ACS Publications. Most Trusted. Most Cited. Most Read
My Activity

Figure 1Loading Img

Ultrafast Formation of a Carotenoid Radical in LH2 Antenna Complexes of Purple Bacteria

View Author Information
Department of Chemical Physics, Lund University, Box 124, S-22100 Lund, Sweden, Department of Chemistry, University of Connecticut, Storrs, Connecticut 06269-3060, and Division of Biochemistry and Molecular Biology, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow G12 8QQ, U.K.
Cite this: J. Phys. Chem. B 2004, 108, 39, 15398–15407
Publication Date (Web):August 27, 2004
Copyright © 2004 American Chemical Society

    Article Views





    Other access options


    The S1-mediated carotenoid to BChl a energy-transfer pathway and carotenoid radical formation have been studied using femtosecond time-resolved transient absorption spectroscopy. A series of LH2 complexes (LH2 = light-harvesting complex 2) from Rhodobacter sphaeroides incorporating carotenoids neurosporene, spheroidene, and spheroidenone were used to explore the effect of conjugation length. The S1 lifetimes of carotenoids in the LH2 complex are significantly shorter than in solution, resulting in efficiencies of the S1-mediated energy transfer of 94%, 82%, and 76%, respectively. In addition to the S1 decay, a low-amplitude component of ∼9 ps was revealed for all carotenoids in LH2 and assigned to the S* state. Besides energy transfer, excitation of the carotenoid S2 state in LH2 complexes also leads to the formation of a carotenoid radical, and this pathway is also conjugation length dependent. The carotenoid radical is formed as a result of electron transfer between the carotenoid and B800 BChl a molecules. The yield of the radical formation is highest for neurosporene (10−15%), while a lower efficiency was observed for spheroidene (5−8%). For spheroidenone, no distinct radical signal was found. The precursor of the carotenoid radical is a charge-transfer state that is populated directly from the S2 state. This charge-transfer state, which represents an excited state of the carotenoid−B800 complex, decays in 300 fs (neurosporene) or 400 fs (spheroidene) to form ground-state carotenoid cation and BChl anion. The charge-separated state has a lifetime of 2 ps (neurosporene) and 8 ps (spheroidene).

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.


    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

     Lund University.


     To whom correspondence should be addressed. E-mail:  tomas. [email protected]. Fax:  +46-46-2224119.

     University of Connecticut.


     University of Glasgow.

    Cited By

    This article is cited by 64 publications.

    1. Jin-Fang Hao, Nami Yamano, Chen-Hui Qi, Yan Zhang, Fei Ma, Peng Wang, Long-Jiang Yu, Jian-Ping Zhang. Carotenoid-Mediated Long-Range Energy Transfer in the Light Harvesting–Reaction Center Complex from Photosynthetic Bacterium Roseiflexus castenholzii. The Journal of Physical Chemistry B 2023, 127 (48) , 10360-10369.
    2. Dariusz M. Niedzwiedzki, C. Neil Hunter, and Robert E. Blankenship . Evaluating the Nature of So-Called S*-State Feature in Transient Absorption of Carotenoids in Light-Harvesting Complex 2 (LH2) from Purple Photosynthetic Bacteria. The Journal of Physical Chemistry B 2016, 120 (43) , 11123-11131.
    3. Gürkan Keşan, Milan Durchan, Josef Tichý, Babak Minofar, Valentyna Kuznetsova, Marcel Fuciman, Václav Šlouf, Cemal Parlak, and Tomáš Polívka . Different Response of Carbonyl Carotenoids to Solvent Proticity Helps To Estimate Structure of the Unknown Carotenoid from Chromera velia. The Journal of Physical Chemistry B 2015, 119 (39) , 12653-12663.
    4. Václav Šlouf, Marcel Fuciman, Alexander Dulebo, David Kaftan, Michal Koblížek, Harry A. Frank, and Tomáš Polívka . Carotenoid Charge Transfer States and Their Role in Energy Transfer Processes in LH1–RC Complexes from Aerobic Anoxygenic Phototrophs. The Journal of Physical Chemistry B 2013, 117 (38) , 10987-10999.
    5. Samuel D. Bockenhauer and W. E. Moerner . Photo-Induced Conformational Flexibility in Single Solution-Phase Peridinin-Chlorophyll-Proteins. The Journal of Physical Chemistry A 2013, 117 (35) , 8399-8406.
    6. Hideki Ikemoto, Sumera Tubasum, Tönu Pullerits, Jens Ulstrup, and Qijin Chi . Nanoscale Confinement and Fluorescence Effects of Bacterial Light Harvesting Complex LH2 in Mesoporous Silicas. The Journal of Physical Chemistry C 2013, 117 (6) , 2868-2878.
    7. Milan Durchan, Josef Tichý, Radek Litvín, Václav Šlouf, Zdenko Gardian, Petr Hříbek, František Vácha, and Tomáš Polívka . Role of Carotenoids in Light-Harvesting Processes in an Antenna Protein from the Chromophyte Xanthonema debile. The Journal of Physical Chemistry B 2012, 116 (30) , 8880-8889.
    8. Lijin Tian, Ivo H. M. van Stokkum, Rob B. M. Koehorst, Aniek Jongerius, Diana Kirilovsky, and Herbert van Amerongen . Site, Rate, and Mechanism of Photoprotective Quenching in Cyanobacteria. Journal of the American Chemical Society 2011, 133 (45) , 18304-18311.
    9. A. Ligia Focsan, Michael K. Bowman, Péter Molnár, József Deli, and Lowell D. Kispert . Carotenoid Radical Formation: Dependence on Conjugation Length. The Journal of Physical Chemistry B 2011, 115 (30) , 9495-9506.
    10. Tomáš Polívka and Harry A. Frank . Molecular Factors Controlling Photosynthetic Light Harvesting by Carotenoids. Accounts of Chemical Research 2010, 43 (8) , 1125-1134.
    11. Dariusz M. Niedzwiedzki, Aaron M. Collins, Amy M. LaFountain, Miriam M. Enriquez, Harry A. Frank and Robert E. Blankenship. Spectroscopic Studies of Carotenoid-to-Bacteriochlorophyll Energy Transfer in LHRC Photosynthetic Complex from Roseiflexus castenholzii 1 Resubmitted to J Phys Chem B.. The Journal of Physical Chemistry B 2010, 114 (26) , 8723-8734.
    12. Tomáš Polívka, Harry A. Frank, Miriam M. Enriquez, Dariusz M. Niedzwiedzki, Synnøve Liaaen-Jensen, Joanna Hemming, John R. Helliwell and Madeleine Helliwell . X-ray Crystal Structure and Time-Resolved Spectroscopy of the Blue Carotenoid Violerythrin. The Journal of Physical Chemistry B 2010, 114 (26) , 8760-8769.
    13. Sergiu Amarie, Kibrom Arefe, Jan Hendrik Starcke, Andreas Dreuw and Josef Wachtveitl. Identification of an Additional Low-Lying Excited State of Carotenoid Radical Cations. The Journal of Physical Chemistry B 2008, 112 (44) , 14011-14017.
    14. Hong Cong, Dariusz M. Niedzwiedzki, George N. Gibson, Amy M. LaFountain, Rhiannon M. Kelsh, Alastair T. Gardiner, Richard J. Cogdell and Harry A. Frank . Ultrafast Time-Resolved Carotenoid to-Bacteriochlorophyll Energy Transfer in LH2 Complexes from Photosynthetic Bacteria. The Journal of Physical Chemistry B 2008, 112 (34) , 10689-10703.
    15. Hong Cong,, Dariusz M. Niedzwiedzki,, George N. Gibson, and, Harry A. Frank. Ultrafast Time-Resolved Spectroscopy of Xanthophylls at Low Temperature. The Journal of Physical Chemistry B 2008, 112 (11) , 3558-3567.
    16. Tomáš Polívka,, Dariusz Niedzwiedzki,, Marcel Fuciman,, Villy Sundström, and, Harry A. Frank. Role of B800 in Carotenoid−Bacteriochlorophyll Energy and Electron Transfer in LH2 Complexes from the Purple Bacterium Rhodobacter sphaeroides. The Journal of Physical Chemistry B 2007, 111 (25) , 7422-7431.
    17. Dariusz Niedzwiedzki,, Jeremy F. Koscielecki,, Hong Cong,, James O. Sullivan,, George N. Gibson,, Robert R. Birge, and, Harry A. Frank. Ultrafast Dynamics and Excited State Spectra of Open-Chain Carotenoids at Room and Low Temperatures. The Journal of Physical Chemistry B 2007, 111 (21) , 5984-5998.
    18. Sergiu Amarie,, Jörg Standfuss,, Tiago Barros,, Werner Kühlbrandt,, Andreas Dreuw, and, Josef Wachtveitl. Carotenoid Radical Cations as a Probe for the Molecular Mechanism of Nonphotochemical Quenching in Oxygenic Photosynthesis. The Journal of Physical Chemistry B 2007, 111 (13) , 3481-3487.
    19. Henriette Wolpher,, Subrata Sinha,, Jingxi Pan,, Anh Johansson,, Maria J. Lundqvist,, Petter Persson,, Reiner Lomoth,, Jonas Bergquist,, Licheng Sun,, Villy Sundström,, Björn Åkermark, and, Tomás Polívka. Synthesis and Electron Transfer Studies of Ruthenium−Terpyridine-Based Dyads Attached to Nanostructured TiO2. Inorganic Chemistry 2007, 46 (3) , 638-651.
    20. Dariusz M. Niedzwiedzki,, James O. Sullivan,, Tomáš Polívka,, Robert R. Birge, and, Harry A. Frank. Femtosecond Time-Resolved Transient Absorption Spectroscopy of Xanthophylls. The Journal of Physical Chemistry B 2006, 110 (45) , 22872-22885.
    21. Ritsuko Fujii,, Toshiyuki Kusumoto,, Tokutake Sashima,, Richard J. Cogdell,, Alastair T. Gardiner, and, Hideki Hashimoto. Sub-μ-second Time-Resolved Absorption Spectroscopy of a Polar Carotenoid Analogue, 2-(All-trans-retinylidene)indan-1,3-dione; Formation of the Dication by Direct Triplet-Excited Sensitization. The Journal of Physical Chemistry A 2005, 109 (49) , 11117-11122.
    22. Helena Hörvin Billsten,, Jingxi Pan,, Subrata Sinha,, Torbjörn Pascher,, Villy Sundström, and, Tomáš Polívka. Excited-State Processes in the Carotenoid Zeaxanthin after Excess Energy Excitation. The Journal of Physical Chemistry A 2005, 109 (31) , 6852-6859.
    23. Giovanna Salbitani, Piergiorgio Cianciullo, Viviana Maresca, Sergio Sorbo, Marilena Insolvibile, Francesco Loreto, Alessia Di Fraia, Adriana Basile, Simona Carfagna. Tissue localization and the physiological effects induced by an environmentally relevant mix of heavy metals in the liverwort Conocephalum conicum L. Dum. Environmental and Experimental Botany 2023, 216 , 105511.
    24. Emrah Özcan, Valentyna Kuznetsova, Gürkan Keşan, Marcel Fuciman, Radek Litvín, Tomáš Polívka. Ultrafast excited states dynamics of metal ion complexes of the carotenoid astaxanthin. Journal of Photochemistry and Photobiology A: Chemistry 2023, 441 , 114737.
    25. Yuan Ye, Sun Hongwei, Wang Yue, Xu Zisong, Han Shixin, He Guoqiang, Yin Kuide, Huihui Zhang. Wood vinegar alleviates photosynthetic inhibition and oxidative damage caused by Pseudomonas syringae pv. tabaci ( Pst ) infection in tobacco leaves. Journal of Plant Interactions 2022, 17 (1) , 801-811.
    26. Donatas Zigmantas, Tomáš Polívka, Petter Persson, Villy Sundström. Ultrafast laser spectroscopy uncovers mechanisms of light energy conversion in photosynthesis and sustainable energy materials. Chemical Physics Reviews 2022, 3 (4)
    27. Ivana Šímová, Valentyna Kuznetsova, Alastair T. Gardiner, Václav Šebelík, Michal Koblížek, Marcel Fuciman, Tomáš Polívka. Carotenoid responds to excess energy dissipation in the LH2 complex from Rhodoblastus acidophilus. Photosynthesis Research 2022, 154 (1) , 75-87.
    28. Xiaojing Chen, Xin Zhang, Hao Chen, Xiaoming Xu. Physiology and proteomics reveal Fulvic acid mitigates Cadmium adverse effects on growth and photosynthetic properties of lettuce. Plant Science 2022, 323 , 111418.
    29. Tuhin Khan, Valentyna Kuznetsova, Maria Agustina Dominguez‐Martin, Cheryl A. Kerfeld, Tomáš Polívka. UV Excitation of Carotenoid Binding Proteins OCP and HCP: Excited‐State Dynamics and Product Formation. ChemPhotoChem 2022, 6 (1)
    30. Huihui Zhang, Zisong Xu, Kaiwen Guo, Yuze Huo, Guoqiang He, Hongwei Sun, Yupeng Guan, Nan Xu, Wei Yang, Guangyu Sun. Toxic effects of heavy metal Cd and Zn on chlorophyll, carotenoid metabolism and photosynthetic function in tobacco leaves revealed by physiological and proteomics analysis. Ecotoxicology and Environmental Safety 2020, 202 , 110856.
    31. Dariusz M. Niedzwiedzki, David J. K. Swainsbury, C. Neil Hunter. Carotenoid-to-(bacterio)chlorophyll energy transfer in LH2 antenna complexes from Rba. sphaeroides reconstituted with non-native (bacterio)chlorophylls. Photosynthesis Research 2020, 144 (2) , 155-169.
    32. Yanchun Cui, Manling Wang, Xuming Yin, Guoyun Xu, Shufeng Song, Mingjuan Li, Kai Liu, Xinjie Xia. OsMSR3, a Small Heat Shock Protein, Confers Enhanced Tolerance to Copper Stress in Arabidopsis thaliana. International Journal of Molecular Sciences 2019, 20 (23) , 6096.
    33. Beibei Cao, Lixiang Shu, Ai Li. Functional characterization of LkERF-B2 for improved salt tolerance ability in Arabidopsis thaliana. 3 Biotech 2019, 9 (7)
    34. 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.
    35. Ying Jia, Ying Shi, Peng Wang, Jian-Ping Zhang. Triplet excitation dynamics of β -carotene studied in three solvents by ns flash photolysis spectroscopy. Chinese Chemical Letters 2017, 28 (1) , 83-88.
    36. Alberta Pinnola, Hristina Staleva-Musto, Stefano Capaldi, Matteo Ballottari, Roberto Bassi, Tomáš Polívka. Electron transfer between carotenoid and chlorophyll contributes to quenching in the LHCSR1 protein from Physcomitrella patens. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2016, 1857 (12) , 1870-1878.
    37. Li Li, Feng Hu, Yu-Qiang Chang, Yan Zhou, Peng Wang, Jian-Ping Zhang. Triplet excitation dynamics of two keto-carotenoids in n-hexane and in methanol as studied by ns flash photolysis spectroscopy. Chemical Physics Letters 2015, 633 , 114-119.
    38. Dariusz M. Niedzwiedzki, Preston L. Dilbeck, Qun Tang, David J. Mothersole, Elizabeth C. Martin, David F. Bocian, Dewey Holten, C. Neil Hunter. Functional characteristics of spirilloxanthin and keto-bearing Analogues in light-harvesting LH2 complexes from Rhodobacter sphaeroides with a genetically modified carotenoid synthesis pathway. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2015, 1847 (6-7) , 640-655.
    39. Qiaoming Fu, Chungui Zhao, Suping Yang, Jihuai Wu. The photoelectric performance of dye-sensitized solar cells fabricated by assembling pigment–protein complexes of purple bacteria on nanocrystalline photoelectrode. Materials Letters 2014, 129 , 195-197.
    40. Gabriela S. Schlau-Cohen, Quan Wang, June Southall, Richard J. Cogdell, W. E. Moerner. Single-molecule spectroscopy reveals photosynthetic LH2 complexes switch between emissive states. Proceedings of the National Academy of Sciences 2013, 110 (27) , 10899-10903.
    41. Smitha Pillai, Janneke Ravensbergen, Antaeres Antoniuk-Pablant, Benjamin D. Sherman, Rienk van Grondelle, Raoul N. Frese, Thomas A. Moore, Devens Gust, Ana L. Moore, John T. M. Kennis. Carotenoids as electron or excited-state energy donors in artificial photosynthesis: an ultrafast investigation of a carotenoporphyrin and a carotenofullerene dyad. Physical Chemistry Chemical Physics 2013, 15 (13) , 4775.
    42. Václav Šlouf, Pavel Chábera, John D. Olsen, Elizabeth C. Martin, Pu Qian, C. Neil Hunter, Tomáš Polívka. Photoprotection in a purple phototrophic bacterium mediated by oxygen-dependent alteration of carotenoid excited-state properties. Proceedings of the National Academy of Sciences 2012, 109 (22) , 8570-8575.
    43. Carolin König, Johannes Neugebauer. Quantum Chemical Description of Absorption Properties and Excited‐State Processes in Photosynthetic Systems. ChemPhysChem 2012, 13 (2) , 386-425.
    44. Larry Lüer, Vladimíra Moulisová, Sarah Henry, Dario Polli, Tatas H. P. Brotosudarmo, Sajjad Hoseinkhani, Daniele Brida, Guglielmo Lanzani, Giulio Cerullo, Richard J. Cogdell. Tracking energy transfer between light harvesting complex 2 and 1 in photosynthetic membranes grown under high and low illumination. Proceedings of the National Academy of Sciences 2012, 109 (5) , 1473-1478.
    45. H.A. Frank, R.J. Cogdell. 8.6 Light Capture in Photosynthesis. 2012, 94-114.
    46. Dariusz M. Niedzwiedzki, Marcel Fuciman, Harry A. Frank, Robert E. Blankenship. Energy transfer in an LH4-like light harvesting complex from the aerobic purple photosynthetic bacterium Roseobacter denitrificans. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2011, 1807 (5) , 518-528.
    47. Andreas Dreuw, Jan Hendrik Starcke, Josef Wachtveitl. Excited state properties of the astaxanthin radical cation: A quantum chemical study. Chemical Physics 2010, 373 (1-2) , 2-7.
    48. Sergiu Amarie, Ute Förster, Nina Gildenhoff, Andreas Dreuw, Josef Wachtveitl. Excited state dynamics of the astaxanthin radical cation. Chemical Physics 2010, 373 (1-2) , 8-14.
    49. Mitsuru Sugisaki, Masazumi Fujiwara, Daisuke Kosumi, Ritsuko Fujii, Mamoru Nango, Richard J. Cogdell, Hideki Hashimoto. Comparison of transient grating signals from spheroidene in an organic solvent and in pigment-protein complexes from Rhodobacter sphaeroides 2.4.1. Physical Review B 2010, 81 (24)
    50. Michael Wormit, Philipp H.P. Harbach, Jan M. Mewes, Sergiu Amarie, Josef Wachtveitl, Andreas Dreuw. Excitation energy transfer and carotenoid radical cation formation in light harvesting complexes — A theoretical perspective. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2009, 1787 (6) , 738-746.
    51. Sergiu Amarie, Laura Wilk, Tiago Barros, Werner Kühlbrandt, Andreas Dreuw, Josef Wachtveitl. Properties of zeaxanthin and its radical cation bound to the minor light-harvesting complexes CP24, CP26 and CP29. Biochimica et Biophysica Acta (BBA) - Bioenergetics 2009, 1787 (6) , 747-752.
    52. Tatsunori Okubo, Tatsuya Tomo, Takumi Noguchi. Detection of the D0→D1 transition of β-carotene radical cation photoinduced in photosystem II. Photochemical & Photobiological Sciences 2009, 8 (2) , 157-161.
    53. Harry A. Frank, Tomáš Polívka. Energy Transfer from Carotenoids to Bacteriochlorophylls. 2009, 213-230.
    54. Tatsunori Okubo, Tatsuya Tomo, Takumi Noguchi. Detection of the D 0 →D 1 transition of β-carotene radical cation photoinduced in photosystem II. Photochem. Photobiol. Sci. 2009, 8 (2) , 157-161.
    55. Cheng-Che Chu, Dario M. Bassani. Challenges and opportunities for photochemists on the verge of solar energy conversion. Photochemical & Photobiological Sciences 2008, 7 (5) , 521-530.
    56. Mary Grace I. Galinato, Dariusz Niedzwiedzki, Cailin Deal, Robert R. Birge, Harry A. Frank. Cation radicals of xanthophylls. Photosynthesis Research 2007, 94 (1) , 67-78.
    57. Michael Wormit, Andreas Dreuw. Quantum chemical insights in energy dissipation and carotenoid radical cation formation in light harvesting complexes. Physical Chemistry Chemical Physics 2007, 9 (23) , 2917.
    58. Michael Wormit, Andreas Dreuw. Carotenoid Radical Cation Formation in LH2 of Purple Bacteria:  A Quantum Chemical Study. The Journal of Physical Chemistry B 2006, 110 (47) , 24200-24206.
    59. Su Lin, Evaldas Katilius, Robielyn P. Ilagan, George N. Gibson, Harry A. Frank, Neal W. Woodbury. Mechanism of Carotenoid Singlet Excited State Energy Transfer in Modified Bacterial Reaction Centers. The Journal of Physical Chemistry B 2006, 110 (31) , 15556-15563.
    60. Tomáš Polívka, Ivo H. M. van Stokkum, Donatas Zigmantas, Rienk van Grondelle, Villy Sundström, Roger G. Hiller. Energy Transfer in the Major Intrinsic Light-Harvesting Complex from Amphidinium carterae. Biochemistry 2006, 45 (28) , 8516-8526.
    61. Eric A. Juban, James K. McCusker. Ultrafast Dynamics of 2 E State Formation in Cr(acac) 3. Journal of the American Chemical Society 2005, 127 (18) , 6857-6865.
    62. Tomáš Polívka, Cheryl A. Kerfeld, Torbjörn Pascher, Villy Sundström. Spectroscopic Properties of the Carotenoid 3‘-Hydroxyechinenone in the Orange Carotenoid Protein from the Cyanobacterium Arthrospira maxima. Biochemistry 2005, 44 (10) , 3994-4003.
    63. Nancy E. Holt, Donatas Zigmantas, Leonas Valkunas, Xiao-Ping Li, Krishna K. Niyogi, Graham R. Fleming. Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting. Science 2005, 307 (5708) , 433-436.
    64. Ali El-Agamey, David J McGarvey. Carotenoid Radicals and Radical Ions. , 119-154.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Your Mendeley pairing has expired. Please reconnect