Skip to main content

Advertisement

SpringerLink
Log in

The contributions of 49ers to the measurements and models of ultrafast photosynthetic energy transfer

  • History and Biography
  • Published:
Photosynthesis Research Aims and scope Submit manuscript

Abstract

Progress in measuring and understanding the mechanism of the elementary energy transfer steps in photosynthetic light harvesting from roughly 1949 to the present is sketched with a focus on the group of scientists born in 1949 ± 1. Improvements in structural knowledge, laser spectroscopic methods, and quantum dynamical theories have led to the ability to record and calculate with reasonable accuracy the timescales of elementary energy transfer steps. The significance of delocalized excited states and of near-field Coulombic coupling is noted. The microscopic understanding enables consistent coarse graining and should enable a much-improved understanding of the regulation of photosynthetic light harvesting.

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

Abbreviations

Chl:

Chlorophyll

BChl:

Bacteriochlorophyll

FMO:

Fenna, Mathews, Olson Complex

2D:

Two-dimensional

References

  • Agarwal R, Rizvi AH, Prall BS, Olsen JD, Hunter CN, Fleming GR (2002) Nature of disorder and inter-complex energy transfer in LH2 at room temperature: a three pulse photon echo peak shift study. J Phys Chem A 106:7573–7578. doi:10.1021/jp014054m

    Article  CAS  Google Scholar 

  • Amarnath K, Bennett D, Schneider AR, Fleming GR (2015) Multiscale model of photosystem II light harvesting in the thylakoid membrane of plants. PNAS 113(5):1156–1161

    Article  Google Scholar 

  • Arnold W, Meek ES (1956) The polarization of fluorescence and energy transfer in grana. Arch Biochem Biophys 60:82–90. doi:10.1016/0003-9861(56)90399-X

    Article  CAS  PubMed  Google Scholar 

  • Beauregard M, Martin I, Holzwarth AR (1991) Kinetic modeling of exciton migration in photosynthetic systems 0.1. effects of pigment heterogeneity and antenna topography on exciton kinetics and charge separation yields. Biochim Biophys Acta 1060:271–283. doi:10.1016/S0005-2728(05)80317-2

    Article  CAS  Google Scholar 

  • Bennett D, Amarnath K, Fleming GR (2013) A structure-based model of energy transfer reveals the principles of light harvesting in photosystem ii supercomplexes. J Am Chem Soc 135(24):9164–9173

    Article  CAS  PubMed  Google Scholar 

  • Bergstrom H, Sundström V, van Grondelle R, Akesson E, Gillbro T (1986) Energy-transfer within the isolated light-harvesting b800–850 pigment-protein complex of Rhodobacter sphaeroides. Biochim Biophys Acta 852:279–287. doi:10.1016/0005-2728(86)90233-1

    Article  Google Scholar 

  • Bopp MA, Jia YW, Li LQ, Cogdell RJ, Hochstrasser RM (1997) Fluorescence and photobleaching dynamics of single light-harvesting complexes. Proc Natl Acad Sci USA 94:10630–10635. doi:10.1073/pnas.94.20.10630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borisov AY, Freiberg AM, Godik VI, Rebane KK, Timpmann KE (1985) Kinetics of picosecond bacteriochlorophyll luminescence invivo as a function of the reaction center state. Biochim Biophys Acta 807:221–229. doi:10.1016/0005-2728(85)90252-X

    Article  CAS  Google Scholar 

  • Bradforth SE, Jimenez R, Vanmourik F, van Grondelle R, Fleming GR (1995) Excitation transfer in the core light-harvesting complex (LH-1) of Rhodobacter sphaeroides: an ultrafast fluorescence depolarization and annihilation study. J Phys Chem 99:16179–16191. doi:10.1021/j100043a071

    Article  CAS  Google Scholar 

  • Brixner T, Stenger J, Vaswani HM, Cho M, Blankenship RE, Fleming GR (2005) Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434:625–628. doi:10.1038/nature03429

    Article  CAS  PubMed  Google Scholar 

  • Chachisvillis M, Kühn O, Pullerits T, Sundström V (1997) Excitons in photosynthetic purple bacteria: wavelike motion or incoherent hopping? J Phys Chem B 101:7275–7283. doi:10.1021/jp963360a

    Article  Google Scholar 

  • Collini E, Wong CY, Wilk KE, Curmi PMG, Brumer P, Scholes GD (2010) Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463:644–647. doi:10.1038/nature08811

    Article  CAS  PubMed  Google Scholar 

  • Cowan ML, Ogilvie JP, Miller RJD (2004) Two-dimensional spectroscopy using diffractive optics based phased-locked photon echoes. Chem Phys Lett 386:184–189. doi:10.1016/j.cplett.2004.01.027

    Article  CAS  Google Scholar 

  • Dean JC, Mirkovic T, Toa ZSD, Oblinsky DG, Scholes GD (2016) Vibronic enhancement of algae light harvesting. J Chem 1, 858–872. doi:10.1016/jchempr.2016.11.002

    CAS  Google Scholar 

  • Du M, Xie X, Mets L, Fleming GR (1994) Direct observation of ultrafast energy-transfer processes in light-harvesting complex-II. J Phys Chem 98:4736–4741. doi:10.1021/j100068a041

    Article  CAS  Google Scholar 

  • Duysens LNM (1952) Transfer of excitation energy in photosynthesis. Proefschrift, Utrecht

    Google Scholar 

  • Duysens LNM (1964) Photosynthesis. Prog Biophys Mol Biol 14:1–104. doi:10.1016/S0079-6107(64)80003-1

    Article  Google Scholar 

  • Eads DD, Castner EW, Alberte RS, Mets L, Fleming GR (1989) Direct observation of energy-transfer in a photosynthetic membrane: chlorophyll-b to chlorophyll-a transfer in LHC. J Phys Chem 93:8271–8275. doi:10.1021/j100363a001

    Article  CAS  Google Scholar 

  • Emerson R, Arnold W (1932) The photochemical reaction in photosynthesis. J Gen Physiol 16:191–205. doi:10.1085/jgp.16.2.191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engel GS et al (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782–786. doi:10.1038/nature05678

    Article  CAS  PubMed  Google Scholar 

  • Förster T (1946) Energiewanderung Und Fluoreszenz. Naturwissenschaften 33:166–175

    Article  Google Scholar 

  • Förster T (1947) Ein Beitrag Zur Theorie Der Photosynthese Z Naturforsch B 2:174–182

  • Förster T (1948) *Zwischenmolekulare Energiewanderung Und Fluoreszenz Ann Phys-Berlin 2:55–75

  • Franck J, Livingston R (1949) Remarks on intra-molecular and inter-molecular migration of excitation energy. Rev Mod Phys 21:505–509. doi:10.1103/RevModPhys.21.505

    Article  CAS  Google Scholar 

  • Fujihashi Y, Fleming GR, Ishizaki A (2015) Impact of environmentally induced fluctuations on quantum mechanically mixed electronic and vibrational pigment states in photosynthetic energy transfer and 2D electronic spectra J Chem Phys. doi:10.1063/1.4914302

    PubMed  Google Scholar 

  • Gaffron H, Wohl K (1936) On the theory of assimilation. Naturwissenschaften 24:81–90

    Article  CAS  Google Scholar 

  • Ishizaki A, Fleming GR (2009) Unified treatment of quantum coherent and incoherent hopping dynamics in electronic energy transfer: reduced hierarchy equation approach J Chem Phys. doi:10.1063/1.3155372

    Google Scholar 

  • Jang SJ, Newton MD, Silbey RJ (2004) Multichromophoric Förster resonance energy transfer Phys Rev Lett. doi:10.1103/PhysRevLett.92.218301

    Google Scholar 

  • Jelezko F, Tietz C, Gerken U, Wrachtrup J, Bittl R (2000) Single-molecule spectroscopy on photosystem I pigment-protein complexes. J Phys Chem B 104:8093–8096. doi:10.1021/jp001332t

    Article  CAS  Google Scholar 

  • Jimenez R, van Mourik F, Yu JY, Fleming GR (1997) Three-pulse photon echo measurements on LH1 and LH2 complexes of Rhodobacter sphaeroides: a nonlinear spectroscopic probe of energy transfer. J Phys Chem B 101:7350–7359. doi:10.1021/jp970299g

    Article  CAS  Google Scholar 

  • Jonas DM (2003) Two-dimensional femtosecond spectroscopy. Annu Rev Phys Chem 54:425–463. doi:10.1146/annurev.physchem.54.011002.103907

    Article  CAS  PubMed  Google Scholar 

  • Joo TH, Jia YW, Yu JY, Lang MJ, Fleming GR (1996a) Third-order nonlinear time domain probes of solvation dynamics. J Chem Phys 104:6089–6108. doi:10.1063/1.471276

    Article  CAS  Google Scholar 

  • Joo TH, Jia YW, Yu JY, Jonas DM, Fleming GR (1996b) Dynamics in isolated bacterial light harvesting antenna (LH2) of Rhodobacter sphaeroides at room temperature. J Phys Chem 100:2399–2409. doi:10.1021/jp951652q

    Article  CAS  Google Scholar 

  • Kollman VH, Shapiro SL, Campillo AJ (1975) Photosynthetic studies with a 10-psec resolution streak camera. Biochem Biophys Res Commun 63:917–923. doi:10.1016/0006-291x(75)90656-7

    Article  CAS  PubMed  Google Scholar 

  • Krueger BP, Scholes GD, Fleming GR (1998) 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. doi:10.1021/jp9811171

    Article  CAS  Google Scholar 

  • Kudzmauskas S, Liuola V, Trinkunas G, Valkunas L (1985) Nonlinear phenomena in chromatophores of photosynthetic bacteria excited by picosecond laser-pulses. Phys Lett A 111:378–381. doi:10.1016/0375-9601(85)90375-5

    Article  Google Scholar 

  • Lewis NHC, Gruenke NL, Oliver TAA, Ballottari M, Bassi R, Fleming GR (2016) Observation of electronic excitation transfer through light harvesting complex II using two-dimensional electronic-vibrational spectroscopy. J Phys Chem Lett 7:4197–4206. doi:10.1021/acs.jpclett.6b02280

    Article  CAS  Google Scholar 

  • London F (1942) On centers of van der Waals attraction. J Phys Chem 46:305–316. doi:10.1021/j150416a009

    Article  CAS  Google Scholar 

  • Maly P, Gruber JM, Cogdell RJ, Mancal T, van Grondelle R (2016) Ultrafast energy relaxation in single light-harvesting complexes. Proc Natl Acad Sci USA 113:2934–2939. doi:10.1073/pnas.1522265113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McDermott G, Prince SM, Freer AA, Hawthornthwaitelawless AM, Papiz MZ, Cogdell RJ, Isaacs NW (1995) Crystal-structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374:517–521. doi:10.1038/374517a0

    Article  CAS  Google Scholar 

  • Mohseni M, Omar Y, Engel GS, Plenio MB Eds (2014) Quantum effects in biology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Monahan DM, Whaley-Mayda L, Ishizaki A, Fleming GR (2015) Influence of weak vibrational-electronic couplings on 2D electronic spectra and inter-site coherence in weakly coupled photosynthetic complexes J Chem Phys. doi:10.1063/1.4928068

    PubMed  Google Scholar 

  • Mukamel S (1995) Principles of nonlinear optical spectroscopy. Oxford series in optical and imaging sciences, vol 6. Oxford University Press, Oxford

    Google Scholar 

  • Nalbach P, Ishizaki A, Fleming GR, Thorwart M (2011) Iterative path-integral algorithm versus cumulant time-nonlocal master equation approach for dissipative biomolecular exciton transport New J Phys. doi:10.1088/1367-2630/13/6/063040

    Google Scholar 

  • Novoderezhkin V, Wendling M, van Grondelle R (2003) Intra- and interband transfers in the B800-B850 antenna of Rhodospirillum molischianum: redfield theory modeling of polarized pump-probe kinetics. J Phys Chem B 107:11534–11548. doi:10.1021/jp035432l

    Article  CAS  Google Scholar 

  • Novoderezhkin V, Marin A, van Grondelle R (2011) Intra- and inter-monomeric transfers in the light harvesting LHCII complex: the Redfield-Förster picture. Phys Chem Chem Phys 13(38):17093–17103. doi:10.1039/c1cp21079c

    Article  CAS  PubMed  Google Scholar 

  • Oliver TAA, Lewis NHC, Fleming GR (2014) Correlating the motion of electrons and nuclei with two-dimensional electronic-vibrational spectroscopy. Proc Natl Acad Sci USA 111:10061–10066. doi:10.1073/pnas.1409207111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Panitchayangkoon G et al (2010) Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc Natl Acad Sci USA 107:12766–12770. doi:10.1073/pnas.1005484107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Porter G, Tredwell CJ, Searle GFW, Barber J (1978) Picosecond time-resolved energy-transfer in Porphyridium cruentum 0.1. intact alga. Biochim Biophys Acta 501:232–245. doi:10.1016/0005-2728(78)90029-4

    Article  CAS  PubMed  Google Scholar 

  • Pullerits T, Freiberg A (1991) Picosecond fluorescence of simple photosynthetic membranes: evidence of spectral inhomogeneity and directed energy-transfer. Chem Phys 149:409–418. doi:10.1016/0301-0104(91)90040-Z

    Article  CAS  Google Scholar 

  • Raszewski G, Renger T (2008) Light harvesting in photosystem II core complexes is limited by the transfer to the trap: can the core complex turn into a photoprotective mode? J Am Chem Soc 130(13):4431–4446. doi:10.1021/ja7099826

    Article  CAS  PubMed  Google Scholar 

  • Redfield AG (1957) On the theory of relaxation processes. IBM J Res Dev 1:19–31

    Article  Google Scholar 

  • Robinson GW (1966) Excitation transfer and trapping in photosynthesis. Brookhaven Sym Biol 19: 16–48

    CAS  Google Scholar 

  • Savikhin S, Buck DR, Struve WS (1997) Oscillating anisotropies in a bacteriochlorophyll protein: evidence for quantum beating between exciton levels. Chem Phys 223:303–312. doi:10.1016/S0301-0104(97)00223-1

    Article  CAS  Google Scholar 

  • Schlau-Cohen GS et al (2015) Single-molecule Identification of quenched and unquenched states of LHCII. J Phys Chem Lett 6:860–867. doi:10.1021/acs.jpclett.5b00034

    Article  CAS  PubMed  Google Scholar 

  • Scholes GD, Fleming GR (2000) On the mechanism of light harvesting in photosynthetic purple bacteria: B800 to B850 energy transfer. J Phys Chem B 104:1854–1868. doi:10.1021/jp993435l

    Article  CAS  Google Scholar 

  • Scholes GD, Jordanides XJ, Fleming GR (2001) Adapting the Förster theory of energy transfer for modeling dynamics in aggregated molecular assemblies. J Phys Chem B 105:1640–1651. doi:10.1021/jp003571m

    Article  CAS  Google Scholar 

  • Singhal GS, Rabinowitch E (1969) Measurement of fluorescence lifetime of chlorophyll a in vivo. Biophys J 9:586–591

    Article  CAS  PubMed  PubMed Central  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. doi:10.1021/jp983477u

    Article  CAS  Google Scholar 

  • Tiwari V, Peters WK, Jonas DM (2013) Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework. Proc Natl Acad Sci USA 110:1203–1208. doi:10.1073/pnas.1211157110

    Article  CAS  PubMed  Google Scholar 

  • van Oijen AM, Ketelaars M, Kohler J, Aartsma TJ, Schmidt J (1999) Unraveling the electronic structure of individual photosynthetic pigment-protein complexes. Science 285:400–402. doi:10.1126/science.285.5426.400

    Article  PubMed  Google Scholar 

  • Wei XP et al (2016) Structure of spinach photosystem II-LHCII supercomplex at 3.2 angstrom resolution. Nature 534:69–76. doi:10.1038/nature18020

    Article  CAS  PubMed  Google Scholar 

  • Yang MN, Fleming GR (2002) Influence of phonons on exciton transfer dynamics: comparison of the Redfield, Förster, and modified Redfield equations. Chem Phys 275:355–372. doi:10.1016/S0301-0104(01)00540-7

    Article  CAS  Google Scholar 

  • Ying LM, Xie XS (1998) Fluorescence spectroscopy, exciton dynamics, and photochemistry of single allophycocyanin trimers. J Phys Chem B 102:10399–10409. doi:10.1021/jp983227d

    Article  CAS  Google Scholar 

  • Yu JY, Nagasawa Y, van Grondelle R, Fleming GR (1997) Three pulse echo peak shift measurements on the B820 subunit of LH1 of Rhodospirillum rubrum. Chem Phys Lett 280:404–410. doi:10.1016/S0009-2614(97)01135-4

    Article  CAS  Google Scholar 

  • Zhang WM, Meier T, Chernyak V, Mukamel S (1998) Exciton-migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes. J Chem Phys 108:7763–7774. doi:10.1063/1.476212

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The author is grateful for the continuous support of the Director, Office of Science, Office of Basic Energy Sciences, US Department of Energy under Contract DE-AC02-05CH11231, and the Division of Chemical Sciences, Geosciences and Biosciences Division, Office of Basic Energy Sciences through Grant DE-AC03-76F000098 (at Lawrence Berkeley National Laboratory and University of California, Berkeley). I also thank Leonas Valkunas and Rienk van Grondelle for help on some of the history.

Author information

Authors and Affiliations

  1. Department of Chemistry and Kavli Energy NanoScience Institute, University of California Berkeley, Berkeley, CA, 94720, USA

    Graham R. Fleming

  2. Molecular Biophysics and Integrated Bioengineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

    Graham R. Fleming

Authors
  1. Graham R. Fleming
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Graham R. Fleming.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fleming, G.R. The contributions of 49ers to the measurements and models of ultrafast photosynthetic energy transfer. Photosynth Res 135, 3–8 (2018). https://doi.org/10.1007/s11120-017-0360-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11120-017-0360-4

Keywords

Search

Navigation