathways on conjugation length of carotenoids in purple bacterial photosynthetic antennae Maruta, Satoshi; Kosumi, Daisuke; Horibe, Tomoko physica status solidi (b), Vol. 248, Issue 2 https://doi.org/10.1002/pssb.201000687	journal	November 2010
Triplet state spectra and dynamics of peridinin analogs having different extents of π-electron conjugation Kaligotla, Shanti; Doyle, Sara; Niedzwiedzki, Dariusz M. Photosynthesis Research, Vol. 103, Issue 3 https://doi.org/10.1007/s11120-010-9535-y	journal	February 2010
Singlet and triplet excited state properties of natural chlorophylls and bacteriochlorophylls Niedzwiedzki, Dariusz M.; Blankenship, Robert E. Photosynthesis Research, Vol. 106, Issue 3 https://doi.org/10.1007/s11120-010-9598-9	journal	November 2010
Triplet excited state spectra and dynamics of carotenoids from the thermophilic purple photosynthetic bacterium Thermochromatium tepidum Niedzwiedzki, Dariusz M.; Kobayashi, Masayuki; Blankenship, Robert E. Photosynthesis Research, Vol. 107, Issue 2 https://doi.org/10.1007/s11120-011-9620-x	journal	January 2011
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
Fluorescence and excited state absorption in modified pigments of bacterial photosynthesis a comparative study of metal-substituted bacteriochlorophylls a Teuchner, K.; Stiel, H.; Leupold, D. Journal of Luminescence, Vol. 72-74 https://doi.org/10.1016/S0022-2313(96)00411-5	journal	June 1997
Ultrafast relaxation kinetics of the dark S1 state in all-trans-β-carotene explored by one- and two-photon pump–probe spectroscopy Kosumi, Daisuke; Abe, Kenta; Karasawa, Hiroshi Chemical Physics, Vol. 373, Issue 1-2 https://doi.org/10.1016/j.chemphys.2009.12.013	journal	July 2010
One- and two-photon pump–probe optical spectroscopic measurements reveal the S1 and intramolecular charge transfer states are distinct in fucoxanthin Kosumi, Daisuke; Kusumoto, Toshiyuki; Fujii, Ritsuko Chemical Physics Letters, Vol. 483, Issue 1-3 https://doi.org/10.1016/j.cplett.2009.10.077	journal	November 2009
The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes Cogdell, Richard J.; Gall, Andrew; Köhler, Jürgen Quarterly Reviews of Biophysics, Vol. 39, Issue 3 https://doi.org/10.1017/S0033583506004434	journal	August 2006
Molecular Factors Controlling Photosynthetic Light Harvesting by Carotenoids Polívka, Tomáš; Frank, Harry A. Accounts of Chemical Research, Vol. 43, Issue 8 https://doi.org/10.1021/ar100030m	journal	August 2010
Photosynthetic Light-Harvesting Pigment−Protein Complexes: Toward Understanding How and Why Pullerits, Tõnu; Sundström, Villy Accounts of Chemical Research, Vol. 29, Issue 8 https://doi.org/10.1021/ar950110o	journal	January 1996
Ultrafast Carotenoid Band Shifts Probe Structure and Dynamics in Photosynthetic Antenna Complexes ^† Herek, J. L.; Polívka, T.; Pullerits, T. Biochemistry, Vol. 37, Issue 20 https://doi.org/10.1021/bi980118g	journal	May 1998
Ultrafast Dynamics of Carotenoid Excited States−From Solution to Natural and Artificial Systems Polívka, Tomáš; Sundström, Villy Chemical Reviews, Vol. 104, Issue 4 https://doi.org/10.1021/cr020674n	journal	April 2004
Photosystem II Does Not Possess a Simple Excitation Energy Funnel: Time-Resolved Fluorescence Spectroscopy Meets Theory Shibata, Yutaka; Nishi, Shunsuke; Kawakami, Keisuke Journal of the American Chemical Society, Vol. 135, Issue 18 https://doi.org/10.1021/ja312586p	journal	April 2013
Ultrafast Carotenoid Band Shifts: Experiment and Theory ^† Herek, J. L.; Wendling, M.; He, Z. The Journal of Physical Chemistry B, Vol. 108, Issue 29 https://doi.org/10.1021/jp040094p	journal	July 2004
Photophysical Properties of the Excited States of Bacteriochlorophyll f in Solvents and in Chlorosomes Niedzwiedzki, Dariusz M.; Orf, Gregory S.; Tank, Marcus The Journal of Physical Chemistry B, Vol. 118, Issue 9 https://doi.org/10.1021/jp409495m	journal	January 2014
Ultrafast Time-Resolved Carotenoid to-Bacteriochlorophyll Energy Transfer in LH2 Complexes from Photosynthetic Bacteria Cong, Hong; Niedzwiedzki, Dariusz M.; Gibson, George N. The Journal of Physical Chemistry B, Vol. 112, Issue 34 https://doi.org/10.1021/jp711946w	journal	August 2008
Exciton Delocalization Length in the B850 Antenna of Rhodobacter sphaeroides Pullerits, Tõnu; Chachisvilis, Mirianas; Sundström, Villy The Journal of Physical Chemistry, Vol. 100, Issue 25 https://doi.org/10.1021/jp953639b	journal	January 1996
Superradiance and Exciton Delocalization in Bacterial Photosynthetic Light-Harvesting Systems Monshouwer, René; Abrahamsson, Malin; van Mourik, Frank The Journal of Physical Chemistry B, Vol. 101, Issue 37 https://doi.org/10.1021/jp963377t	journal	September 1997
Time-Resolved Spectral Investigation of Bacteriochlorophyll a and Its Transmetalated Derivatives [Zn]-Bacteriochlorophyll a and [Pd]-Bacteriochlorophyll a Musewald, Christian; Hartwich, Gerhard; Pöllinger-Dammer, Florian The Journal of Physical Chemistry B, Vol. 102, Issue 42 https://doi.org/10.1021/jp982309z	journal	October 1998
Photosynthetic Light-Harvesting: Reconciling Dynamics and Structure of Purple Bacterial LH2 Reveals Function of Photosynthetic Unit Sundström, Villy; Pullerits, Tõnu; van Grondelle, Rienk The Journal of Physical Chemistry B, Vol. 103, Issue 13 https://doi.org/10.1021/jp983722+	journal	March 1999
Control Mechanism of Excitation Energy Transfer in a Complex Consisting of Photosystem II and Fucoxanthin Chlorophyll a / c -Binding Protein Nagao, Ryo; Yokono, Makio; Tomo, Tatsuya The Journal of Physical Chemistry Letters, Vol. 5, Issue 17 https://doi.org/10.1021/jz501496p	journal	August 2014
Femto- to Microsecond Photodynamics of an Unusual Bacteriophytochrome Mathes, Tilo; Ravensbergen, Janneke; Kloz, Miroslav The Journal of Physical Chemistry Letters, Vol. 6, Issue 2 https://doi.org/10.1021/jz502408n	journal	December 2014
Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria McDermott, G.; Prince, S. M.; Freer, A. A. Nature, Vol. 374, Issue 6522 https://doi.org/10.1038/374517a0	journal	April 1995
Molecular basis of photoprotection and control of photosynthetic light-harvesting Pascal, Andrew A.; Liu, Zhenfeng; Broess, Koen Nature, Vol. 436, Issue 7047 https://doi.org/10.1038/nature03795	journal	July 2005
Identification of a mechanism of photoprotective energy dissipation in higher plants Ruban, Alexander V.; Berera, Rudi; Ilioaia, Cristian Nature, Vol. 450, Issue 7169 https://doi.org/10.1038/nature06262	journal	November 2007
Structure of the LH1–RC complex from Thermochromatium tepidum at 3.0 Å Niwa, Satomi; Yu, Long-Jiang; Takeda, Kazuki Nature, Vol. 508, Issue 7495 https://doi.org/10.1038/nature13197	journal	March 2014
Mechanism of photoprotection in the cyanobacterial ancestor of plant antenna proteins Staleva, Hristina; Komenda, Josef; Shukla, Mahendra K. Nature Chemical Biology, Vol. 11, Issue 4 https://doi.org/10.1038/nchembio.1755	journal	February 2015
On the origin of ultrafast nonradiative transitions in nitro-polycyclic aromatic hydrocarbons: Excited-state dynamics in 1-nitronaphthalene Reichardt, Christian; Vogt, R. Aaron; Crespo-Hernández, Carlos E. The Journal of Chemical Physics, Vol. 131, Issue 22 https://doi.org/10.1063/1.3272536	journal	December 2009
Ultrafast excited state dynamics of spirilloxanthin in solution and bound to core antenna complexes: Identification of the S* and T ₁ states Kosumi, Daisuke; Maruta, Satoshi; Horibe, Tomoko The Journal of Chemical Physics, Vol. 137, Issue 6 https://doi.org/10.1063/1.4737129	journal	August 2012
Broadband ultraviolet-visible transient absorption spectroscopy in the nanosecond to microsecond time domain with sub-nanosecond time resolution Lang, Bernhard; Mosquera-Vázquez, Sandra; Lovy, Dominique Review of Scientific Instruments, Vol. 84, Issue 7 https://doi.org/10.1063/1.4812705	journal	July 2013
An unusual pathway of excitation energy deactivation in carotenoids: Singlet-to-triplet conversion on an ultrafast timescale in a photosynthetic antenna Gradinaru, C. C.; Kennis, J. T. M.; Papagiannakis, E. Proceedings of the National Academy of Sciences, Vol. 98, Issue 5 https://doi.org/10.1073/pnas.051501298	journal	February 2001
On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls Bode, S.; Quentmeier, C. C.; Liao, P. -N. Proceedings of the National Academy of Sciences, Vol. 106, Issue 30 https://doi.org/10.1073/pnas.0903536106	journal	July 2009
An alternative carotenoid-to-bacteriochlorophyll energy transfer pathway in photosynthetic light harvesting Papagiannakis, E.; Kennis, J. T. M.; van Stokkum, I. H. M. Proceedings of the National Academy of Sciences, Vol. 99, Issue 9 https://doi.org/10.1073/pnas.092626599	journal	April 2002
Fluorescence and photobleaching dynamics of single light-harvesting complexes Bopp, M. A.; Jia, Y.; Li, L. Proceedings of the National Academy of Sciences, Vol. 94, Issue 20 https://doi.org/10.1073/pnas.94.20.10630	journal	September 1997
Comparison of transient grating signals from spheroidene in an organic solvent and in pigment-protein complexes from Rhodobacter sphaeroides 2.4.1 Sugisaki, Mitsuru; Fujiwara, Masazumi; Kosumi, Daisuke Physical Review B, Vol. 81, Issue 24 https://doi.org/10.1103/PhysRevB.81.245112	journal	June 2010
Exciton Delocalization Probed by Excitation Annihilation in the Light-Harvesting Antenna LH2 Trinkunas, G.; Herek, J. L.; Polívka, T. Physical Review Letters, Vol. 86, Issue 18 https://doi.org/10.1103/PhysRevLett.86.4167	journal	April 2001
Carotenoids in Photosynthesis Frank, Harry A.; Cogdell, Richard J. Photochemistry and Photobiology, Vol. 63, Issue 3 https://doi.org/10.1111/j.1751-1097.1996.tb03022.x	journal	March 1996
Crystal Structure of the RC-LH1 Core Complex from Rhodopseudomonas palustris Roszak, A. W. Science, Vol. 302, Issue 5652 https://doi.org/10.1126/science.1088892	journal	December 2003
Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein Ahn, T. K.; Avenson, T. J.; Ballottari, M. Science, Vol. 320, Issue 5877 https://doi.org/10.1126/science.1154800	journal	May 2008
Phycobilisomes Supply Excitations to Both Photosystems in a Megacomplex in Cyanobacteria Liu, H.; Zhang, H.; Niedzwiedzki, D. M. Science, Vol. 342, Issue 6162 https://doi.org/10.1126/science.1242321	journal	November 2013

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Photoprotection Mechanism of Light-Harvesting Antenna Complex from Purple Bacteria

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