Photosynthetic Light Harvesting: Excitons and Coherence

Overview

Journal J R Soc Interface

Specialties Biology
Biomedical Engineering
Biophysics

Date 2013 Dec 20

PMID 24352671

Citations 59

Authors

Francesca Fassioli

Rayomond Dinshaw

Paul C Arpin

Gregory D Scholes

Affiliations

Soon will be listed here.

Abstract

Photosynthesis begins with light harvesting, where specialized pigment-protein complexes transform sunlight into electronic excitations delivered to reaction centres to initiate charge separation. There is evidence that quantum coherence between electronic excited states plays a role in energy transfer. In this review, we discuss how quantum coherence manifests in photosynthetic light harvesting and its implications. We begin by examining the concept of an exciton, an excited electronic state delocalized over several spatially separated molecules, which is the most widely available signature of quantum coherence in light harvesting. We then discuss recent results concerning the possibility that quantum coherence between electronically excited states of donors and acceptors may give rise to a quantum coherent evolution of excitations, modifying the traditional incoherent picture of energy transfer. Key to this (partially) coherent energy transfer appears to be the structure of the environment, in particular the participation of non-equilibrium vibrational modes. We discuss the open questions and controversies regarding quantum coherent energy transfer and how these can be addressed using new experimental techniques.

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References

Jang S, Newton M, Silbey R . 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. 2007; 111(24):6807-14. DOI: 10.1021/jp070111l. View

Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W . Cyanobacterial photosystem II at 2.9-A resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol. 2009; 16(3):334-42. DOI: 10.1038/nsmb.1559. View

Cho M . Coherent two-dimensional optical spectroscopy. Chem Rev. 2008; 108(4):1331-418. DOI: 10.1021/cr078377b. View

Ishizaki A, Fleming G . Unified treatment of quantum coherent and incoherent hopping dynamics in electronic energy transfer: reduced hierarchy equation approach. J Chem Phys. 2009; 130(23):234111. DOI: 10.1063/1.3155372. View

Ishizaki A, Fleming G . Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature. Proc Natl Acad Sci U S A. 2009; 106(41):17255-60. PMC: 2762676. DOI: 10.1073/pnas.0908989106. View

Marin A, Doust A, Scholes G, Wilk K, Curmi P, van Stokkum I . Flow of excitation energy in the cryptophyte light-harvesting antenna phycocyanin 645. Biophys J. 2011; 101(4):1004-13. PMC: 3175068. DOI: 10.1016/j.bpj.2011.07.012. View

Selvin P . The renaissance of fluorescence resonance energy transfer. Nat Struct Biol. 2000; 7(9):730-4. DOI: 10.1038/78948. View

Scholes G, Fleming G, Olaya-Castro A, van Grondelle R . Lessons from nature about solar light harvesting. Nat Chem. 2011; 3(10):763-74. DOI: 10.1038/nchem.1145. View

Turner D, Arpin P, McClure S, Ulness D, Scholes G . Coherent multidimensional optical spectra measured using incoherent light. Nat Commun. 2013; 4:2298. DOI: 10.1038/ncomms3298. View

10.

Nield J, Barber J . Refinement of the structural model for the Photosystem II supercomplex of higher plants. Biochim Biophys Acta. 2006; 1757(5-6):353-61. DOI: 10.1016/j.bbabio.2006.03.019. View

11.

Cogdell R, Gall A, Kohler J . The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Q Rev Biophys. 2006; 39(3):227-324. DOI: 10.1017/S0033583506004434. View

12.

Khalil M, Demirdoven N, Tokmakoff A . Obtaining absorptive line shapes in two-dimensional infrared vibrational correlation spectra. Phys Rev Lett. 2003; 90(4):047401. DOI: 10.1103/PhysRevLett.90.047401. View

13.

Hossein-Nejad H, Olaya-Castro A, Scholes G . Phonon-mediated path-interference in electronic energy transfer. J Chem Phys. 2012; 136(2):024112. DOI: 10.1063/1.3675844. View

14.

Cheng Y, Silbey R . Coherence in the B800 ring of purple bacteria LH2. Phys Rev Lett. 2006; 96(2):028103. DOI: 10.1103/PhysRevLett.96.028103. View

15.

Lee H, Cheng Y, Fleming G . Coherence dynamics in photosynthesis: protein protection of excitonic coherence. Science. 2007; 316(5830):1462-5. DOI: 10.1126/science.1142188. View

16.

Abramavicius D, Palmieri B, Voronine D, Sanda F, Mukamel S . Coherent multidimensional optical spectroscopy of excitons in molecular aggregates; quasiparticle versus supermolecule perspectives. Chem Rev. 2009; 109(6):2350-408. PMC: 2975548. DOI: 10.1021/cr800268n. View

17.

Calhoun T, Ginsberg N, Schlau-Cohen G, Cheng Y, Ballottari M, Bassi R . Quantum coherence enabled determination of the energy landscape in light-harvesting complex II. J Phys Chem B. 2009; 113(51):16291-5. DOI: 10.1021/jp908300c. View

18.

Kolli A, OReilly E, Scholes G, Olaya-Castro A . The fundamental role of quantized vibrations in coherent light harvesting by cryptophyte algae. J Chem Phys. 2012; 137(17):174109. DOI: 10.1063/1.4764100. View

19.

Read E, Schlau-Cohen G, Engel G, Georgiou T, Papiz M, Fleming G . Pigment organization and energy level structure in light-harvesting complex 4: insights from two-dimensional electronic spectroscopy. J Phys Chem B. 2009; 113(18):6495-504. DOI: 10.1021/jp809713q. View

20.

Cao J, Silbey R . Optimization of exciton trapping in energy transfer processes. J Phys Chem A. 2009; 113(50):13825-38. DOI: 10.1021/jp9032589. View