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.
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Blankenship, R. E. Molecular Mechanisms of Photosynthesis (Blackwell Science, 2002).
Beddard, G. S. & Porter, G. Concentration quenching in chlorophyll. Nature 260, 366–367 (1976).
Myers, J. A. The 1932 experiments. Photosynth. Res. 40, 303–310 (1994).
van Grondelle, R. & van Gorkom, H. The birth of the photosynthetic reaction center: the story of Lou Duysens. Photosynth. Res. 120, 3–7 (2014).
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).
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).
Zouni, A. et al. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409, 739–743 (2001).
Ferreira, K. N., Iverson, T. M., Maghlaoui, K., Barber, J. & Iwata, S. Architecture of the photosynthetic oxygen-evolving center. Science 303, 1831–1838 (2004).
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.
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).
van Amerongen, H., Valkunas, L. & van Grondelle, R. Photosynthetic Excitons (World Scientific, 2000). This book proposes the concept of the disordered photosynthetic exciton model.
Frenkel, J. On the transformation of light into heat in solids. I. Phys. Rev. 37, 17–44 (1931).
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).
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).
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).
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).
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).
Steffen, M. A., Lao, K. & Boxer, S. G. Dielectric asymmetry in the photosynthetic reaction center. Science 264, 810–816 (1994).
Amesz, J. & Hoff, A. J. Biophysical Techniques in Photosynthesis Vol. 3 (Kluwer Academic, 1996).
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).
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).
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).
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).
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).
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).
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).
Allen, J. P. & Williams, J. C. in The Biophysics of Photosynthesis (eds Golbeck, J. H. & van der Est, A.) 275–295 (Springer, 2014).
Wydrzynski, T. J. & Satoh, K. Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase (Springer, 2005).
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).
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).
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.
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.
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).
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.
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).
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).
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).
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).
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.
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).
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).
Dekker, J. P. & van Grondelle, R. Primary charge separation in photosystem II. Photosynth. Res. 63, 195–208 (2000).
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).
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).
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).
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).
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).
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).
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.
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).
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).
Romero, E. et al. Mixed exciton-charge-transfer states in photosystem II: Stark spectroscopy on site-directed mutants. Biophys. J. 103, 185–194 (2012).
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).
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).
Brixner, T. et al. Two-dimensional spectroscopy of electronic couplings in photosynthesis. Nature 434, 625–628 (2005).
Zigmantas, D. et al. Two-dimensional electronic spectroscopy of the B800–B820 light-harvesting complex. Proc. Natl Acad. Sci. USA 103, 12672–12677 (2006).
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.
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).
Collini, E. et al. Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature. Nature 463, 644–647 (2010).
Panitchayangkoon, G. et al. Long-lived quantum coherence in photosynthetic complexes at physiological temperature. Proc. Natl Acad. Sci. USA 107, 12766–12770 (2010).
Schlau-Cohen, G. S. et al. Elucidation of the timescales and origins of quantum electronic coherence in LHCII. Nature Chem. 4, 389–395 (2012).
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).
Lee, H., Cheng, Y. C. & Fleming, G. R. Coherence dynamics in photosynthesis: protein protection of excitonic coherence. Science 316, 1462–1465 (2007).
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).
Collini, E. Spectroscopic signatures of quantum-coherent energy transfer. Chem. Soc. Rev. 42, 4932–4947 (2013).
Cheng, Y. C. & Fleming, G. R. Dynamics of light harvesting in photosynthesis. Annu. Rev. Phys. Chem. 60, 241–262 (2009).
Prior, J., Chin, A. W., Huelga, S. F. & Plenio, M. B. Efficient simulation of strong system-environment interactions. Phys. Rev. Lett. 105, 050404 (2010).
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).
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).
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).
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).
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.
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).
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).
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).
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).
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.
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).
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).
Fuller, F. D. et al. Vibronic coherence in oxygenic photosynthesis. Nature Chem. 6, 706–711 (2014).
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).
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).
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).
O'Regan, B. & Gratzel, M. A low-cost, high-efficiency solar cell based on dye-sensitized colloidal TiO2 films. Nature 353, 737–740 (1991).
Hagfeldt, A., Boschloo, G., Sun, L., Kloo, L. & Pettersson, H. Dye-sensitized solar cells. Chem. Rev. 110, 6595–6663 (2010).
Polman, A., Knight, M., Garnett, E. C., Ehrler, B. & Sinke, W. C. Photovoltaic materials: present efficiencies and future challenges. Science 352, aad4424 (2016).
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).
Bredas, J.-L., Sargent, E. H. & Scholes, G. D. Photovoltaic concepts inspired by coherence effects in photosynthetic systems. Nature Mater. 16, 35–44 (2017).
Bakulin, A. A. et al. The role of driving energy and delocalized states for charge separation in organic semiconductors. Science 335, 1340–1344 (2012).
Falke, S. M. et al. Coherent ultrafast charge transfer in an organic photovoltaic blend. Science 344, 1001–1005 (2014).
De Sio, A. et al. Tracking the coherent generation of polaron pairs in conjugated polymers. Nature Commun. 7, 13742 (2016).
Ramamurthy, V. & Inoue, Y. Supramolecular Photochemistry: Controlling Photochemical Processes (Wiley, 2011).
Ajayaghosh, A., Praveen, V. K. & Vijayakumar, C. Organogels as scaffolds for excitation energy transfer and light harvesting. Chem. Soc. Rev. 37, 109–122 (2008).
Pinheiro, A. V., Han, D., Shih, W. M. & Yan, H. Challenges and opportunities for structural DNA nanotechnology. Nature Nanotechnol. 6, 763–772 (2011).
Moser, C. C. et al. in Methods in Enzymology Vol. 580 (ed. Pecoraro, V. L.) 365–388 (Academic, 2016).
Zhang, J. Z. et al. Competing charge transfer pathways at the photosystem II–electrode interface. Nature Chem. Biol. 12, 1046–1052 (2016).
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).
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).
Dahlberg, P. D. et al. Coherences observed in vivo in photosynthetic bacteria using two-dimensional electronic spectroscopy. J. Chem. Phys. 143, 101101 (2015).
Dostál, J., Pšenčík, J. & Zigmantas, D. In situ mapping of the energy flow through the entire photosynthetic apparatus. Nature Chem. 8, 705–710 (2016).
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.
The authors declare no competing financial interests.
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Reviewer Information Nature thanks J. Minagawa and the other anonymous reviewer(s) for their contribution to the peer review of this work.
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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
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