Skip to main content
SpringerLink
Log in

Triplet Excitation Transfer between Carotenoids in the LH2 Complex from Photosynthetic Bacterium Rhodopseudomonas palustris

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

We have studied, by means of sub-microsecond time-resolved absorption spectroscopy, the triplet-excited state dynamics of carotenoids (Cars) in the intermediate-light adapted LH2 complex (ML–LH2) from Rhodopseudomonas palustris containing Cars with different numbers of conjugated double bonds. Following pulsed photo-excitation at 590 nm at room temperature, rapid spectral equilibration was observed either as a red shift of the isosbestic wavelength on a time scale of 0.6–1.0 μs, or as a fast decay in the shorter-wavelength side of the Tn←T1 absorption of Cars with a time constant of 0.5–0.8 μs. Two major spectral components assignable to Cars with 11 and 12 conjugated double bonds were identified. The equilibration was not observed in the ML–LH2 at 77 K, or in the LH2 complex from Rhodobacter sphaeroides G1C containing a single type of Car. The unique spectral equilibration was ascribed to temperature-dependent triplet excitation transfer among different Car compositions. The results suggest that Cars of 11 and 12 conjugated bonds, both in close proximity of BChls, may coexist in an α,β-subunit of the ML–LH2 complex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987) Structure of the reaction centre from Rhodobacter sphaeroides R-26: the cofactors. Proc Natl Acad Sci USA 84: 5730–5734

    Article  PubMed  CAS  Google Scholar 

  • Angerhofer A, Bornhäuser F, Gall A and Cogdell RJ (1995) Optical and optically detected magnetic resonance investigation on purple photosynthetic bacterial antenna complexes. Chem Phys 194: 259–274

    Article  CAS  Google Scholar 

  • Arellano JB, Raju BB, Naqvi KR and Gillbro T (1998) Estimation of pigment stoichiometries in photosynthetic systems of purple bacteria: special reference to the (absence of) second carotenoid in LH2. Photochem Photobiol 68: 84–87

    Article  CAS  Google Scholar 

  • Bittl R, Schlodder E, Geisenheimer I, Lubitz W and Cogdell RJ (2001) Transient EPR and absorption studies of carotenoid triplet formation in purple bacterial antenna complexes. J Phys Chem B 105: 5525–5535

    Article  CAS  Google Scholar 

  • Bose SK (1963) Media for anaerobic growth of photosynthetic bacteria. In: Gest H, Pietro AS and Vernon LP (eds) Bacterial Photosynthesis, pp 501–511. The Antioch Press, Yellow Springs, Ohio

    Google Scholar 

  • Clayton RK (1966) Spectroscopic analysis of bacteriochlorophylls in vitro and in vivo. Photochem Photobiol 5: 669–677

    CAS  Google Scholar 

  • Cogdell RJ, Hipkins MF, MacDonald W and Truscott TG (1981) Energy transfer between the carotenoid and the bacteriochlorophyll within the B-800–850 light-harvesting pigment-protein complex of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 634: 191–202

    Article  PubMed  CAS  Google Scholar 

  • Cogdell RJ, Howard TD, Bittl R, Schlodder E, Geisenheimer I and Lubitz W (2000) How carotenoids protect bacterial photosynthesis. Phil Trans R Soc London Ser B 355: 1345–1349

    Article  CAS  Google Scholar 

  • Connolly JS, Samuel EB and Janzen F (1982) Effects of solvent on the fluorescence properties of bacteriachlorophyll a. Photochem Photobiol 36: 565–574

    CAS  Google Scholar 

  • Crystall B, Booth PJ, Klug DR, Barber J and Porter G (1989) Resolution of a long lived fluorescence component from D1/D2/cytochrome b-559 reaction centres. FEBS Lett 249: 75–78

    Article  CAS  Google Scholar 

  • Deisenhofer J, Epp O, Miki K, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature 318: 618–624

    Article  Google Scholar 

  • Damjanović A, Ritz T and Schulten K (1999) Energy transfer between carotenoids and bacteriochlorophylls in light-harvesting complex II of purple bacteria. Phys Rev E 59: 3293–3311

    Article  Google Scholar 

  • Dexter DL (1953) A theory of sensitized luminescence in solids. J Chem Phys 21: 836–850

    Article  CAS  Google Scholar 

  • Ermler U, Fritzsch G, Buchanan SK and Michel H (1994) Structure of the photosynthetic reaction centre from Rhodobacter sphaeroides at 2. 65 Å resolution: cofactors and protein-cofactor interactions. Structure 2: 925–936

    Article  PubMed  CAS  Google Scholar 

  • Evans MB, Hawthornthwaite AM and Cogdell RJ (1990) Isolation and characterization of the different B800–B850 light-harvesting complexes from low-and high-light grown cells of Rhodopseudomonas palustris, strain 2. 1. 6. Biochim Biophys Acta. 1016: 71–76

    Article  CAS  Google Scholar 

  • Farhoosh R, Chynwat V, Gebhard R, Lugtenburg J and Frank HA (1994) Triplet energy transfer between bacteriochlorophyll and carotenoids in B850 light–harvesting complexes of Rhodobacter sphaeroides R-26. 1. Photosynth Res 42: 157–166

    Article  CAS  Google Scholar 

  • Frank HA and Cogdell RJ (1993) The photochemistry and function of carotenoids in photosynthesis. In: Young A and Britton G (eds) Carotenoids in Photosynthesis, pp 252–321. Chapman & Hall, London

    Google Scholar 

  • Freer A, Prince S, Sauer K, Papiz M, Hawthornthwaite-Lawless A, McDermott G, Cogdell R and Isaacs NW (1996) Pigment-pigment interactions and energy transfer in the antenna complex of the photosynthetic bacterium Rhodopseudomonas acidophila. Structure 4: 449–462

    Article  PubMed  CAS  Google Scholar 

  • Fujii R, Onaka K, Kuki M, Koyama Y and Watanabe Y (1998) The 2Ag -) energies of all-trans-neurosporene and spheroidene as determined by fluorescence spectroscopy. Chem Phys Lett 288: 847–853

    Article  CAS  Google Scholar 

  • Gradinaru CC, Kennis JTM, Papagiannakis E, van Stokkum IHM, Cogdell RJ, Fleming GR, Niederman RA and van Grondelle R (2001) 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 USA 98: 2364–2369

    Article  PubMed  CAS  Google Scholar 

  • Hartigan N, Tharia HA, Sweeney F, Lawless AM and Papiz MZ (2002) The 7. 5-Å electron density and spectroscopic properties of a novel low-light B800 LH2 from Rhodopseudomonas palustris. Biophys J 82: 963–977

    Article  PubMed  CAS  Google Scholar 

  • Herek JL, Polívka T, Pullerits T, Fowler GJS, Hunter CN and Sundström V (1998) Ultrafast carotenoid band shifts probe structure and dynamics in photosynthetic antenna complexes. Biochemistry 37: 7057–7061

    Article  PubMed  CAS  Google Scholar 

  • Kingma H, van Grondelle R and Duysens LNM (1985) 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 808: 383–399

    Article  CAS  Google Scholar 

  • Koepke J, Hu X, Muenke C, Schulten K and Michel H (1996) The crystal structure of the light-harvesting complex II (B800–B850) from Rhodospirillum molischianum. Structure 4: 581–597

    Article  PubMed  CAS  Google Scholar 

  • Koyama Y, Kuki M, Andersson PO and Gillbro T (1996) Singlet excited states and the light harvesting function of carotenoids in bacterial photosynthesis. Photochem Photobiol 63: 243–256

    CAS  Google Scholar 

  • McDermott G, Prince SM, Freer AA, Hawthornthwaite-Lawless AM, Papiz MZ, Cogdell RJ and Isaacs NW (1995) Crystal Structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374: 517–521

    Article  CAS  Google Scholar 

  • Monger TG, Cogdell RJ and Parson WW (1976) Triplet states of bacteriochlorophyll and carotenoids in chromatophores of photosynthetic bacteria. Biochim Biophys Acta 449: 136–153

    Article  PubMed  CAS  Google Scholar 

  • Monger TG and Parson WW (1977) Singlet-triplet fusion in Rhodopseudomonas sphaeroides chromatophores, a probe of the organization of the photosynthetic apparatus. Biochim Biophys Acta 460: 393–407

    Article  PubMed  CAS  Google Scholar 

  • Nagae H, Kakitani T, Katoh T and Mimuro M (1993) Calculation of the excitation transfer-matrix elements between the S2 or S1 state of carotenoid and the S2 or S1 state of bacteriochlorophyll. J Chem Phys 98: 8012–8023

    Article  CAS  Google Scholar 

  • Papiz MZ, Prince SM, Howard T, Cogdell RJ and Isaacs NW (2003) The structure and thermal motion of the B800–850 LH2 complex from Rps. acidophila at 2.0 Å resolution and 93. 100 K: new structural features and functionally relevant motions. J Mol Biol 326: 1523–1538

    Article  PubMed  CAS  Google Scholar 

  • Qian P, Saiki K, Mizoguchi T, Hara K, Sashima T, Fujii R and Koyama Y (2001) Time-dependent changes in the carotenoid composition and preferential binding of spirilloxanthin to the reaction center and anhydrorhodovibrin to the LH1 antenna complex in Rhodobium marinum. Photochem Photobiol 74: 444–452

    Article  PubMed  CAS  Google Scholar 

  • Rademaker H, Hoff AJ, van Grondelle R and Duysens LNM (1980) Carotenoid triplet yields in normal and deuterated Rhodospirillum Rubrum. Biochim Biophys Acta 592: 240–257

    Article  PubMed  CAS  Google Scholar 

  • Ritz T, Damjanovic A, Schulten K, Zhang JP and Koyama Y (2000) Understanding efficient light-harvesting through carotenoids with novel theoretical and experimental techniques, Photosynth Res 66: 125–144

    Article  PubMed  CAS  Google Scholar 

  • Schmidt K (1978) Biosynthesis of carotenoids. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 729–750. Plenum Press, New York

    Google Scholar 

  • Tharia HA, Nightingale TD, Papiz MZ and Lawless AM (1999) Characterization of hydrophobic peptides by RP-HPLC from different spectral forms of LH2 isolated from Rps. palustris. Photosynth Res 61: 157–167

    Article  CAS  Google Scholar 

  • Truscott TG, Land EJ and Sykes A (1973) The in vitro photochemistry of biological molecules-III. Absorption spectra, lifetimes and rates of oxygen quenching of the triplet states of β-carotene, retinal and related polyenes. Photochem Photobiol 17: 43–51

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The State Key Laboratory for Structural Chemistry of Unstable and Stable Species, Institute of Chemistry, Chinese Academy of Sciences, 1st North Street, Haidian District, Beijing, 100080, P. R. China

    Juan Feng, Yi-Shi Wu, Xi-Cheng Ai, Xu-Jia Zhang & You-Guo Huang

  2. The National Laboratory of BioMacromolecules, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, P. R. China

    Qian Wang, Xing-Kang Zhang & Jian-Ping Zhang

Authors
  1. Juan Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qian Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yi-Shi Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xi-Cheng Ai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xu-Jia Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. You-Guo Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Xing-Kang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jian-Ping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Feng, J., Wang, Q., Wu, YS. et al. Triplet Excitation Transfer between Carotenoids in the LH2 Complex from Photosynthetic Bacterium Rhodopseudomonas palustris . Photosynthesis Research 82, 83–94 (2004). https://doi.org/10.1023/B:PRES.0000040445.71124.96

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PRES.0000040445.71124.96

Search

Navigation