Skip to main content
SpringerLink
Log in

Efficient light harvesting through carotenoids

  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

We review the factors that control the efficiency of carotenoid-chlorophyll excitation transfer in photosynthetic light harvesting. For this we summarize first the recently developed theory that describes electronic couplings between carotenoids and chlorophylls and we outline in particular the influence of length of conjugated system and of symmetry breaking on the couplings. We focus hereby on the structurally solved lycopene-BChl system of LH 2 from Rhodospirillum molischianum and the peridinin-Chl a system of PCP from Amphidinium carterae. In addition, we review recent spectroscopic data for neurosporene, spheroidene and lycopene, three carotenoids with different lengths of conjugated systems. On the basis of the measured energies, emission lineshapes, solution and protein environment lifetimes for their 2A− g and 1Bu + states as well as of the theoretically determined couplings, we conclude that the transfer efficiencies from the 2Ag − state are controlled by the Car(2Ag −)–BChl(Qg) electronic couplings and the 2Ag − → 1Ag − internal conversion rates. We suggest that symmetry breaking and geometry rather than length of conjugated system dominate couplings involving the 2Ag − state. Differences in transfer efficiencies from the 1Bu + state in LH 2 and PCP are found to be dominated by the differences in spectral overlap. The role of the 1Bu + state is likely to be influenced by a lower-lying (in longer polyenes), optically forbidden 1Bu − state.

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

  • Akimoto S, Takaichi S, Ogata T, Nishimura Y, Yamazaki I and Mimuro M (1996) Excitation energy transfer in carotenoid-chlorophyll protein complexes probed by femtosecond fluorescence decays. Chem Phys Lett 260: 147–152

    Article  CAS  Google Scholar 

  • Angerhofer A, Cogdell R and Hipkins M (1986) A spectral characterization of the light-harvesting pigment-protein complexes from Rhodopseudomonas acidophila. Biochim Biophys Acta 848: 333–341

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bautista J, Hiller R, Sharples F, Gosztola D, Wasielewski M and Frank H (1999a) Singlet and triplet transfer in the Peridinin-Chlorophyll a-protein from Amphidinium carterae. J Phys Chem A 103: 2267–2273

    Article  CAS  Google Scholar 

  • Bautista JA, Connors RE, Raju BB, Hiller RG, Sharples FP, Gosztola D, Wasielewski M and Frank HA (1999b) Exited state properties of peridinin: Observation of solvent dependence of the lowest excited singlet state lifetime and spectral behavior unique among carotenoids. J Phys Chem B 103: 8751–8758

    Article  CAS  Google Scholar 

  • Chadwick B, Zhang C, Cogdell R and Frank H (1987) The effects of lithium dodecyl sulfate and sodium borohydride on the absorption spectrum of the B800–850 light harvesting complex from Rhodopseudomonas acidophila 7750. Biochim Biophys Acta 893: 444–451

    Article  CAS  Google Scholar 

  • Christensen R (1999) The electronic states of carotenoids. In: Frank H, Young A, Britton G and Cogdell R (eds) The Photochemistry of Carotenoids, pp 137–159, The Netherlands

  • Cogdell R, Hipkins M, MacDonald W and Truscott T (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 R, Andersson P and Gillbro T (1992) Carotenoid singlet states and their involvement in photosynthetic light-harvesting pigments. J Photochem Photobiol B 15: 105–112

    Article  CAS  Google Scholar 

  • Cogdell R, Isaacs N, Howard T, McLuskey K, Fraser N and Prince S (1999) How photosynthetic bacteria harvest solar energy. J Bacteriol 181: 3869–3879

    PubMed  CAS  Google Scholar 

  • Cory MG, Zerner MC, Hu X and Schulten K (1998) Electronic Excitations in Aggregates of Bacteriochlorophylls. J Phys Chem B 102(39): 7640–7650

    Article  CAS  Google Scholar 

  • Damjanović A, Ritz T and Schulten K (1999) Energy transfer between carotenoids and bacteriochlorophylls in a light harvesting protein. Phys Rev E 59: 3293–3311

    Article  Google Scholar 

  • Damjanović A, Ritz T and Schulten K (2000a) Excitation energy trapping by the reaction center of Rhodobacter sphaeroides. Int J Quantum Chem 77: 139–151

    Article  Google Scholar 

  • Damjanović A, Ritz T and Schulten K (2000b) Excitation transfer in the peridinin-chlorophyll-protein of Amphidinium carterae. Biophys J 79: 1695–1705

    Article  PubMed  Google Scholar 

  • Desamero R, Chynwat V, Van der Hoef I, Jansen F, Lugtenburg J, Gosztola D, Wasielewski M, Cua A, Bocian D and Frank H (1998) Mechanism of energy transfer from carotenoids to bacteriochlorophyll: Light-harvesting by carotenoids having different extents of π-electron conjugation incorporated in the B850 antenna complex from the carotenoidless bacterium Rhodobacter sphaeroides R-26.1. J Phys Chem B 102: 8151–8162

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Englman R and Jortner J (1970) The energy gap law for radiationless transitions in large molecules. Mol Phys 18: 145–164

    Article  CAS  Google Scholar 

  • Farshoosh R, Chynwat V, Gebhard R, Lugtenburg J and Frank H (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  Google Scholar 

  • Farshoosh R, Chynwat V, Gebhard R, Lugtenburg J and Frank H (1997) Triplet energy transfer between the primary donor and carotenoids in Rhodobacter sphaeroides R-26.1 reaction center incorporated with spheroidene analogs having different extent of π-electron conjugation. Photochem Photobiol 66: 97–104

    Google Scholar 

  • Förster T (1948) Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann Phys (Leipzig) 2: 55–75

    Google Scholar 

  • Förster T (1965) Delocalized Excitation and Excitation Transfer, pp. 93–137. Academic Press, New York

    Google Scholar 

  • Frank H (1993) Carotenoids in photosynthetic bacterial reaction centers: structure, spectroscopy, and photochemistry. In: The Photosynthetic Reaction Center, Vol. 2, pp 221–237.

    CAS  Google Scholar 

  • Frank H, Bautista J, Josue J and Young A (2000a) Mechanism of nonphotochemical quenching in green plants: Energies of the lowest excited singlet states of violaxanthin and zeaxanthin. Biochemistry 39: 2831–2837

    Article  PubMed  CAS  Google Scholar 

  • Frank H, Chynwat V, Desamero R, Farshoosh R, Erickson J and Bautista J (1997) On the photophysics and photochemical properties of carotenoids and their role as light-harvesting pigments in photosynthesis. Pure Appl Chem 68: 2117–2124

    Google Scholar 

  • Frank H and Cogdell R (1996) Carotenoids in photosynthesis. Photochem Photobiol 63: 257–264

    PubMed  CAS  Google Scholar 

  • Frank HA, Bautista JA, Josue J, Pendon Z, Hiller RG, Sharples FP, Gosztola D and Wasielewski MR (2000b) Effect of the solvent environment on the spectroscopic properties and dynamics of the lowest excited states of carotenoids. J Phys Chem B 104: 4569–4577

    Article  CAS  Google Scholar 

  • Freer A, Prince S, Sauer K, Papiz M, Hawthornthwaite-Lawless A, McDermott G, Cogdell R and Isaacs N (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 A −g energies of all-trans-neurosporene and spheroidene as determined by fluorescence spectroscopy. Chem Phys Lett 288: 847–863

    Article  CAS  Google Scholar 

  • Gillbro T, Cogdell RF and Sundström V (1988) Energy transfer from carotenoid to bacteriochlorophyll a in the B800–820 antenna complexes from Rhodopseudomonas acidophila strain 7050. FEBS Lett 235: 169–172

    Article  CAS  Google Scholar 

  • Herek J, Polivka T, Pullerits T, Fowler G, Hunter C and Sundstrom V (1998) Ultrafast carotenoid band shifts probe structure and dynamics in photosynthetic antenna complexes. Biochem 37: 7057–7061

    Article  CAS  Google Scholar 

  • Hofmann E, Wrench P, Sharples F, Hiller R, Welte W and Diederichs K (1996) Structural basis of light harvesting by carotenoids: peridinin-chlorophyll-protein from Amphidinium carterae. Science 272: 1788–1791

    PubMed  CAS  Google Scholar 

  • Hu X, Ritz T, Damjanović A and Schulten K (1997) Pigment organization and transfer of electronic excitation in the purple bacteria. J Phys Chem B 101: 3854–3871

    Article  CAS  Google Scholar 

  • Hudson B and Kohler B (1972) Chem Phys Lett 14: 299–304

    Article  CAS  Google Scholar 

  • Humphrey WF, Dalke A and Schulten K (1996) VMD — visual molecular dynamics. J Mol Graphics 14: 33–38

    Article  CAS  Google Scholar 

  • Koepke J, Hu X, Münke C, Schulten K and Michel H (1996) The crystal structure of the light harvesting complex II (B800–850) from Rhodospirillum molischianum. Structure 4: 581–597

    Article  PubMed  CAS  Google Scholar 

  • Koyama Y, Kuki M, Andersson P 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 

  • Kramer H, Van Grondelle R, Hunter CN, Westerhuis W and Amesz J (1984) Pigment organization of the B800–850 antenna complex of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 765: 156–165

    Article  CAS  Google Scholar 

  • Krueger B, Scholes G, Jimenez R and Fleming G (1998a) Electronic excitation transfer from carotenoid to bacteriochlorophyll in the purple bacterium Rhodopseudomonas acidophila. J Phys Chem B 102: 2284–2292

    Article  CAS  Google Scholar 

  • Krueger BP, Scholes GD and Fleming GR (1998b) Calculation of couplings and energy-transfer pathways between the pigments of LH2 by the ab initio transition density cube method. J Phys Chem B 102: 5378–5386

    Article  CAS  Google Scholar 

  • Krueger B, Scholes G, Gould I and Fleming G (1999) Carotenoid mediated B800–850 coupling in LH2. Phys Chem Comm 8: 9/03172C.

  • Kuki M, Nagae H, Cogdell R and Koyama Y (1994) Solvent Effect on spheroidene in nonpolar and polar solutions and the environment of spheroidene in the light-harvesting complexes of Rhodobacter sphaeroides 2.4.1 as revealed by the energy of the (1)A(g)(−)B-1(U)+ absorption and the frequencies of the vibronically coupled C=C stretching Raman lines in the (1)A(G)(−) And 2(1)A(G)(−) states. Photochem Photobiol 59: 116

    CAS  Google Scholar 

  • Macpherson A and Gillbro T (1998) Solvent dependence of the ultrfast S2-S1 internal conversion rate of β-carotene. J Phys Chem A 102: 5049–5058

    Article  CAS  Google Scholar 

  • Macpherson AM, Arellano JB, Fraser NJ, Cogdell RJ and Gillbro T (1998) Ultrafast energy transfer from rhodopin glucoside in the light harvesting complexes of Rps. acidophila. In: Garab G (ed) Photosynthesis: Mechanism and Effects, Vol. 1, pp. 9–14. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • McDermott G, Prince S, Freer A, Hawthornthwaite-Lawless A, Papiz M, Cogdell R and Isaacs N (1995) Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374: 517–521

    Article  CAS  Google Scholar 

  • McWeeny R (1992) Academic Press, London

  • Mimuro M, Nagashima U, Takaichi S, Nishimura Y, Yamazaki I and Katoh T (1992) Molecular structure and optical properties of carotenoids for the in vivo energy transfer function in the algal photosynthetic pigment system. Biochim Biophys Acta 1098: 271–274

    CAS  Google Scholar 

  • Mukai K, Abe S and Sumi H (1999) Theory of rapid excitation-energy transfer from B800 to optically-forbidden exciton states of B850 in the antenna system LH 2 of Photosynthetic purple bacteria. J Phys Chem B 103: 6096–6102

    Article  CAS  Google Scholar 

  • Nagae H, Kakitani T, Katohi 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 

  • Nagae H, Kuki M, Zhang J-P, Sashima T, Mukai Y and Koyama Y (2000) Vibronic coupling through the in-phase C=C stretching mode plays a major role in the 2A −g -to-1A −g internal conversion of all-trans-β-carotene. J Phys Chem A 104: 4155–4166

    Article  CAS  Google Scholar 

  • Naqvi KR (1980) The mechanism of singlet-singlet excitation energy transfer from carotenoids to chlorophyll. Photochem Photobiol 31: 523–524

    Google Scholar 

  • Noguchi T, Kolaczkowski S, Gartner W and Atkinson GH (1990) Resonance Raman spectra of 13-demethylretinal bacteriorhodopsin and of a picosecond bathochromic photocycle intermediate. J Phys Chem 94: 4920–4926

    Article  CAS  Google Scholar 

  • Polivka T, Herek J, Zigmantas D, Akerlund H-E and Sundstrom V (1999) Direct observation of the (forbidden) S1 state in carotenoids. Proc Natl Acad Sci USA 96: 4914–4917

    Article  PubMed  CAS  Google Scholar 

  • Ricci M, Bradforth SE, Jimenez R and Fleming GR (1996) Internal conversion and energy transfer dynamics of spheroidene in solution and in the LII-1 and LII-2 light-harvesting complexes. Chem Phys Lett 259: 381–390

    Article  CAS  Google Scholar 

  • Ritz T, Damjanović A and Schulten K (1998a) Light-harvesting and photoprotection by carotenoids: Structure-based calculations for photosynthetic antenna systems. In: Garab G (ed) Photosynthesis: Mechanisms and Effects (Proceedings of the XIth International Congress on Photosynthesis), Vol 1, pp 487–490. Kluwer Academic Publishers, Dordrecht, The Netherlands

    Google Scholar 

  • Ritz T, Hu X, Damjanović A and Schulten K (1998b) Excitons and excitation transfer in the photosynthetic unit of purple bacteria. J Luminescence 76–77: 310–321

    Article  Google Scholar 

  • Sashima T, Shiba M, Hashimoto H, Nagae H and Koyama Y (1998) The A −g energy of crystalline all-trans-spheroidene as determinded by resonance-Raman excitation profiles. Chem Phys Lett 290: 36–42

    Article  CAS  Google Scholar 

  • Sashima T, Nagae H, Kuki M and Koyama Y (1999) A new singlet-excited state of all-trans-spheroidene as detected by resonance-Raman excitation profiles. Chem Phys Lett 299: 187–194

    Article  CAS  Google Scholar 

  • Sashima T, Koyama Y, Yamada T and Hashimoto H (2000) The 1B −u and 2A −g energies of lycopene, β-carotene and Mini-9-β-carotene as determined by resonance-Raman excitation profile: Dependence of the 1B −u -state energy on the conjugation length. J Phys Chem B 104: 5011–5019

    Article  CAS  Google Scholar 

  • Scholes G, Gould I, Cogdell R and Fleming G (1999) Ab initio molecular orbital calculations of electronic couplings in the LH 2 bacterial light-harvesting complex of Rps. acidophila. J Phys Chem B 103: 2543–2553

    Article  CAS  Google Scholar 

  • Scholes G, Harcourt R and Ghiggino K (1995) Rate expressions for excitation transfer. An ab initio study of electronic factors in excitation transfer and exciton resonance interactions. J Chem Phys 102: 7302–7312

    Article  Google Scholar 

  • Scholes GD, Harcourt RD and Fleming GR (1997) Electronic interactions in photosynthetic light-harvesting complexes: The role of carotenoids. J Phys Chem B 101: 7302–7312

    Article  CAS  Google Scholar 

  • Schulten K and Karplus M (1972) On the origin of a low-lying forbidden transition in polyenes and related molecules. Chem Phys Lett 14(3): 305–309

    Article  CAS  Google Scholar 

  • Schulten K, Ohmine I and Karplus M (1976) Correlation effects in the spectra of polyenes. J Chem Phys 64: 4422–4441

    Article  CAS  Google Scholar 

  • Shreve AP, Trautman JK, Frank HA, Owens TG and Albrecht AC (1991) Femtosecond Energy-transfer Processes in the B800–850 Light-harvesting Complex of Rhodobacter sphaeroides-2.4.1. Biochim Biophys Acta 1058: 280–288

    PubMed  CAS  Google Scholar 

  • Sumi H (1999) Theory on rates of excitation-energy transfer between molecular aggregates through distributed transition dipoles with application to the antenna system in bacterial photosynthesis. J Phys Chem B 103: 252–260

    Article  CAS  Google Scholar 

  • Sundstrom V, Pullerits T and Van Grondelle R (1999) Photosynthetic light-harvesting: Reconciling dynamics and structure of purple bacterial LH 2 reveals function of photosynthetic unit. J Phys Chem B 103: 2327–2346

    Article  Google Scholar 

  • Tavan P and Schulten K (1979) The 21 A g -11 B u energy gap in the polyenes: An extended configuration interaction study. J Chem Phys 70(12): 5407–5413

    Article  CAS  Google Scholar 

  • Tavan P and Schulten K (1986) The low-lying electronic excitations in long polyenes: A PPP-MRD-CI study. J Chem Phys 85(11): 6602–6609

    Article  CAS  Google Scholar 

  • Tavan P and Schulten K (1987) Electronic excitations in finite and infinite polyenes. Phys Rev B 36(8): 4337–4358

    Article  CAS  Google Scholar 

  • Thrash R, Fang H-B and Leroi G (1979) On the role of forbidden low-lying excited states of light-harvesting carotenoids in photosynthesis. Photochem Photobiol 29: 1049–1050

    CAS  Google Scholar 

  • Trautmann J, Shreve A, Violette C, Frank HA, Owens T and Albrecht A (1990) Femtosecond dynamics of energy transfer in B800–850 light-harvesting complexes of Rhodobacter sphaeroides. Proc Natl Acad Sci USA 87: 215–219

    Article  Google Scholar 

  • Van Grondelle R, Kramer H and Rijgersberg C (1982) Energy transfer in the B800–B850-carotenoid light-harvesting complex of various mutants of Rhodopseudomonas sphaeroides and of Rhodopseudomonas capsulata. Biochim Biophys Acta 682: 208–215

    Article  Google Scholar 

  • Watanabe M and Karplus M (1993) Dynamics of molecules with internal degrees of freedom by multiple time-step methods. J Chem Phys 99(10): 8063–8074

    Article  CAS  Google Scholar 

  • Young A and Frank H (1996) Energy transfer reactions involving carotenoids: Quenching of chlorophyll fluorescence. Photochem Photobiol B 36: 3–16

    Article  CAS  Google Scholar 

  • Zhang J-P, Fujii R, Qian P, Inaba T, Mizoguchi T and Koyama Y (2000) Mechanism of the carotenoid-to-bacteriochlorophyll energy transfer via the S1 state in the LH 2 complexes from purple bacteria. J Phys Chem B 104: 3683–3691

    Article  CAS  Google Scholar 

  • Zhang Z, Huang L, Chi Y-I, Kim KK, Crofts AR, Berry EA and Kim S-H (1998) Electron transfer by domain movement in cytochrome bc 1. Nature 392: 677–684

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Theoretical Biophysics Group, Beckman Institute, University of Illinois at Urbana–Champaign, Urbana, IL, 61801, USA

    Thorsten Ritz & Ana Damjanović

  2. Theoretical Biophysics Group, Beckman Institute, University of Illinois at Urbana–Champaign, Urbana, IL, 61801, USA

    Klaus Schulten

  3. Faculty of Science, Kwansei Gakuin University, Uegahara, Nishinomiya, 662, Japan

    Jian-Ping Zhang & Yasushi Koyama

Authors
  1. Thorsten Ritz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ana Damjanović
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Klaus Schulten
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jian-Ping Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasushi Koyama
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Klaus Schulten.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ritz, T., Damjanović, A., Schulten, K. et al. Efficient light harvesting through carotenoids. Photosynthesis Research 66, 125–144 (2000). https://doi.org/10.1023/A:1010750332320

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1010750332320

Search

Navigation