Ultrafast energy transfer and excited state coupling in an artificial photosynthetic antenna

Journal of Physical Chemistry B

Volumn 117, Issue 46, 2013, Pages 14183-14190

  Maiuri, M ^a   Snellenburg, J J ^b   Van Stokkum, I H M ^b   Pillai, S ^c   Wongcarter, K ^c   Gust, D ^c   Moore, T A ^c   Moore, A L ^c   Van Grondelle, R ^b   Cerullo, G ^a   Polli, D ^a  

^a POLITECNICO DI MILANO   (Italy)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENERGY TRANSFER DYNAMICS; HIGH TEMPORAL RESOLUTION; LIGHT-HARVESTING; LIGHT-HARVESTING COMPLEX; PHOTOSYNTHETIC ACTIVITY; SELECTIVE EXCITATIONS; SPECTRAL SIGNATURE; TRANSIENT ABSORPTION SPECTROSCOPIES;

ENERGY TRANSFER; EXCITED STATES;

ANTENNAS;

EID: 84888581579     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp401073w     Document Type: Article

References (53)

1. van Amerongen, H.; Valkunas, L.; van Grondelle, R. Photosynthetic Excitons; World Scientific: Singapore, 2000.
2. van Grondelle, R.; Novoderezhkin, V. I. Energy Transfer in Photosynthesis: Experimental Insights and Quantitative Models Phys. Chem. Chem. Phys. 2006, 8, 793-807
3. Novoderezhkin, V. I.; van Grondelle, R. Physical Origins and Models of Energy Transfer in Photosynthetic Light-Harvesting Phys. Chem. Chem. Phys. 2010, 12, 7352-7365
4. Frank, H. A.; Cogdell, R. J. Carotenoids in Photosynthesis Photochem. Photobiol. 1996, 63, 257-264
5. Niyogi, K. K. Safety Valves for Photosynthesis Curr. Opin. Plant Biol. 2000, 3, 455-460
6. Ruban, A. V.; Johnson, M. P.; Duffy, C. D. P. The Photoprotective Molecular Switch in the Photosystem II Antenna Biochim. Biophys. Acta, Bioenerg. 2012, 1817, 167-181
7. Ruban, A. V.; Berera, R.; Ilioaia, C.; van Stokkum, I. H. M.; Kennis, J. T. M.; Pascal, A. A.; van Amerongen, H.; Robert, B.; Horton, P.; van Grondelle, R. Identification of a Mechanism of Photoprotective Energy Dissipation in Higher Plants Nature 2007, 450, 575-578
8. Holt, N. E.; Zigmantas, D.; Valkunas, L.; Li, X.-P.; Niyogi, K. K.; Fleming, G. R. Carotenoid Cation Formation and the Regulation of Photosynthetic Light Harvesting Science 2005, 307, 433-436
9. Ahn, T. K.; Avenson, T. J.; Ballottari, M.; Cheng, Y.-C.; Niyogi, K. K.; Bassi, R.; Fleming, G. R. Architecture of a Charge-Transfer State Regulating Light Harvesting in a Plant Antenna Protein Science 2008, 320, 794-797
10. Pascal, A. A.; Liu, Z.; Broess, K.; van Oort, B.; van Amerongen, H.; Wang, C.; Horton, P.; Robert, B.; Chang, W.; Ruban, A. Molecular Basis of Photoprotection and Control of Photosynthetic Light-Harvesting Nature 2005, 436, 134-137
11. Hudson, B. S.; Kohler, B. E. A Low-Lying Weak Transition in the Polyene α,ω-Diphenyloctatetraene Chem. Phys. Lett. 1972, 14, 299-304
12. Schulten, K.; Karplus, M. On the Origin of a Low-lying Forbidden Transition in Polyenes and Related Molecules Chem. Phys. Lett. 1972, 14, 305-309
13. Polívka, T.; Sundström, V. Ultrafast Dynamics of Carotenoid Excited States-From Solution to Natural and Artificial Systems Chem. Rev. 2004, 104, 2021-2072
14. Polívka, T.; Frank, H. J. Molecular Factors Controlling Photosynthetic Light Harvesting by Carotenoids Acc. Chem. Res. 2010, 43, 1125-1134
15. Polívka, T.; Sundström, V. Dark Excited States of Carotenoids: Consensus and Controversy Chem. Phys. Lett. 2009, 477, 1-11
16. Cerullo, G.; Polli, D.; Lanzani, G.; De Silvestri, S.; Hashimoto, H.; Cogdell, R. J. Photosynthetic Light Harvesting by Carotenoids: Detection of an Intermediate Excited State Science 2002, 298, 2395-2398
17. Ostroumov, E.; Müller, M. G.; Marian, C. M.; Kleinschmidt, M.; Holzwarth, A. R. Electronic Coherence Provides a Direct Proof for Energy-Level Crossing in Photoexcited Lutein and β-Carotene Phys. Rev. Lett. 2009, 103, 108302
18. Marek, M. S.; Buckup, T.; Motzkus, M. Direct Observation of a Dark State in Lycopene Using Pump-DFWM J. Phys. Chem. B 2011, 115, 8328-8337
19. Liddell, P. A.; Kuciauskas, D.; Sumida, J. P.; Nash, B.; Nguyen, D.; Moore, A. L.; Moore, T. A.; Gust, D. Photoinduced Charge Separation and Charge Recombination to a Triplet State in a Carotene-Porphyrin-Fullerene Triad J. Am. Chem. Soc. 1997, 119, 1400-1405
20. Kodis, G.; Herrero, C.; Palacios, R.; Mariño-Ochoa, E.; Gould, S.; De La Garza, L.; Van Grondelle, R.; Gust, D.; Moore, T. A.; Moore, A. L. Light Harvesting and Photoprotective Functions of Carotenoids in Compact Artificial Photosynthetic Antenna Designs J. Phys. Chem. B 2004, 108, 414-425
21. Gust, D.; Moore, T. A.; Moore, A. L. Solar Fuels via Artificial Photosynthesis Acc. Chem. Res. 2009, 42, 1890-1898
22. Kloz, M.; Pillai, S.; Kodis, G.; Gust, D.; Moore, T. A.; Moore, A. L.; van Grondelle, R.; Kennis, J. T. M. Carotenoid Photoprotection in Artificial Photosynthetic Antennas J. Am. Chem. Soc. 2011, 133, 7007-7015
23. Kloz, M.; Pillai, S.; Kodis, G.; Gust, D.; Moore, T. A.; Moore, A. L.; van Grondelle, R.; Kennis, J. T. M. New Light-Harvesting Roles of Hot and Forbidden Carotenoid States in Artificial Photosynthetic Constructs Chem. Sci. 2012, 3, 2052-2061
24. Gust, D.; Moore, T. A.; Moore, A. L.; Devadoss, C.; Liddell, P. A.; Hermant, R.; Nieman, R. A.; Demanche, L. J.; Degraziano, J. M.; Gouni, I. Triplet and Singlet Energy Transfer in Carotene-Porphyrin Dyads: Role of the Linkage Bonds J. Am. Chem. Soc. 1992, 114, 3590-3603
25. Manzoni, C.; Polli, D.; Cerullo, G. Two-Color Pump-probe System Broadly Tunable over the Visible and the Near Infrared with Sub-30 fs Temporal Resolution Rev. Sci. Instrum. 2006, 77, 023103
26. Polli, D.; Lüer, L.; Cerullo, G. High-Time-Resolution Pump-Probe System with Broadband Detection for the Study of Time-Domain Vibrational Dynamics Rev. Sci. Instrum. 2007, 78, 103108
27. van Stokkum, I. H. M.; Larsen, D. S.; van Grondelle, R. Global and Target Analysis of Time-Resolved Spectra Biochim. Biophys. Acta 2004, 1657, 82-104
28. Snellenburg, J. J.; Laptenok, S. P.; Seger, R.; Mullen, K. M.; van Stokkum, I. H. M. Glotaran: A Java-Based Graphical User Interface for the R Package TIMP J. Stat. Software 2012, 49, 1-22
29. de Weerd, F. L.; van Stokkum, I. H..; van Grondelle, R. Subpicosecond Dynamics in the Excited State Absorption of All-Trans-β-Carotene Chem. Phys. Lett. 2002, 354, 38-43
30. Polli, D.; Cerullo, G.; Lanzani, G.; De Silvestri, S.; Hashimoto, H.; Cogdell, R. J. Carotenoid-Bacteriochlorophyll Energy Transfer in LH2 Complexes Studied with 10-fs Time Resolution Biophys. J. 2006, 90, 2486-2497
31. Gradinaru, C. C.; Kennis, J. T.; Papagiannakis, E.; van Stokkum, I. H.; Cogdell, R. J.; Fleming, G. R.; Niederman, R. A.; van Grondelle, R. An Unusual Pathway of Excitation Energy Deactivation in Carotenoids: Singlet-to-Triplet Conversion on an Ultrafast Timescale in a Photosynthetic Antenna Proc. Natl. Acad. Sci. U. S. A. 2001, 98, 2364-2369
32. Papagiannakis, E.; Kennis, J. T. M.; van Stokkum, I. H. M.; Cogdell, R. J.; van Grondelle, R. An Alternative Carotenoid-to-Bacteriochlorophyll Energy Transfer Pathway in Photosynthetic Light Harvesting Proc. Natl. Acad. Sci. U. S. A. 2002, 99, 6017-6022
33. Savolainen, J.; Buckup, T.; Hauer, J.; Jafarpour, A.; Serrat, C.; Motzkus, M.; Herek, J. L. Carotenoid Deactivation in an Artificial Light-Harvesting Complex via a Vibrationally Hot Ground State Chem. Phys. 2009, 357, 181-187
34. Papagiannakis, E.; van Stokkum, I. H. M.; Vengris, M.; Cogdell, R. J.; van Grondelle, R.; Larsen, D. S. Excited-State Dynamics of Carotenoids in Light-Harvesting Complexes. 1. Exploring the Relationship Between the S1 and S* States J. Phys. Chem. B 2006, 110, 5727-5736
35. Krueger, B. P.; Scholes, G. D.; Jimenez, R.; Fleming, G. R. Electronic Excitation Transfer from Carotenoid to Bacteriochlorophyll in the Purple Bacterium Rhodopseudomonas Acidophila J. Phys. Chem. B 1998, 102, 2284-2292
36. Macpherson, a N.; Arellano, J. B.; Fraser, N. J.; Cogdell, R. J.; Gillbro, T. Efficient Energy Transfer from the Carotenoid S(2) State in a Photosynthetic Light-Harvesting Complex Biophys. J. 2001, 80, 923-930
37. Wohlleben, W.; Buckup, T.; Herek, J. L.; Cogdell, R. J.; Motzkus, M. Multichannel Carotenoid Deactivation in Photosynthetic Light Harvesting as Identified by an Evolutionary Target Analysis Biophys. J. 2003, 85, 442-450
38. Savolainen, J.; Dijkhuizen, N.; Fanciulli, R.; Liddell, P. A.; Gust, D.; Moore, T. A.; Moore, A. L.; Hauer, J.; Buckup, T.; Motzkus, M. Ultrafast Energy Transfer Dynamics of a Bioinspired Dyad Molecule J. Phys. Chem. B 2008, 112, 2678-2685
39. Cong, H.; Niedzwiedzki, D. M.; Gibson, G. N.; LaFountain, A. M.; Kelsh, R. M.; Gardiner, A. T.; Cogdell, R. J.; Frank, H. A Ultrafast Time-Resolved Carotenoid to-Bacteriochlorophyll Energy Transfer in LH2 Complexes from Photosynthetic Bacteria J. Phys. Chem. B 2008, 112, 10689-10703
40. Berera, R.; van Stokkum, I. H. M.; Kodis, G.; Keirstead, A. E.; Pillai, S.; Herrero, C.; Palacios, R. E.; Vengris, M.; van Grondelle, R.; Gust, D. Energy Transfer, Excited-State Deactivation, and Exciplex Formation in Artificial Caroteno-Phthalocyanine Light-Harvesting Antennas J. Phys. Chem. B 2007, 111, 6868-6877
41. Papagiannakis, E.; Das, S. K.; Gall, A.; Van Stokkum, I. H. M.; Robert, B.; van Grondelle, R.; Frank, H. A.; Kennis, J. T. M. Light Harvesting by Carotenoids Incorporated into the B850 Light-Harvesting Complex from Rhodobacter sphaeroides R-26.1: Excited-State Relaxation, Ultrafast Triplet Formation, and Energy Transfer to Bacteriochlorophyll J. Phys. Chem. B 2003, 107, 5642-5649
42. Wohlleben, W.; Buckup, T.; Hashimoto, H.; Cogdell, R. J.; Herek, J. L.; Motzkus, M. Pump-Deplete-Probe Spectroscopy and the Puzzle of Carotenoid Dark States J. Phys. Chem. B 2004, 108, 3320-3325
43. Rademaker, H.; Hoff, A. J.; Van Grondelle, R.; Duysens, L. N. M. Carotenoid Triplet Yields in Normal and Deuterated Rhodospirillum rubrum Biochim. Biophys. Acta, Bioenerg. 1980, 592, 240-257
44. Kingma, H.; van Grondelle, R.; Duysens, L. N. M. Magnetic-Field Effects in Photosynthetic Bacteria. II. Formation of Triplet States in the Reaction Center and the Antenna of Rhodospirillum rubrum and Rhodopseudomonas sphaeroides. Magnetic-Field Effects Biochim. Biophys. Acta, Bioenerg. 1985, 808, 383-399
45. Niedzwiedzki, D.; Koscielecki, J. F.; Cong, H.; O Sullivan, J.; Gibson, G. N.; Birge, R. R.; Frank, H. A. Ultrafast Dynamics and Excited State Spectra of Open-Chain Carotenoids at Room and Low Temperatures J. Phys. Chem. B 2007, 111, 5984-5998
46. Bode, S.; Quentmeier, C. C.; Liao, P.-N.; Hafi, N.; Barros, T.; Wilk, L.; Bittner, F.; Walla, P. J. On the Regulation of Photosynthesis by Excitonic Interactions Between Carotenoids and Chlorophylls Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 12311-12316
47. Berera, R.; Herrero, C.; van Stokkum, I. H. M.; Vengris, M.; Kodis, G.; Palacios, R. E.; van Amerongen, H.; van Grondelle, R.; Gust, D.; Moore, T. A. A Simple Artificial Light-Harvesting Dyad as a Model for Excess Energy Dissipation in Oxygenic Photosynthesis Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 5343-5348
48. Frank, H. A.; Cua, A.; Chynwat, V.; Young, A.; Gosztola, D.; Wasielewski, M. R. Photophysics of the Carotenoids Associated with the Xanthophyll Cycle in Photosynthesis Photosynth. Res. 1994, 41, 389-395
49. Palacios, R. E.; Kodis, G.; Herrero, C.; Ochoa, E. M.; Gervaldo, M.; Gould, S. L.; Kennis, J. T. M.; Gust, D.; Moore, T. A.; Moore, A. L. Tetrapyrrole Singlet Excited State Quenching by Carotenoids in an Artificial Photosynthetic Antenna J. Phys. Chem. B 2006, 110, 25411-25420
50. Liao, P.-N.; Pillai, S.; Gust, D.; Moore, T. A.; Moore, A. L.; Walla, P. J. Two-Photon Study on the Electronic Interactions Between the First Excited Singlet States in Carotenoid-Tetrapyrrole Dyads J. Phys. Chem. A 2011, 115, 4082-4091
51. Engel, G. S.; Calhoun, T. R.; Read, E. L.; Ahn, T.-K.; Mancal, T.; Cheng, Y.-C.; Blankenship, R. E.; Fleming, G. R. Evidence for Wavelike Energy Transfer through Quantum Coherence in Photosynthetic Systems Nature 2007, 446, 782-786
52. Collini, E.; Wong, C. Y.; Wilk, K. E.; Curmi, P. M. G.; Brumer, P.; Scholes, G. D. Coherently Wired Light-Harvesting in Photosynthetic Marine Algae at Ambient Temperature Nature 2010, 463, 644-647
53. Calhoun, T. R.; Ginsberg, N. S.; Schlau-Cohen, G. S.; Cheng, Y.-C.; Ballottari, M.; Bassi, R.; Fleming, G. R. Quantum Coherence Enabled Determination of the Energy Landscape in Light-Harvesting Complex II J. Phys. Chem. B 2009, 113, 16291-16295