Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review Article
  • Published:

Lessons from nature about solar light harvesting

Nature Chemistry volume 3, pages 763–774 (2011)Cite this article

Subjects

Abstract

Solar fuel production often starts with the energy from light being absorbed by an assembly of molecules; this electronic excitation is subsequently transferred to a suitable acceptor. For example, in photosynthesis, antenna complexes capture sunlight and direct the energy to reaction centres that then carry out the associated chemistry. In this Review, we describe the principles learned from studies of various natural antenna complexes and suggest how to elucidate strategies for designing light-harvesting systems. We envisage that such systems will be used for solar fuel production, to direct and regulate excitation energy flow using molecular organizations that facilitate feedback and control, or to transfer excitons over long distances. Also described are the notable properties of light-harvesting chromophores, spatial-energetic landscapes, the roles of excitonic states and quantum coherence, as well as how antennas are regulated and photoprotected.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Structural organization of light-harvesting complexes and reaction centres in higher plants and green algae.
Figure 2: Antenna complexes matter more in low light conditions.
Figure 3: Structure and spectroscopy of the major light-harvesting complex of higher plants, LHCII.
Figure 4: Organization of light-harvesting antenna complexes relative to the photosynthetic membrane.
Figure 5: How electronic coherence creates chromophores.
Figure 6: Two-dimensional electronic spectroscopy for the detection of quantum coherence104.

Similar content being viewed by others

References

  1. Field, C. B., Behrenfeld, M. J., Randerson, J. T. & Falkowski, P. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281, 237–240 (1998).

    CAS  PubMed  Google Scholar 

  2. Larkum, A. W. D. Limitations and prospects of natural photosynthesis for bioenergy production. Curr. Opin. Biotechnol. 21, 271–276 (2010).

    CAS  PubMed  Google Scholar 

  3. Blankenship, R. E. et al. Comparing photosynthetic efficienciencies and recognizing the potential for improvement. Science 332, 805–809 (2011).

    CAS  PubMed  Google Scholar 

  4. Lewis, N. S. & Nocera, D. G. Powering the planet: Chemical challenges in solar energy utilization. Proc. Natl Acad. Sci. USA 103, 15729–15735 (2006).

    CAS  PubMed  Google Scholar 

  5. Remacle, F., Speiser, S. & Levine, R. D. Intermolecular and intramolecular logic gates. J. Phys. Chem. B 105, 5589–5591 (2001).

    CAS  Google Scholar 

  6. Credi, A. Molecules that make decisions. Angew. Chem. Int. Ed. 46, 5472–5475 (2007).

    CAS  Google Scholar 

  7. Szacilowski, K. Digital information processing in molecular systems. Chem. Rev. 108, 3481–3548 (2008).

    CAS  PubMed  Google Scholar 

  8. Green, B. R. & Parson, W. W. (eds) Light-Harvesting Antennas in Photosynthesis (Kluwer, Dordrecht, 2003).

    Google Scholar 

  9. Gust, D., Moore, T. A. & Moore, A. L. Solar fuels via artificial photosynthesis. Acc. Chem. Res. 42, 1890–1898 (2009).

    CAS  PubMed  Google Scholar 

  10. Wasielewski, M. R. Self-assembly strategies for integrating light harvesting and charge separation in artificial photosynthetic systems. Acc. Chem. Res. 42, 1910–1921 (2009).

    CAS  Google Scholar 

  11. Guldi, D. M. Fullerene-porphyrin architectures; photosynthetic antenna and reaction center models. Chem. Soc. Rev. 31, 22–36 (2002).

    CAS  PubMed  Google Scholar 

  12. Ball, P. The dawn of quantum biology. Nature 474, 272–274 (2011).

    CAS  PubMed  Google Scholar 

  13. Blankenship, R. E. Molecular Mechanisms of Photosynthesis (Blackwell, 2002).

    Google Scholar 

  14. Ke, B. Photosynthesis: Photobiochemistry and Photobiophysics (Advances in Photosynthesis series Vol. 10, Kluwer Academic, 2001).

    Google Scholar 

  15. van Grondelle, R., Dekker, J. P., Gillbro, T. & Sundström, V. Energy transfer and trapping in photosynthesis. Biochim. Biophys. Acta 1187, 1–65 (1994).

    Google Scholar 

  16. van Amerongen, H., Valkunas, L. & van Grondelle, R. Photosynthetic Excitons (World Scientific, 2000).

    Google Scholar 

  17. Sundström, V., Pullerits, T. & van Grondelle, R. Photosynthetic light-harvesting: Reconciling dynamics and structure of purple bacterial LH2 reveals function of photosynthetic unit. J. Phys. Chem. B 103, 2327–2346 (1999).

    Google Scholar 

  18. Grossman, A. R., Bhaya, D., Apt, K. E. & Kehoe, D. M. Light-harvesting complexes in oxygenic photosynthesis: Diversity, control, and evolution. Annu. Rev. Genetics 29, 231–288 (1995).

    CAS  Google Scholar 

  19. Cheng, Y. C. & Fleming, G. R. Dynamics of light harvesting in photosynthesis. Annu. Rev. Phys. Chem. 60, 241–262 (2009).

    CAS  PubMed  Google Scholar 

  20. Cogdell, R. J., Gall, A. & Köhler, J. The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Quarterly Rev. Biophys. 39, 227–324 (2006).

    CAS  Google Scholar 

  21. Scholes, G. D. Long-range resonance energy transfer in molecular systems. Annu. Rev. Phys. Chem. 54, 57–87 (2003).

    Article  CAS  Google Scholar 

  22. Olaya-Castro, A. & Scholes, G. D. Energy transfer from Förster-Dexter theory to quantum coherent light-harvesting. Int. Rev. Phys. Chem. 30, 49–77 (2011).

    CAS  Google Scholar 

  23. Beljonne, D., Curutchet, C., Scholes, G. D. & Silbey, R. Beyond Förster resonance energy transfer in biological and nanoscale systems. J. Phys. Chem. B 113, 6583–6599 (2009).

    CAS  PubMed  Google Scholar 

  24. Braslavsky, S. E. et al. Pitfalls and limitations in the practical use of Förster's theory of resonance energy transfer. Photochem. Photobiol. Sci. 7, 1444–1448 (2008).

    CAS  PubMed  Google Scholar 

  25. Clegg, R. M. Fluorescence resonance energy transfer. Curr. Opin. Biotech. 6, 103–110 (1995).

    CAS  PubMed  Google Scholar 

  26. Scholes, G. D. & Fleming, G. R. Energy transfer in photosynthesis. Adv. Chem. Phys. 132, 57–129 (2005).

    Google Scholar 

  27. Scholes, G. D. & Fleming, G. R. On the mechanism of light-harvesting in photosynthetic purple bacteria: B800 to B850 energy transfer. J. Phys. Chem. B 104, 1854–1868 (2000).

    CAS  Google Scholar 

  28. Van Grondelle, R. & Novoderezhkin, V. I. Energy transfer in photosynthesis: experimental insights and quantitative models. Phys. Chem. Chem. Phys. 8, 793–807 (2006).

    CAS  PubMed  Google Scholar 

  29. Novoderezhkin, V. & van Grondelle, R. Physical origins and models of energy transfer in photosynthetic light-harvesting. Phys. Chem. Chem. Phys. 12, 7352–7365 (2010).

    CAS  PubMed  Google Scholar 

  30. Sener, M. K., Olsen, J. D., Hunter, C. N. & Schulten, K. Atomic-level structural and functional model of a bacterial photosynthetic membrane vesicle. Proc. Natl Acad. Sci. USA 104, 15723–15728 (2007).

    CAS  PubMed  Google Scholar 

  31. Renger, T. Theory of excitation energy transfer: from structure to function. Photosynth. Res. 102, 471–485 (2009).

    CAS  PubMed  Google Scholar 

  32. Renger, T. & Schodder, E. Primary photophysical processes in photosystem II: Bridging the gap between crystal structure and optical spectra. ChemPhysChem 11, 1141–1153 (2010).

    CAS  PubMed  Google Scholar 

  33. Swager, T. M. The molecular wire approach to sensory signal amplification. Acc. Chem. Res. 31, 201–207 (1998).

    CAS  Google Scholar 

  34. Andrews, D. L. & Bradshaw, D. S. Optically nonlinear energy transfer in light-harvesting dendrimers. J. Chem. Phys. 121, 2445–2454 (2004).

    CAS  PubMed  Google Scholar 

  35. Singh-Rachford, T. N. & Castellano, F. N. Photon upconversion based on sensitized triplet-triplet annihilation. Coord. Chem. Rev. 254, 2560–2573 (2010).

    CAS  Google Scholar 

  36. Overmann, J., Cypionka, H. & Pfennig, N. An extremely low-light adapted phototrophic sulfur bacterium from the Black Sea. Limnol. Oceanogr. 37, 150–155 (1992).

    CAS  Google Scholar 

  37. Fassioli, F., Olaya-Castro, A., Scheuring, S., Sturgis, J. N. & Johnson, N. F. Energy transfer in light-adapted photosynthetic membranes: From active to saturated photosynthesis. Biophys. J. 97, 2464–2473 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Krueger, B. P., Scholes, G. D. & Fleming, G. R. 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 (1998).

    CAS  Google Scholar 

  39. Björn, L. O., Papageorgiou, G. C., Blankenship, R. E. & Govindjee. A viewpoint: Why chlorophyll a? Photosynth. Res. 99, 85–98 (2009).

    PubMed  Google Scholar 

  40. Tretiak, S. & Mukamel, S. Density matrix analysis and simulation of electronic excitations in conjugated and aggregated molecules. Chem. Rev. 102, 3171–3212 (2002).

    CAS  PubMed  Google Scholar 

  41. Scholes, G. D. & Rumbles, G. Excitons in nanoscale systems. Nature Mater. 5, 683–696 (2006).

    CAS  Google Scholar 

  42. Tretiak, S., Chernyak, V. & Mukamel, S. Chemical bonding and size scaling of nonlinear polarizabilities of conjugated polymers. Phys. Rev. Lett. 77, 4656–4659 (1996).

    CAS  PubMed  Google Scholar 

  43. Marder, S. R. et al. A unified description of the linear and nonlinear polarization in organic polymethine dyes. Science 265, 632–635 (1994).

    CAS  PubMed  Google Scholar 

  44. Birks, J. B. in Organic Molecular Photophysics Vol. 1 (ed. J. B. Birks) Ch. 1, 1–55 (Wiley, 1973).

    Google Scholar 

  45. Platt, J. R. Classification of the spectra of cata-condensed hydrocarbons. J. Chem. Phys. 17, 484–495 (1949).

    CAS  Google Scholar 

  46. Law, K. Y. Squaraine chemistry. Absorption, fluorescence emission, and photophysics of unsymmetrical squaraines. J. Phys. Chem. 99, 9818–9824 (1995).

    CAS  Google Scholar 

  47. Duysens, L. N. M. Transfer of light energy within the pigment systems present in photosynthesizing cells. Nature 168, 548–550 (1951).

    CAS  PubMed  Google Scholar 

  48. Blumen, A. & Manz, J. On the concentration and time dependence of the energy transfer to randomly distributed acceptors. J. Chem. Phys. 71, 4694–4702 (1979).

    CAS  Google Scholar 

  49. Den Hollander, W. T. F., Bakker, J. G. C. & van Grondelle, R. Trapping, loss and annihilation of excitations in a photosynthetic system. 1. Theoretical aspects. Biochim. Biophys. Acta 725, 492–507 (1983).

    CAS  Google Scholar 

  50. Anthanasopoulos, S., Hennebicq, E., Beljonne, D. & Walker, A. B. Trap limited transport in conjugated polymers. J. Phys. Chem. C 112, 11532–11538 (2008).

    Google Scholar 

  51. Livingston, R. Intermolecular transfer of electronic excitation. J. Phys. Chem. 61, 860–864 (1957).

    CAS  Google Scholar 

  52. Beddard, G. S. & Porter, G. Concentration quenching in chlorophyll. Nature 260, 366–367 (1976).

    CAS  Google Scholar 

  53. Scholes, G. D. & Ghiggino, K. P. Electronic interactions and interchromophore excitation transfer. J. Phys. Chem. 98, 4580–4590 (1994).

    CAS  Google Scholar 

  54. Samuel, I. D. W. et al. The efficiency and time-dependence of luminescence from poly(p-phenylene vinylene) and derivatives. Chem. Phys. Lett. 213, 472–478 (1993).

    CAS  Google Scholar 

  55. Brédas, J. L., Beljonne, D., Coropceanu, V. & Cornil, J. Charge-transfer and energy-transfer processes in pi-conjugated oligomers and polymers: A molecular picture. Chem. Rev. 104, 4971–5003 (2004).

    PubMed  Google Scholar 

  56. Calzaferri, G., Huber, S., Maas, H. & Minkowski, C. Host-guest antenna materials. Angew. Chem. Int. Ed. 42, 3732–3758 (2003).

    CAS  Google Scholar 

  57. Fetisova, Z. G., Freiberg, A. M. & Timpmann, K. E. Long-range molecular order as an efficient strategy for light harvesting in photosynthesis. Nature 334, 633–634 (1988).

    CAS  Google Scholar 

  58. Scholak, T., de Melo, F., Wellens, T., Mintert, F. & Buchleitner, A. Efficient and coherent excitation transfer across disordered molecular networks. Phys. Rev. E 83, 021912 (2011).

    Google Scholar 

  59. Schlau-Cohen, G. S. et al. Pathways of energy flow in LHCII from two-dimensional electronic spectroscopy. J. Phys. Chem. B 113, 15352–1536, (2009).

    CAS  PubMed  Google Scholar 

  60. Calhoun, T. R. et al. Quantum coherence enabled determination of the energy landscape in light-harvesting complex II. J. Phys. Chem. B 113, 16291–16295 (2009).

    CAS  PubMed  Google Scholar 

  61. Müh, F., Madjet, M. E. & Renger, T. Structure-based identification of energy sinks in plant light-harvesting complex II. J. Phys. Chem. B 114, 13517–13535 (2010).

    PubMed  Google Scholar 

  62. Scheuring, A. & Sturgis, J. N. Atomic force microscopy of the bacterial photosynthetic apparatus: plain pictures of an elaborate machinery Photosynth. Res. 102, 197–211 (2009).

    CAS  PubMed  Google Scholar 

  63. Bahatyrova, S. et al. The native architecture of a photosynthetic membrane. Nature 430, 1058–1062 (2004).

    CAS  PubMed  Google Scholar 

  64. Andrews, D. L. & Rodriguez, J. Resonance energy transfer: Spectral overlap, efficiency, and direction. J. Chem. Phys. 127, 084509 (2007).

    PubMed  Google Scholar 

  65. Shortreed, M. R. et al. Directed energy transfer funnels in dendrimeric antenna supermolecules. J. Phys. Chem. B 101, 6318–6322 (1997).

    Google Scholar 

  66. Balzani, V. & Scandola, F. Supramolecular Photochemistry (Ellis Horwood, 1991).

    Google Scholar 

  67. MacColl, R. Cyanobacterial phycobilisomes. J. Struct. Biol. 124, 311–334 (1998).

    CAS  PubMed  Google Scholar 

  68. Arteni, A. A., Ajlani, G. & Boekema, E. J. Structural organisation of phycobilisomes from Synechocystis sp. strain PCC6803 and their interaction with the membrane. Biochim. Biophys. Acta 1787, 272–279 (2009).

    CAS  PubMed  Google Scholar 

  69. Su, H.-N., Xie, B.-B., Zhang, X.-Y., Zhou, B.-C. & Zhang, Y.-Z. The supramolecular architecture, function, and regulation of thylakoid membranes in red algae: an overview. Photosynth. Res. 106, 73–87 (2010).

    CAS  PubMed  Google Scholar 

  70. David, L., Marx, A. & Adir, N. High-resolution crystal structures of trimeric and rod phycocyanin. J. Mol. Biol. 405, 201–213 (2011).

    CAS  PubMed  Google Scholar 

  71. Wen, J., Zhang, H., Gross, M. L. & Blankenship, R. E. Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting. Proc. Natl Acad. Sci. USA 106, 6134–6139 (2009).

    CAS  PubMed  Google Scholar 

  72. Frigaard, N. U., Chew, A. G. M., Li, H., Maresca, J. A. & Bryant, D. A. Chlorobium tepidum: insights into the structure, physiology, and metabolism of a green sulfur bacterium derived from the complete genome sequence. Photosynth. Res. 78, 93–117 (2003).

    CAS  PubMed  Google Scholar 

  73. Gantt, E., Edwards, M. R. & Provasoli, L. Chloroplast structure of cryptophyceae - evidence for phycobiliproteins within intrathylakoidal spaces. J. Cell Biol. 48, 280–290 (1971).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Fowler, G. J. S., Visschers, R. W., Grief, G. G., van Grondelle, R. & Hunter, C. N. Genetically modified photosynthetic antenna complexes with blueshifted absorbance bands. Nature 355, 848–850 (1992).

    CAS  PubMed  Google Scholar 

  75. Trissl, H.-W., Law, C. J. & Cogdell, R. J. Uphill energy transfer in LH2-containing purple bacteria at room temperature. Biochim. Biophys. Acta 1412, 149–172 (1999).

    CAS  PubMed  Google Scholar 

  76. Curutchet, C. et al. Photosynthetic light-harvesting is tuned by the heterogeneous polarizable environment of the protein. J. Am. Chem. Soc. 133, 3078–3084 (2011).

    CAS  PubMed  Google Scholar 

  77. Kasha, M. Energy transfer mechanisms and molecular exciton model for molecular aggregates. Radiation Research 20, 55–71 (1963).

    CAS  PubMed  Google Scholar 

  78. McDermott, G. et al. Crystal structure of an integral membrane light-harvesting complex from photosynthetic bacteria. Nature 374, 517–521 (1995).

    CAS  Google Scholar 

  79. Scholes, G. D., Gould, I. R., Cogdell, R. J. & Fleming, G. R. Ab initio molecular orbital calculations of electronic couplings in the LH2 bacterial light-harvesting complex of Rps. Acidophila. J. Phys. Chem. B 103, 2543–2553, (1999).

    CAS  Google Scholar 

  80. Koolhaas, M. et al. Identification of the upper exciton component of the B850 bacteriochlorophylls of the LH2 antenna complex, using a B800-free mutant of Rhodobacter sphaeroides. Biochemistry 37, 4693–4698 (1998).

    CAS  Google Scholar 

  81. Scholes, G. D., Jordanides, X. J. & Fleming, G. R. Adapting the Förster theory of energy transfer for modeling dynamics in aggregated molecular assemblies. J. Phys. Chem. B 105, 1640–1651 (2001).

    CAS  Google Scholar 

  82. Sumi, H. 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 (1999).

    CAS  Google Scholar 

  83. Sumi, H. Bacterial photosynthesis begins with quantum-mechanical coherence. Chem. Rec. 1, 480–493 (2001).

    CAS  PubMed  Google Scholar 

  84. Jang, S., Newton, M. D. & Silbey, R. J. Multichromophoric Förster resonance energy transfer from B800 to B850 in the light harvesting complex 2: Evidence for subtle energetic optimization by purple bacteria. J. Phys. Chem. B 111, 6807–6814 (2007).

    CAS  PubMed  Google Scholar 

  85. Chachisvilis, M., Kühn, O., Pullerits, T. & Sundström, V. Excitons in photosynthetic purple bacteria: Wavelike motion or incoherent hopping? J. Phys. Chem. B 101, 7275–7283 (1997).

    CAS  Google Scholar 

  86. Jimenez, R., Dikshit, S. N., Bradforth, S. E. & Fleming, G. R. Electronic excitation transfer in the LH2 complex of Rhodobacter sphaeroides. J. Phys. Chem. 100, 6825–6834 (1996).

    CAS  Google Scholar 

  87. Pullerits, T., Chachisvilis, M. & Sundström, V. Exciton delocalization length in the B850 antenna of Rhodobacter sphaeroides. J. Phys. Chem. 100, 10787–10792 (1996).

    CAS  Google Scholar 

  88. Novoderezhkin, V., Monshouwer, R. & van Grondelle, R. Exciton (de)localization in the LH2 antenna of Rhodobacter sphaeroides as revealed by relative difference absorption measurements of the LH2 antenna and the B820 subunit. J. Phys. Chem. B 103, 10540–10548 (1999).

    CAS  Google Scholar 

  89. Monshouwer, R., Abrahamsson, M., van Mourik, F. & van Grondelle, R. Superradience and exciton delocalization in bacterial photosynthetic light-harvesting systems. J. Phys. Chem. B 101, 7241–7248 (1997).

    CAS  Google Scholar 

  90. Mercer, I. P. et al. Instantaneous mapping of coherently coupled electronic transitions and energy transfers in a photosynthetic complex using angle-resolved coherent optical wave-mixing. Phys. Rev. Lett. 102, 057402 (2009).

    PubMed  Google Scholar 

  91. Melkozernov, A. N., Barber, J. & Blankenship, R. E. Light harvesting in photosystem I supercomplexes. Biochem. 45, 331–345 (2006).

    CAS  Google Scholar 

  92. Gobets, B. & van Grondelle, R. Energy transfer and trapping in photosystem I. Biochim. Biophys. Acta 1507, 80–99 (2001).

    CAS  PubMed  Google Scholar 

  93. Yang, M., Damjanovic, A., Vaswani, H. M. & Fleming, G. R. Energy transfer in photosystem I of cyanobacteria Synechococcus elongatus: Model study with structure-based semi-empirical Hamiltonian and experimental spectral density. Biophys. J. 85, 140–158 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Craig, D. P. & Walmsley, S. H. Excitons in Molecular Crystals (Benjamin, 1968).

    Google Scholar 

  95. Simpson, W. T. & Peterson, D. L. Coupling strength for resonance force transfer of electronic energy in van der Waals solids. J. Chem. Phys. 26, 588–593 (1957).

    CAS  Google Scholar 

  96. Rebentrost, P., Mohseni, M. & Aspuru-Guzik, A. Role of quantum coherence and environmental fluctuations in chromophoric energy transport. J. Phys. Chem. B 113, 9942–9947 (2009).

    CAS  PubMed  Google Scholar 

  97. Rebentrost, P., Mohseni, M., Kassal, I., S., L. & Aspuru-Guzik, A. Environment-assisted quantum transport. New J. Phys. 11, 033003 (2009).

    Google Scholar 

  98. Plenio, M. B. & Huelga, S. F. Dephasing-assisted transport: quantum networks and biomolecules. New J. Phys. 10, 113019 (2008).

    Google Scholar 

  99. Rackovsky, S. & Silbey, R. Electronic energy transfer in impure solids I. Two molecules embedded in a lattice. Mol. Phys. 25, 61–72 (1973).

    CAS  Google Scholar 

  100. Engel, G. S. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782–786 (2007).

    CAS  PubMed  Google Scholar 

  101. Collini, E. & Scholes, G. D. Coherent intrachain energy migration in a conjugated polymer at room temperature. Science 323, 369–373 (2009).

    CAS  PubMed  Google Scholar 

  102. Collini, E. et al. Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463, 644–648 (2010).

    CAS  PubMed  Google Scholar 

  103. Panitchayangkoon, G. et al. Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc. Natl Acad. Sci. USA 107, 12766–12770 (2010).

    CAS  PubMed  Google Scholar 

  104. Calhoun, T. R. & Fleming, G. R. Quantum coherence in photosynthetic complexes. Phys. Status Solidi B 248, 833–838 (2011).

    CAS  Google Scholar 

  105. Turner, D. B., Wilk, K. E., Curmi, P. M. G. & Scholes, G. D. Comparison of electronic and vibrational coherence measured by two-dimensional electronic spectroscopy. J. Phys. Chem. Lett. 2, 1904–1911 (2011).

    CAS  Google Scholar 

  106. Olaya-Castro, A., Lee, C. F., Olsen, F. F. & Johnson, N. F. Efficiency of energy transfer in a light-harvesting system under quantum coherence. Phys. Rev. B 78, 085115 (2008).

    Google Scholar 

  107. Fassioli, F., Nazir, A. & Olaya-Castro, A. Quantum state tuning of energy transfer in a correlated environment. J. Phys. Chem. Lett. 1, 2139–2143 (2010).

    CAS  Google Scholar 

  108. Kempe, J. Quantum random walks: An introductory overview. Contemp. Phys. 44, 307–327 (2003).

    Google Scholar 

  109. Agliari, E., Blumen, A. & Mülken, O. Dynamics of continuous-time random walks in restricted geometries. J. Phys. A 41, 445301–445321 (2008).

    Google Scholar 

  110. Fujii, K. & Yamamoto, K. Anti-zeno effect for quantum transport in disordered system. Phys. Rev. A 82, 042109 (2010).

    Google Scholar 

  111. Lunt, R. R., Benziger, J. B. & Forrest, S. R. Relationship between crystalline order and exciton diffusion length in molecular organic semiconductors. Adv. Mater. 22, 1233–1236 (2010).

    CAS  PubMed  Google Scholar 

  112. Lee, H., Cheng, Y.-C. & Fleming, G. R. Coherence dynamics in photosynthesis: Protein protection of excitonic coherence. Science 316, 1462–1465 (2007).

    CAS  PubMed  Google Scholar 

  113. Hossein-Nejad, H., Curutchet, C., Kubica, A. & Scholes, G. D. Delocalization-enhanced long-range energy transfer between cryptophyte algae PE545 antenna proteins. J. Phys. Chem. B 115, 5243–5253 (2011).

    CAS  PubMed  Google Scholar 

  114. Ishizaki, A. & Fleming, G. R. Unified treatment of quantum coherent and incoherent hopping dynamics in electronic energy transfer: Reduced hierarchy equation approach. J. Chem. Phys. 130, 234111 (2009).

    PubMed  Google Scholar 

  115. Yarkony, D. & Silbey, R. Comments on exciton phonon coupling - temperature-dependence. J. Chem. Phys. 65, 1042–1052 (1976).

    CAS  Google Scholar 

  116. Yarkony, D. R. & Silbey, R. Variational approach to exciton transport in molecular-crystals. J. Chem. Phys. 67, 5818–5827 (1977).

    CAS  Google Scholar 

  117. Jang, S., Cheng, Y.-C., Reichman, D. R. & Eaves, J. D. Theory of coherent resonance energy transfer. J. Chem. Phys. 129, 101104 (2008).

    PubMed  Google Scholar 

  118. Scholes, G. D. Quantum-coherent electronic energy transfer: Did nature think of it first? J. Phys. Chem. Lett. 1, 2–8 (2010).

    CAS  Google Scholar 

  119. Ishizaki, A., Calhoun, T. R., Schlau-Cohen, G. S. & Fleming, G. R. Quantum coherence and its interplay with protein environments in photosynthetic electronic energy transfer. Phys. Chem. Chem. Phys. 12, 7319–7337 (2010).

    CAS  PubMed  Google Scholar 

  120. Horton, P., Ruban, A. V. & Walters, R. G. Regulation of light harvesting in green plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 655–684 (1996).

    CAS  PubMed  Google Scholar 

  121. Demmig-Adams, B. & Adams, W. Photoprotection and other responses of plants to high light stress. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43, 599–626 (1992).

    CAS  Google Scholar 

  122. Björkman, O. & Demmig-Adams, B. in Ecophysiology of Photosynthesis (eds Schulze, E.-D. & Caldwell, M. M.) 17–57 (Springer, 1994).

    Google Scholar 

  123. Niyogi, K. Safety valves for photosynthesis. Curr. Opin. Plant Biol. 3, 455–460 (2000).

    CAS  PubMed  Google Scholar 

  124. Terazono, Y. et al. Mimicking the role of the antenna in photosynthetic photoprotection. J. Am. Chem. Soc. 133, 2916–2922 (2011).

    CAS  PubMed  Google Scholar 

  125. Peterman, E., Monshouwer, R., van Stokkum, I., van Grondelle, R. & van Amerongen, H. Ultrafast singlet excitation transfer from carotenoids to chlorophylls via different pathways in light-harvesting complex II of higher plants. Chem. Phys. Lett. 264, 279–284 (1997).

    CAS  Google Scholar 

  126. Gradinaru, C., van Stokkum, I., Pascal, A., van Grondelle, R. & van Amerongen, H. Identifying the pathways of energy transfer between carotenoids and chlorophylls in LHCII and CP29. A multi-color, femtosecond pump-probe study. J. Phys. Chem. B 104, 9330–9342 (2000).

    CAS  Google Scholar 

  127. Peterman, E., Dukker, F., van Grondelle, R. & van Amerongen, H. Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys. J. 69, 2670–2678 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Holt, N. E., Fleming, G. R. & Niyogi, K. Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43, 8281–8289 (2004).

    CAS  PubMed  Google Scholar 

  129. Niyogi, K., Björkman, O. & Grossman, A. R. The roles of specific xanthophylls in photoprotection. Proc. Natl Acad. Sci. USA 94, 14162–14167 (1997).

    CAS  PubMed  Google Scholar 

  130. Demmig-Adams, B. & Adams, W. Xanthophyll cycle and light stress in nature: uniform response to excess direct sunlight among higher plant species. Planta 198, 460–470 (1996).

    CAS  Google Scholar 

  131. Ahn, T. et al. Architecture of a charge-transfer state regulating light harvesting in a plant antenna protein. Science 320, 794–797 (2008).

    CAS  PubMed  Google Scholar 

  132. Holt, N. et al. Carotenoid cation formation and the regulation of photosynthetic light harvesting. Science 307, 433–436 (2005).

    CAS  PubMed  Google Scholar 

  133. Ruban, A. et al. Identification of a mechanism of photoprotective energy dissipation in higher plants. Nature 450, 575–578 (2007).

    CAS  PubMed  Google Scholar 

  134. Bode, S. et al. On the regulation of photosynthesis by excitonic interactions between carotenoids and chlorophylls. Proc. Natl Acad. Sci. USA 106, 12311–12316 (2009).

    CAS  PubMed  Google Scholar 

  135. Iwata, S. & Barber, J. Structure of photosystem II and molecular architecture of the oxygen-evolving centre. Curr. Opin. Struct. Biol. 14, 447–453 (2004).

    CAS  PubMed  Google Scholar 

  136. Nield, J. & Barber, J. Refinement of the structural model for the Photosystem II supercomplex of higher plants. Biochim. Biophys. Acta 1757, 353–361 (2006).

    CAS  PubMed  Google Scholar 

  137. Standfuss, J., Terwisscha van Scheltinga, A. C., Lamborghini, M. & Kühlbrandt, W. Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 Å resolution. EMBO J. 24, 919–928 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Guskov, A. et al. Cyanobacterial photosystem II at 2.9 Å resolution and the role of quinones, lipids, channels and chloride. Nature Struct. Mol. Biol. 16, 224–342 (2009).

    Google Scholar 

  139. Scheuring, S. & Sturgis, J. N. Chromatic adaptation of photsynthetic membranes. Science 309, 484–487 (2005).

    CAS  PubMed  Google Scholar 

  140. Feynman, R. P. & Hibbs, A. R. Quantum Mechanics and Path Integrals (McGraw-Hill, 1965).

    Google Scholar 

  141. Ishizaki, A. & Fleming, G. R. Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature. Proc. Natl Acad. Sci. USA 106, 17255–17260 (2009).

    PubMed  Google Scholar 

Download references

Acknowledgements

The Natural Sciences and Engineering Research Council of Canada, DARPA (QuBE), the Engineering and Physical Sciences Research Council of the United Kingdom (grant EP/G005222/1), the Netherlands Organization for Scientific Research (NWO), the European Research Council (ERC) and the Director, Office of Science, Office of Basic Energy Sciences, of the US Department of Energy under Contract DE-AC02-05CH11231 and the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the US Department of Energy through Grant DE-AC03-76SF000098 are gratefully acknowledged for support of this research.

Author information

Authors and Affiliations

  1. Department of Chemistry, University of Toronto, 80 St George Street, Toronto, M5S 3H6, Ontario, Canada

    Gregory D. Scholes

  2. Department of Chemistry, University of California, Berkeley, 94720, California, USA

    Graham R. Fleming

  3. Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, 94720, California, USA

    Graham R. Fleming

  4. Department of Physics and Astronomy, University College London, Gower Street, London, WC1E 6BT, UK

    Alexandra Olaya-Castro

  5. Department of Biophysics, Faculty of Sciences, VU University Amsterdam, De Boelelaan 1081, Amsterdam, 1081 HV, The Netherlands

    Rienk van Grondelle

Authors
  1. Gregory D. Scholes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Graham R. Fleming
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Alexandra Olaya-Castro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rienk van Grondelle
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregory D. Scholes.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scholes, G., Fleming, G., Olaya-Castro, A. et al. Lessons from nature about solar light harvesting. Nature Chem 3, 763–774 (2011). https://doi.org/10.1038/nchem.1145

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nchem.1145

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing