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:

Quantum design of photosynthesis for bio-inspired solar-energy conversion

Abstract

Photosynthesis is the natural process that converts solar photons into energy-rich products that are needed to drive the biochemistry of life. Two ultrafast processes form the basis of photosynthesis: excitation energy transfer and charge separation. Under optimal conditions, every photon that is absorbed is used by the photosynthetic organism. Fundamental quantum mechanics phenomena, including delocalization, underlie the speed, efficiency and directionality of the charge-separation process. At least four design principles are active in natural photosynthesis, and these can be applied practically to stimulate the development of bio-inspired, human-made energy conversion systems.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Absorption spectra and X-ray structure of the bacterial reaction centre and the PSII reaction centre.
Figure 2: Resonant vibrations promote effective charge separation.

Similar content being viewed by others

References

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

    Google Scholar 

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

    ADS  CAS  Google Scholar 

  3. Myers, J. A. The 1932 experiments. Photosynth. Res. 40, 303–310 (1994).

    ADS  CAS  PubMed  Google Scholar 

  4. van Grondelle, R. & van Gorkom, H. The birth of the photosynthetic reaction center: the story of Lou Duysens. Photosynth. Res. 120, 3–7 (2014).

    CAS  PubMed  Google Scholar 

  5. Deisenhofer, J., Epp, O., Miki, K., Huber, R. & Michel, H. X-ray structure-analysis of a membrane-protein complex: electron-density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis . J. Mol. Biol. 180, 385–398 (1984).

    CAS  PubMed  Google Scholar 

  6. Koepke, J. et al. pH modulates the quinone position in the photosynthetic reaction center from Rhodobacter sphaeroides in the neutral and charge separated states. J. Mol. Biol. 371, 396–409 (2007).

    CAS  PubMed  Google Scholar 

  7. Zouni, A. et al. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409, 739–743 (2001).

    ADS  CAS  PubMed  Google Scholar 

  8. Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838 (2004).

    ADS  CAS  PubMed  Google Scholar 

  9. Umena, Y., Kawakami, K., Shen, J.-R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 55–60 (2011). This paper presents the crystal structure of PSII at atomic resolution.

    ADS  CAS  Google Scholar 

  10. Scholes, G. D., Fleming, G. R., Olaya-Castro, A. & van Grondelle, R. Lessons from nature about solar light harvesting. Nature Chem. 3, 763–774 (2011).

    ADS  CAS  Google Scholar 

  11. van Amerongen, H., Valkunas, L. & van Grondelle, R. Photosynthetic Excitons (World Scientific, 2000). This book proposes the concept of the disordered photosynthetic exciton model.

    Google Scholar 

  12. Frenkel, J. On the transformation of light into heat in solids. I. Phys. Rev. 37, 17–44 (1931).

    ADS  CAS  MATH  Google Scholar 

  13. Durrant, J. R. et al. Subpicosecond equilibration of excitation energy in isolated photosystem II reaction centers. Proc. Natl Acad. Sci. USA 89, 11632–11636 (1992).

    ADS  CAS  PubMed  Google Scholar 

  14. Zinth, W. & Wachtveitl, J. The first picoseconds in bacterial photosynthesis: ultrafast electron transfer for the efficient conversion of light energy. ChemPhysChem 6, 871–880 (2005).

    CAS  PubMed  Google Scholar 

  15. Rappaport, F. & Diner, B. A. Primary photochemistry and energetics leading to the oxidation of the (Mn)4Ca cluster and to the evolution of molecular oxygen in photosystem II. Coord. Chem. Rev. 252, 259–272 (2008).

    CAS  Google Scholar 

  16. Croce, R. & van Amerongen, H. Light-harvesting and structural organization of photosystem II: from individual complexes to thylakoid membrane. J. Photochem. Photobiol. B 104, 142–153 (2011).

    CAS  PubMed  Google Scholar 

  17. Rutherford, A. W., Osyczka, A. & Rappaport, F. Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2 . FEBS Lett. 586, 603–616 (2012).

    CAS  PubMed  Google Scholar 

  18. Steffen, M. A., Lao, K. & Boxer, S. G. Dielectric asymmetry in the photosynthetic reaction center. Science 264, 810–816 (1994).

    ADS  CAS  PubMed  Google Scholar 

  19. Amesz, J. & Hoff, A. J. Biophysical Techniques in Photosynthesis Vol. 3 (Kluwer Academic, 1996).

    Google Scholar 

  20. Berera, R., Van Grondelle, R. & Kennis, J. T. M. Ultrafast transient absorption spectroscopy: principles and application to photosynthetic systems. Photosynth. Res. 101, 105–118 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Schlau-Cohen, G. S., Dawlaty, J. M. & Fleming, G. R. Ultrafast multidimensional spectroscopy: principles and applications to photosynthetic systems. IEEE J. Sel. Top. Quantum Electron. 18, 283–295 (2012).

    ADS  CAS  Google Scholar 

  22. Shkuropatov, A. Y. et al. Reaction centers of photosystem II with a chemically-modified pigment composition: exchange of pheophytins with 131-deoxo-131-hydroxy-pheophytin a . FEBS Lett. 450, 163–167 (1999).

    CAS  PubMed  Google Scholar 

  23. Vacha, F. et al. Photochemistry and spectroscopy of a five-chlorophyll reaction center of photosystem II isolated by using a Cu affinity column. Proc. Natl Acad. Sci. USA 92, 2929–2933 (1995).

    ADS  CAS  PubMed  Google Scholar 

  24. Diner, B. A. et al. Site-directed mutations at D1-His198 and D2-His197 of photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation triplet stabilization. Biochemistry 40, 9265–9281 (2001).

    CAS  PubMed  Google Scholar 

  25. Zhang, W. M., Meier, T., Chernyak, V. & Mukamel, S. Exciton migration and three-pulse femtosecond optical spectroscopies of photosynthetic antenna complexes. J. Chem. Phys. 108, 7763–7774 (1998).

    ADS  CAS  Google Scholar 

  26. Raszewski, G., Diner, B. A., Schlodder, E. & Renger, T. Spectroscopic properties of reaction center pigments in photosystem II core complexes: revision of the multimer model. Biophys. J. 95, 105–119 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Allen, J. P. & Williams, J. C. in The Biophysics of Photosynthesis (eds Golbeck, J. H. & van der Est, A.) 275–295 (Springer, 2014).

    Google Scholar 

  28. Wydrzynski, T. J. & Satoh, K. Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Springer, 2005).

    Google Scholar 

  29. Allen, J. P. et al. Effects of hydrogen bonding to a bacteriochlorophyll–bacteriopheophytin dimer in reaction centers from Rhodobacter sphaeroides . Biochemistry 35, 6612–6619 (1996).

    CAS  PubMed  Google Scholar 

  30. Romero, E., Novoderezhkin, V. I. & van Grondelle, R. in Quantum Effects in Biology (eds Mohseni, M., Omar, Y., Engel, G. S. & Plenio, M. B.) 179–197 (Cambridge Univ. Press, 2014).

    Google Scholar 

  31. van Brederode, M. E., Jones, M. R., van Mourik, F., van Stokkum, I. H. M. & van Grondelle, R. A new pathway for transmembrane electron transfer in photosynthetic reaction centers of Rhodobacter sphaeroides not involving the excited special pair. Biochemistry 36, 6855–6861 (1997). This paper reveals the discovery of multiple pathways for charge separation in the bacterial reaction centre.

    CAS  PubMed  Google Scholar 

  32. Vos, M. H., Rappaport, F., Lambry, J.-C., Breton, J. & Martin, J.-L. Visualization of coherent nuclear motion in a membrane protein by femtosecond spectroscopy. Nature 363, 320–325 (1993). This paper shows that vibrational wave packets form in bacterial reaction centres after they are excitated with a femtosecond laser pulse.

    ADS  CAS  Google Scholar 

  33. Yakovlev, A. G., Shkuropatov, A. Y. & Shuvalov, V. A. Nuclear wave packet motion between P* and P+BA potential surfaces with a subsequent electron transfer to HA in bacterial reaction centers at 90 K. Electron transfer pathway. Biochemistry 41, 14019–14027 (2002).

    CAS  PubMed  Google Scholar 

  34. Novoderezhkin, V. I., Yakovlev, A. G., Van Grondelle, R. & Shuvalov, V. A. Coherent nuclear and electronic dynamics in primary charge separation in photosynthetic reaction centers: a Redfield theory approach. J. Phys. Chem. B 108, 7445–7457 (2004). This article describes coherent vibrational and electronic dynamics during charge separation in bacterial reaction centers.

    CAS  Google Scholar 

  35. Danielius, R. V. et al. The primary reaction of photosystem II in the D1–D2–cytochrome b-559 complex. FEBS Lett. 213, 241–244 (1987).

    CAS  Google Scholar 

  36. Bosch, M. K., Proskuryakov, I. I., Gast, P. & Hoff, A. J. Relative orientation of the optical transition dipole and triplet axes of the photosystem II primary donor. A magnetophoto-selection study. J. Phys. Chem. 99, 15310–15316 (1995).

    CAS  Google Scholar 

  37. Konermann, L. & Holzwarth, A. R. Analysis of the absorption spectrum of photosystem II reaction centers: temperature dependence, pigment assignment and inhomogeneous broadening. Biochemistry 35, 829–842 (1996).

    CAS  PubMed  Google Scholar 

  38. Tetenkin, V. L., Gulyaev, B. A., Seibert, M. & Rubin, A. B. Spectral properties of stabilized D1/D2/cytochrome b-559 photosystem II reaction center complex. FEBS Lett. 250, 459–463 (1989).

    CAS  Google Scholar 

  39. Durrant, J. R. et al. A multimer model for P680, the primary electron donor of photosystem II. Proc. Natl Acad. Sci. USA 92, 4798–4802 (1995). This paper proposes the original multimer model for the PSII reaction centre.

    ADS  CAS  PubMed  Google Scholar 

  40. Peterman, E. J. G., van Amerongen, H., van Grondelle, R. & Dekker, J. P. The nature of the excited state of the reaction center of photosystem II of green plants: a high-resolution fluorescence spectroscopy study. Proc. Natl Acad. Sci. USA 95, 6128–6133 (1998).

    ADS  CAS  PubMed  Google Scholar 

  41. Renger, T. & Marcus, R. A. Photophysical properties of PS-2 reaction centers and a discrepancy in exciton relaxation times. J. Phys. Chem. B 106, 1809–1819 (2002).

    CAS  Google Scholar 

  42. Dekker, J. P. & van Grondelle, R. Primary charge separation in photosystem II. Photosynth. Res. 63, 195–208 (2000).

    CAS  PubMed  Google Scholar 

  43. Prokhorenko, V. I. & Holzwarth, A. R. Primary processes and structure of the photosystem II reaction center: a photon echo study. J. Phys. Chem. B 104, 11563–11578 (2000).

    CAS  Google Scholar 

  44. Raszewski, G., Saenger, W. & Renger, T. Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor. Biophys. J. 88, 986–998 (2005).

    CAS  PubMed  Google Scholar 

  45. Groot, M. L. et al. Initial electron donor and acceptor in isolated photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc. Natl Acad. Sci. USA 102, 13087–13092 (2005).

    ADS  CAS  PubMed  Google Scholar 

  46. Holzwarth, A. R. et al. Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc. Natl Acad. Sci. USA 103, 6895–6900 (2006).

    ADS  CAS  PubMed  Google Scholar 

  47. Novoderezhkin, V. I., Andrizhiyevskaya, E. G., Dekker, J. P. & van Grondelle, R. Pathways and timescales of primary charge separation in the photosystem II reaction center as revealed by simultaneous fit of time-resolved fluorescence and transient absorption. Biophys. J. 89, 1464–1481 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Novoderezhkin, V. I., Dekker, J. P. & van Grondelle, R. Mixing of exciton and charge-transfer states in photosystem II reaction centers: modeling of Stark spectra with modified Redfield theory. Biophys. J. 93, 1293–1311 (2007).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  49. Romero, E., van Stokkum, I. H. M., Novoderezhkin, V. I., Dekker, J. P. & van Grondelle, R. Two different charge separation pathways in photosystem II. Biochemistry 49, 4300–4307 (2010). This article reveals the discovery of two pathways for charge separation in the PSII reaction centre.

    CAS  PubMed  Google Scholar 

  50. Novoderezhkin, V. I., Romero, E., Dekker, J. P. & van Grondelle, R. Multiple charge separation pathways in photosystem II: modeling of transient absorption kinetics. ChemPhysChem 12, 681–688 (2011).

    CAS  PubMed  Google Scholar 

  51. van Stokkum, I. H. M., Larsen, D. S. & van Grondelle, R. Global and target analysis of time-resolved spectra. Biochim. Biophys. Acta 1657, 82–104 (2004).

    CAS  PubMed  Google Scholar 

  52. Romero, E. et al. Mixed exciton-charge-transfer states in photosystem II: Stark spectroscopy on site-directed mutants. Biophys. J. 103, 185–194 (2012).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  53. Reimers, J. R. et al. Challenges facing an understanding of the nature of low-energy excited states in photosynthesis. Biochim. Biophys. Acta 1857, 1627–1640 (2016).

    CAS  PubMed  Google Scholar 

  54. Savikhin, S., Buck, D. R. & Struve, W. S. Oscillating anisotropies in a bacteriochlorophyll protein: evidence for quantum beating between exciton levels. Chem. Phys. 223, 303–312 (1997).

    CAS  Google Scholar 

  55. Brixner, T. et al. Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434, 625–628 (2005).

    ADS  CAS  PubMed  Google Scholar 

  56. Zigmantas, D. et al. Two-dimensional electronic spectroscopy of the B800–B820 light-harvesting complex. Proc. Natl Acad. Sci. USA 103, 12672–12677 (2006).

    ADS  CAS  PubMed  Google Scholar 

  57. Engel, G. S. et al. Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446, 782–786 (2007). This paper presents the first observation of quantum dynamics in photosynthesis.

    ADS  CAS  PubMed  Google Scholar 

  58. 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 

  59. Collini, E. et al. Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463, 644–647 (2010).

    ADS  CAS  PubMed  Google Scholar 

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

    ADS  CAS  PubMed  Google Scholar 

  61. Schlau-Cohen, G. S. et al. Elucidation of the timescales and origins of quantum electronic coherence in LHCII. Nature Chem. 4, 389–395 (2012).

    ADS  CAS  Google Scholar 

  62. Hildner, R., Brinks, D., Nieder, J. B., Cogdell, R. J. & van Hulst, N. F. Quantum coherent energy transfer over varying pathways in single light-harvesting complexes. Science 340, 1448–1451 (2013).

    ADS  CAS  PubMed  Google Scholar 

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

    ADS  CAS  PubMed  Google Scholar 

  64. Westenhoff, S., Palecek, D., Edlund, P., Smith, P. & Zigmantas, D. Coherent picosecond exciton dynamics in a photosynthetic reaction center. J. Am. Chem. Soc. 134, 16484–16487 (2012).

    CAS  PubMed  Google Scholar 

  65. Collini, E. Spectroscopic signatures of quantum-coherent energy transfer. Chem. Soc. Rev. 42, 4932–4947 (2013).

    CAS  PubMed  Google Scholar 

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

    ADS  CAS  PubMed  Google Scholar 

  67. Prior, J., Chin, A. W., Huelga, S. F. & Plenio, M. B. Efficient simulation of strong system-environment interactions. Phys. Rev. Lett. 105, 050404 (2010).

    ADS  PubMed  Google Scholar 

  68. Womick, J. M. & Moran, A. M. Vibronic enhancement of exciton sizes and energy transport in photosynthetic complexes. J. Phys. Chem. B 115, 1347–1356 (2011).

    CAS  PubMed  Google Scholar 

  69. Kolli, A., Nazir, A. & Olaya-Castro, A. Electronic excitation dynamics in multichromophoric systems described via a polaron-representation master equation. J. Chem. Phys. 135, 154112 (2011).

    ADS  PubMed  Google Scholar 

  70. Christensson, N., Kauffmann, H. F., Pullerits, T. & Mancal, T. Origin of long-lived coherences in light-harvesting complexes. J. Phys. Chem. B 116, 7449–7454 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Chin, A. W., Huelga, S. F. & Plenio, M. B. Coherence and decoherence in biological systems: principles of noise-assisted transport and the origin of long-lived coherences. Phil. Trans. R. Soc. A 370, 3638–3657 (2012).

    ADS  MathSciNet  CAS  PubMed  Google Scholar 

  72. Kolli, A., O'Reilly, E. J., Scholes, G. D. & Olaya-Castro, A. The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae. J. Chem. Phys. 137, 174109 (2012). This article demonstrates the role of discrete and quantized vibrations in photosynthetic light harvesting.

    ADS  PubMed  Google Scholar 

  73. Butkus, V., Zigmantas, D., Valkunas, L. & Abramavicius, D. Vibrational vs. electronic coherences in 2D spectrum of molecular systems. Chem. Phys. Lett. 545, 40–43 (2012).

    ADS  CAS  Google Scholar 

  74. Chin, A. W. et al. The role of non-equilibrium vibrational structures in electronic coherence and recoherence in pigment-protein complexes. Nature Phys. 9, 113–118 (2013).

    ADS  CAS  Google Scholar 

  75. Tiwari, V., Peters, W. K. & Jonas, D. M. Electronic resonance with anticorrelated pigment vibrations drives photosynthetic energy transfer outside the adiabatic framework. Proc. Natl Acad. Sci. USA 110, 1203–1208 (2013).

    ADS  CAS  PubMed  Google Scholar 

  76. O'Reilly, E. J. & Olaya-Castro, A. Non-classicality of the molecular vibrations assisting exciton energy transfer at room temperature. Nature Commun. 5, 3012 (2014).

    ADS  Google Scholar 

  77. Romero, E. et al. Quantum coherence in photosynthesis for efficient solar-energy conversion. Nature Phys. 10, 676–682 (2014). This paper presents the discovery of quantum coherence in charge separation in the PSII reaction centre and is the first to correlate coherence with the efficiency of charge separation.

    ADS  CAS  Google Scholar 

  78. Novoderezhkin, V. I., Romero, E. & van Grondelle, R. How exciton-vibrational coherences control charge separation in the photosystem II reaction center. Phys. Chem. Chem. Phys. 17, 30828–30841 (2015).

    CAS  PubMed  Google Scholar 

  79. Novoderezhkin, V. I., Romero, E., Prior, J. & van Grondelle, R. Exciton-vibrational resonance and dynamics of charge separation in the photosystem II reaction center. Phys. Chem. Chem. Phys. 19, 5195–5208 (2017).

    CAS  PubMed  Google Scholar 

  80. Fuller, F. D. et al. Vibronic coherence in oxygenic photosynthesis. Nature Chem. 6, 706–711 (2014).

    ADS  CAS  Google Scholar 

  81. Novoderezhkin, V. I. & 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 

  82. Reimers, J. R. et al. Assignment of the Q-bands of the chlorophylls: coherence loss via Q x –Q y mixing. Sci. Rep. 3, 2761 (2013).

    PubMed  PubMed Central  Google Scholar 

  83. 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).

    ADS  PubMed  Google Scholar 

  84. O'Regan, B. & Gratzel, M. A low-cost, high-efficiency solar cell based on dye-sensitized colloidal TiO2 films. Nature 353, 737–740 (1991).

    ADS  CAS  Google Scholar 

  85. Hagfeldt, A., Boschloo, G., Sun, L., Kloo, L. & Pettersson, H. Dye-sensitized solar cells. Chem. Rev. 110, 6595–6663 (2010).

    CAS  PubMed  Google Scholar 

  86. Polman, A., Knight, M., Garnett, E. C., Ehrler, B. & Sinke, W. C. Photovoltaic materials: present efficiencies and future challenges. Science 352, aad4424 (2016).

    PubMed  Google Scholar 

  87. Liu, C., Colón, B. C., Ziesack, M., Silver, P. A. & Nocera, D. G. Water splitting-biosynthetic system with CO2 reduction efficiencies exceeding photosynthesis. Science 352, 1210–1213 (2016).

    ADS  CAS  PubMed  Google Scholar 

  88. Bredas, J.-L., Sargent, E. H. & Scholes, G. D. Photovoltaic concepts inspired by coherence effects in photosynthetic systems. Nature Mater. 16, 35–44 (2017).

    ADS  CAS  Google Scholar 

  89. Bakulin, A. A. et al. The role of driving energy and delocalized states for charge separation in organic semiconductors. Science 335, 1340–1344 (2012).

    ADS  CAS  PubMed  Google Scholar 

  90. Falke, S. M. et al. Coherent ultrafast charge transfer in an organic photovoltaic blend. Science 344, 1001–1005 (2014).

    ADS  CAS  PubMed  Google Scholar 

  91. De Sio, A. et al. Tracking the coherent generation of polaron pairs in conjugated polymers. Nature Commun. 7, 13742 (2016).

    ADS  Google Scholar 

  92. Ramamurthy, V. & Inoue, Y. Supramolecular Photochemistry: Controlling Photochemical Processes (Wiley, 2011).

    Google Scholar 

  93. Ajayaghosh, A., Praveen, V. K. & Vijayakumar, C. Organogels as scaffolds for excitation energy transfer and light harvesting. Chem. Soc. Rev. 37, 109–122 (2008).

    CAS  PubMed  Google Scholar 

  94. Pinheiro, A. V., Han, D., Shih, W. M. & Yan, H. Challenges and opportunities for structural DNA nanotechnology. Nature Nanotechnol. 6, 763–772 (2011).

    ADS  CAS  Google Scholar 

  95. Moser, C. C. et al. in Methods in Enzymology Vol. 580 (ed. Pecoraro, V. L.) 365–388 (Academic, 2016).

    Google Scholar 

  96. Zhang, J. Z. et al. Competing charge transfer pathways at the photosystem II–electrode interface. Nature Chem. Biol. 12, 1046–1052 (2016).

    CAS  Google Scholar 

  97. Ringsmuth, A. K., Landsberg, M. J. & Hankamer, B. Can photosynthesis enable a global transition from fossil fuels to solar fuels, to mitigate climate change and fuel-supply limitations? Renew. Sustain. Energy Rev. 62, 134–163 (2016).

    CAS  Google Scholar 

  98. Flanagan, M. L. et al. Mutations to R. sphaeroides reaction center perturb energy levels and vibronic coupling but not observed energy transfer rates. J. Phys. Chem. A 120, 1479–1487 (2016).

    CAS  PubMed  Google Scholar 

  99. Dahlberg, P. D. et al. Coherences observed in vivo in photosynthetic bacteria using two-dimensional electronic spectroscopy. J. Chem. Phys. 143, 101101 (2015).

    ADS  PubMed  PubMed Central  Google Scholar 

  100. Dostál, J., Pšenčík, J. & Zigmantas, D. In situ mapping of the energy flow through the entire photosynthetic apparatus. Nature Chem. 8, 705–710 (2016).

    ADS  Google Scholar 

Download references

Acknowledgements

E.R. and R.v.G. were supported by: the VU University Amsterdam; the Laserlab-Europe consortium; TOP grant 700.58.305 from the Foundation of Chemical Sciences, part of Netherlands Organisation for Scientific Research (NWO); European Research Council Advanced Grant 267333 (PHOTPROT); and the European Union FP7 project PAPETS (grant agreement 323901). R.v.G. gratefully acknowledges his Academy Professorship from the Netherlands Royal Academy of Sciences and was also supported by the Canadian Institute for Advanced Research. V.I.N. was supported by the Russian Foundation for Basic Research (grant number 15-04-02136) and by an NWO visitor grant.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Elisabet Romero.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Reprints and permissions information is available at www.nature.com/reprints.

Reviewer Information Nature thanks J. Minagawa and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Romero, E., Novoderezhkin, V. & van Grondelle, R. Quantum design of photosynthesis for bio-inspired solar-energy conversion. Nature 543, 355–365 (2017). https://doi.org/10.1038/nature22012

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature22012

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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