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Carotenoid Charge Transfer States and Their Role in Energy Transfer Processes in LH1–RC Complexes from Aerobic Anoxygenic Phototrophs

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Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
Department of Chemistry, University of Connecticut, 55 North Eagleville Road, Storrs, Connecticut 06269-3060, United States
§ Institute of Microbiology, Department of Phototrophic Microorganisms − Algatech, 379 81 Třeboň, Czech Republic
Biological Centre, Czech Academy of Sciences, Branišovská 31, 370 05 České Budějovice, Czech Republic
Cite this: J. Phys. Chem. B 2013, 117, 38, 10987–10999
Publication Date (Web):November 6, 2012
https://doi.org/10.1021/jp309278y
Copyright © 2012 American Chemical Society

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    Abstract

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    Light-harvesting complexes ensure necessary flow of excitation energy into photosynthetic reaction centers. In the present work, transient absorption measurements were performed on LH1–RC complexes isolated from two aerobic anoxygenic phototrophs (AAPs), Roseobacter sp. COL2P containing the carotenoid spheroidenone, and Erythrobacter sp. NAP1 which contains the carotenoids zeaxanthin and bacteriorubixanthinal. We show that the spectroscopic data from the LH1–RC complex of Roseobacter sp. COL2P are very similar to those previously reported for Rhodobacter sphaeroides, including the transient absorption spectrum originating from the intramolecular charge-transfer (ICT) state of spheroidenone. Although the ICT state is also populated in LH1–RC complexes of Erythrobacter sp. NAP1, its appearance is probably related to the polarity of the bacteriorubixanthinal environment rather than to the specific configuration of the carotenoid, which we hypothesize is responsible for populating the ICT state of spheroidenone in LH1–RC of Roseobacter sp. COL2P. The population of the ICT state enables efficient S1/ICT-to-bacteriochlorophyll (BChl) energy transfer which would otherwise be largely inhibited for spheroidenone and bacteriorubixanthinal due to their low energy S1 states. In addition, the triplet states of these carotenoids appear well-tuned for efficient quenching of singlet oxygen or BChl-a triplets, which is of vital importance for oxygen-dependent organisms such as AAPs.

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    Chromatogram demonstrating purity of bacteriorubixanthinal, global fitting results of bacteriorubixanthinal in solution and of LH1–RC from Roseobacter sp. COL2P in carotenoid radical region, kinetics of carotenoid signals in the LH1–RC complexes vs in solution together with BChl-a bleaching signal, comparison of LH1–RC transient absorption spectra of Roseobacter sp. COL2P and Rba. sphaeroides, and transient absorption spectra of LH1–RC complexes from Roseobacter sp. COL2P and Erythrobacter sp. NAP1 after excitation at 866 nm. This material is available free of charge via the Internet at http://pubs.acs.org.

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    5. Nao Yukihira, Chiasa Uragami, Kota Horiuchi, Daisuke Kosumi, Alastair T. Gardiner, Richard J. Cogdell, Hideki Hashimoto. Intramolecular charge-transfer enhances energy transfer efficiency in carotenoid-reconstituted light-harvesting 1 complex of purple photosynthetic bacteria. Communications Chemistry 2022, 5 (1) https://doi.org/10.1038/s42004-022-00749-6
    6. Hideki Hashimoto, Chiasa Uragami, Nao Yukihira, Kota Horiuchi, Richard J. Cogdell. Ultrafast laser spectroscopic studies on carotenoids in solution and on those bound to photosynthetic pigment-protein complexes. 2022, 1-51. https://doi.org/10.1016/bs.mie.2022.03.055
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    8. Elliot J. Taffet, Gregory D. Scholes. The A g + state falls below 3 A g - at carotenoid-relevant conjugation lengths. Chemical Physics 2018, 515 , 757-767. https://doi.org/10.1016/j.chemphys.2017.12.008
    9. Kasia Piwosz, David Kaftan, Jason Dean, Jiří Šetlík, Michal Koblížek. Nonlinear effect of irradiance on photoheterotrophic activity and growth of the aerobic anoxygenic phototrophic bacterium Dinoroseobacter shibae. Environmental Microbiology 2018, 20 (2) , 724-733. https://doi.org/10.1111/1462-2920.14003
    10. A. P. Razjivin, E. P. Lukashev, V. O. Kompanets, V. S. Kozlovsky, A. A. Ashikhmin, S. V. Chekalin, A. A. Moskalenko, V. Z. Paschenko. Excitation energy transfer from the bacteriochlorophyll Soret band to carotenoids in the LH2 light-harvesting complex from Ectothiorhodospira haloalkaliphila is negligible. Photosynthesis Research 2017, 133 (1-3) , 289-295. https://doi.org/10.1007/s11120-017-0341-7
    11. Dariusz M. Niedzwiedzki, Preston L. Dilbeck, Qun Tang, Elizabeth C. Martin, David F. Bocian, C. Neil Hunter, Dewey Holten. New insights into the photochemistry of carotenoid spheroidenone in light-harvesting complex 2 from the purple bacterium Rhodobacter sphaeroides. Photosynthesis Research 2017, 131 (3) , 291-304. https://doi.org/10.1007/s11120-016-0322-2
    12. Vladimir Yurkov, Elizabeth Hughes. Aerobic Anoxygenic Phototrophs: Four Decades of Mystery. 2017, 193-214. https://doi.org/10.1007/978-3-319-46261-5_6
    13. Vadim Selyanin, Dzmitry Hauruseu, Michal Koblížek. The variability of light-harvesting complexes in aerobic anoxygenic phototrophs. Photosynthesis Research 2016, 128 (1) , 35-43. https://doi.org/10.1007/s11120-015-0197-7
    14. Michal Koblížek, . Ecology of aerobic anoxygenic phototrophs in aquatic environments. FEMS Microbiology Reviews 2015, 39 (6) , 854-870. https://doi.org/10.1093/femsre/fuv032
    15. Yuki Sato-Takabe, Koji Hamasaki, Koji Suzuki. Photosynthetic Competence of the Marine Aerobic Anoxygenic Phototrophic Bacterium Roseobacter sp. under Organic Substrate Limitation. Microbes and Environments 2014, 29 (1) , 100-103. https://doi.org/10.1264/jsme2.ME13130

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