Femtosecond dynamics of the forbidden carotenoid S1 state in light-harvesting complexes of purple bacteria observed after two-photon excitation.

Time-resolved excited-state absorption intensities after direct two-photon excitation of the carotenoid S(1) state are reported for light-harvesting complexes of purple bacteria. Direct excitation of the carotenoid S(1) state enables the measurement of subsequent dynamics on a fs time scale without interference from higher excited states, such as the optically allowed S(2) state or the recently discovered dark state situated between S(1) and S(2). The lifetimes of the carotenoid S(1) states in the B800-B850 complex and B800-B820 complex of Rhodopseudomonas acidophila are 7+/-0.5 ps and 6+/-0.5 ps, respectively, and in the light-harvesting complex 2 of Rhodobacter sphaeroides approximately 1.9+/-0.5 ps. These results explain the differences in the carotenoid to bacteriochlorophyll energy transfer efficiency after S(2) excitation. In Rps. acidophila the carotenoid S(1) to bacteriochlorophyll energy transfer is found to be quite inefficient (phi(ET1) <28%) whereas in Rb. sphaeroides this energy transfer is very efficient (phi(ET1) approximately 80%). The results are rationalized by calculations of the ensemble averaged time constants. We find that the Car S(1) --> B800 electronic energy transfer (EET) pathway ( approximately 85%) dominates over Car S(1) --> B850 EET ( approximately 15%) in Rb. sphaeroides, whereas in Rps. acidophila the Car S(1) --> B850 EET ( approximately 60%) is more efficient than the Car S(1) --> B800 EET ( approximately 40%). The individual electronic couplings for the Car S(1) --> BChl energy transfer are estimated to be approximately 5-26 cm(-1). A major contribution to the difference between the energy transfer efficiencies can be explained by different Car S(1) energy gaps in the two species.

[1]  Graham R. Fleming,et al.  On the Mechanism of Light Harvesting in Photosynthetic Purple Bacteria: B800 to B850 Energy Transfer , 2000 .

[2]  D. L. Dexter.  A Theory of Sensitized Luminescence in Solids , 1953 .

[3]  David J. Gosztola,et al.  Effect of the Solvent Environment on the Spectroscopic Properties and Dynamics of the Lowest Excited States of Carotenoids , 2000 .

[4]  R. W. Visschers,et al.  Two-dimensional crystals of LH2 light-harvesting complexes from Ectothiorhodospira sp. and Rhodobacter capsulatus investigated by electron microscopy. , 1996 .

[5]  Klaus Schulten,et al.  Energy transfer between carotenoids and bacteriochlorophylls in light-harvesting complex II of purple bacteria , 1999 .

[6]  M. Wasielewski,et al.  Spectroscopic Properties of Spheroidene Analogs Having Different Extents of π-Electron Conjugation , 1997 .

[7]  Y. Koyama,et al.  The 2Ag− energies of all-trans-neurosporene and spheroidene as determined by fluorescence spectroscopy , 1998 .

[8]  T. Gillbro,et al.  Solvent Dependence of the Ultrafast S2−S1 Internal Conversion Rate of β-Carotene , 1998 .

[9]  R. Cogdell,et al.  Carotenoids in Photosynthesis , 1996, Photochemistry and photobiology.

[10]  Y. Koyama,et al.  A new singlet-excited state of all-trans-spheroidene as detected by resonance-Raman excitation profiles , 1999 .

[11]  Hideki Hashimoto,et al.  THE 2AG- ENERGY OF CRYSTALLINE ALL-TRANS-SPHEROIDENE AS DETERMINED BY RESONANCE-RAMAN EXCITATION PROFILES , 1998 .

[12]  Graham R. Fleming,et al.  Electronic Excitation Transfer from Carotenoid to Bacteriochlorophyll in the Purple Bacterium Rhodopseudomonas acidophila , 1998 .

[13]  G. Fleming,et al.  Electronic Interactions in Photosynthetic Light-Harvesting Complexes: The Role of Carotenoids , 1997 .

[14]  H. Frank,et al.  The application of the energy gap law to the S1 energies and dynamics of carotenoids , 1995 .

[15]  T. Gillbro,et al.  Femtosecond dynamics of carotenoid-to-bacteriochlorophyll a energy transfer in the light-harvesting antenna complexes from the purple bacterium Chromatium purpuratum , 1996 .

[16]  R. Cogdell,et al.  Generation of triplet and cation-radical bacteriochlorophyll a in carotenoidless LH1 and LH2 antenna complexes from Rhodobacter sphaeroides. , 1998, Biochemistry.

[17]  S. Mukamel,et al.  Superradiance coherence sizes in single-molecule spectroscopy of LH2 antenna complexes , 1999 .

[18]  W. W. Parson,et al.  Femtosecond Pump−Probe Spectroscopy of the B850 Antenna Complex of Rhodobacter sphaeroides at Room Temperature , 1999 .

[19]  R. Cogdell,et al.  A spectral characterisation of the light-harvesting pigment-protein complexes from Rhodopseudomonas acidophila , 1986 .

[20]  G. Fleming,et al.  Calculation of Couplings and Energy-Transfer Pathways between the Pigments of LH2 by the ab Initio Transition Density Cube Method , 1998 .

[21]  N. W. Isaacs,et al.  Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria , 1995, Nature.

[22]  K. Schulten,et al.  The crystal structure of the light-harvesting complex II (B800-850) from Rhodospirillum molischianum. , 1996, Structure.

[23]  G. Fleming,et al.  Two-Photon Excitation Spectrum of Light-Harvesting Complex II and Fluorescence Upconversion after One- and Two-Photon Excitation of the Carotenoids , 2000 .

[24]  T. Inaba,et al.  Mechanism of the Carotenoid-to-Bacteriochlorophyll Energy Transfer via the S1 State in the LH2 Complexes from Purple Bacteria , 2000 .

[25]  W. M. McClain.  Excited State Symmetry Assignment Through Polarized Two‐Photon Absorption Studies of Fluids , 1971 .

[26]  M. Mimuro,et al.  Calculation of the excitation transfer matrix elements between the S2 or S1 state of carotenoid and the S2 or S1 state of bacteriochlorophyll , 1993 .

[27]  T. Walz,et al.  Projection structures of three photosynthetic complexes from Rhodobacter sphaeroides: LH2 at 6 A, LH1 and RC-LH1 at 25 A. , 1998, Journal of molecular biology.

[28]  I. Gould,et al.  Ab Initio Molecular Orbital Calculations of Electronic Couplings in the LH2 Bacterial Light-Harvesting Complex of Rps. Acidophila , 1999 .

[29]  H. Frank,et al.  On the photophysics and photochemical properties of carotenoids and their role as light-harvesting pigments in photosynthesis , 1997 .

[30]  W. M. McClain,et al.  Two-photon excitation spectra of the low energy excited states of diphenylhexatriene and diphenyloctatetraene , 1976 .

[31]  M. Wasielewski,et al.  Singlet and triplet energy transfer in the peridinin-chlorophyll a-protein from Amphidinium carterae , 1999 .

[32]  G. Fleming,et al.  Observation of the S1 state of spheroidene in LH2 by two-photon fluorescence excitation , 1999 .

[33]  P. Tavan,et al.  Electronic excitations in finite and infinite polyenes. , 1987, Physical review. B, Condensed matter.

[34]  A. Oijen,et al.  Unraveling the electronic structure of individual photosynthetic pigment-protein complexes , 1999, Science.

[35]  F. Young.  Biochemistry , 1955, The Indian Medical Gazette.

[36]  T. Gillbro,et al.  Singlet Excited States and the Light‐Harvesting Function of Carotenoids in Bacterial Photosynthesis , 1996 .

[37]  Tõnu Pullerits,et al.  Photosynthetic light-harvesting: Reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit , 1999 .