Theoretical examination of quantum coherence in a photosynthetic system at physiological temperature

The observation of long-lived electronic coherence in a photosynthetic pigment–protein complex, the Fenna–Matthews–Olson (FMO) complex, is suggestive that quantum coherence might play a significant role in achieving the remarkable efficiency of photosynthetic electronic energy transfer (EET), although the data were acquired at cryogenic temperature [Engel GS, et al. (2007) Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems. Nature 446:782–786]. In this paper, the spatial and temporal dynamics of EET through the FMO complex at physiological temperature are investigated theoretically. The numerical results reveal that quantum wave-like motion persists for several hundred femtoseconds even at physiological temperature, and suggest that the FMO complex may work as a rectifier for unidirectional energy flow from the peripheral light-harvesting antenna to the reaction center complex by taking advantage of quantum coherence and the energy landscape of pigments tuned by the protein scaffold. A potential role of quantum coherence is to overcome local energetic traps and aid efficient trapping of electronic energy by the pigments facing the reaction center complex.

[1]  Masoud Mohseni,et al.  Role of quantum coherence and environmental fluctuations in chromophoric energy transport. , 2008, The journal of physical chemistry. B.

[2]  G. Fleming,et al.  On the adequacy of the Redfield equation and related approaches to the study of quantum dynamics in electronic energy transfer. , 2009, The Journal of chemical physics.

[3]  G. Fleming,et al.  Unified treatment of quantum coherent and incoherent hopping dynamics in electronic energy transfer: reduced hierarchy equation approach. , 2009, The Journal of chemical physics.

[4]  M. Gross,et al.  Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting , 2009, Proceedings of the National Academy of Sciences.

[5]  Graham R Fleming,et al.  Dynamics of light harvesting in photosynthesis. , 2009, Annual review of physical chemistry.

[6]  G. Scholes,et al.  Electronic and vibrational coherences in resonance energy transfer along MEH-PPV chains at room temperature. , 2009, The journal of physical chemistry. A.

[7]  G. Scholes,et al.  Coherent Intrachain Energy Migration in a Conjugated Polymer at Room Temperature , 2009, Science.

[8]  Seogjoo J. Jang,et al.  Theory of coherent resonance energy transfer. , 2008, The Journal of chemical physics.

[9]  M. B. Plenio,et al.  Dephasing-assisted transport: quantum networks and biomolecules , 2008, 0807.4902.

[10]  G. Fleming,et al.  Visualization of excitonic structure in the Fenna-Matthews-Olson photosynthetic complex by polarization-dependent two-dimensional electronic spectroscopy. , 2008, Biophysical journal.

[11]  Masoud Mohseni,et al.  Environment-assisted quantum transport , 2008, 0807.0929.

[12]  M. Mohseni,et al.  Role of Quantum Coherence in Chromophoric Energy Transport , 2008, 0806.4725.

[13]  S. Lloyd,et al.  Environment-assisted quantum walks in photosynthetic energy transfer. , 2008, The Journal of chemical physics.

[14]  Graham R Fleming,et al.  Coherence quantum beats in two-dimensional electronic spectroscopy. , 2008, The journal of physical chemistry. A.

[15]  B. Rabenstein,et al.  α-Helices direct excitation energy flow in the Fenna–Matthews–Olson protein , 2007, Proceedings of the National Academy of Sciences.

[16]  Gregory S Engel,et al.  Cross-peak-specific two-dimensional electronic spectroscopy , 2007, Proceedings of the National Academy of Sciences.

[17]  Hohjai Lee,et al.  Coherence Dynamics in Photosynthesis: Protein Protection of Excitonic Coherence , 2007, Science.

[18]  T. Mančal,et al.  Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems , 2007, Nature.

[19]  T. Renger,et al.  How proteins trigger excitation energy transfer in the FMO complex of green sulfur bacteria. , 2006, Biophysical journal.

[20]  Graham R Fleming,et al.  Two-dimensional electronic spectroscopy of the B800–B820 light-harvesting complex , 2006, Proceedings of the National Academy of Sciences.

[21]  Y. Tanimura Stochastic Liouville, Langevin, Fokker–Planck, and Master Equation Approaches to Quantum Dissipative Systems , 2006 .

[22]  Andrei V. Pisliakov,et al.  Two-dimensional optical three-pulse photon echo spectroscopy. II. Signatures of coherent electronic motion and exciton population transfer in dimer two-dimensional spectra. , 2006, The Journal of chemical physics.

[23]  H. Frank,et al.  Isolation and Characterization of Carotenosomes from a Bacteriochlorophyll c-less Mutant ofChlorobium tepidum , 2005, Photosynthesis Research.

[24]  Graham R Fleming,et al.  Exciton analysis in 2D electronic spectroscopy. , 2005, The journal of physical chemistry. B.

[25]  Graham R. Fleming,et al.  Two-dimensional spectroscopy of electronic couplings in photosynthesis , 2005, Nature.

[26]  Graham R Fleming,et al.  Phase-stabilized two-dimensional electronic spectroscopy. , 2004, The Journal of chemical physics.

[27]  D. Jonas Two-dimensional femtosecond spectroscopy. , 2003, Annual review of physical chemistry.

[28]  R. Marcus,et al.  Variable-range hopping electron transfer through disordered bridge states: Application to DNA , 2003 .

[29]  Thomas Renger,et al.  On the relation of protein dynamics and exciton relaxation in pigment–protein complexes: An estimation of the spectral density and a theory for the calculation of optical spectra , 2002 .

[30]  Milosz A. Przyjalgowski,et al.  Electron-vibrational coupling in the Fenna-Matthews-Olson complex of Prosthecochloris aestuarii determined by temperature dependent absorption and fluorescence line narrowing measurements , 2000 .

[31]  J. Amesz,et al.  EXCITED STATE DYNAMICS IN FMO ANTENNA COMPLEXES FROM PHOTOSYNTHETIC GREEN SULFUR BACTERIA : A KINETIC MODEL , 1999 .

[32]  R. Louwe,et al.  Excited-State Structure and Dynamics in FMO Antenna Complexes from Photosynthetic Green Sulfur Bacteria , 1998 .

[33]  R. Agarwal,et al.  Three-Pulse Photon Echo Measurements on the Accessory Pigments in the Reaction Center of Rhodobacter sphaeroides , 1998 .

[34]  C. Francke,et al.  Isolation and pigment composition of the antenna system of four species of green sulfur bacteria , 1997, Photosynthesis Research.

[35]  S. Savikhin,et al.  Oscillating anisotropies in a bacteriochlorophyll protein: Evidence for quantum beating between exciton levels , 1997 .

[36]  Robert Eugene Blankenship,et al.  Crystal structure of the bacteriochlorophyll a protein from Chlorobium tepidum. , 1997, Journal of molecular biology.

[37]  Graham R. Fleming,et al.  CHROMOPHORE-SOLVENT DYNAMICS , 1996 .

[38]  Gert-Ludwig Ingold,et al.  Quantum Brownian motion: The functional integral approach , 1988 .

[39]  B. Matthews,et al.  Chlorophyll arrangement in a bacteriochlorophyll protein from Chlorobium limicola , 1975, Nature.

[40]  Ryogo Kubo,et al.  STOCHASTIC LIOUVILLE EQUATIONS , 1963 .

[41]  H. Frank,et al.  Isolation and characterization of carotenosomes from a bacteriochlorophyll c-less mutant of Chlorobium tepidum. , 2005, Photosynthesis research.

[42]  A. Cámara-Artigas,et al.  The structure of the FMO protein from Chlorobium tepidum at 2.2 Å resolution , 2004, Photosynthesis Research.

[43]  Robert Eugene Blankenship Molecular mechanisms of photosynthesis , 2002 .

[44]  S. Rackovsky,et al.  Electronic energy transfer in impure solids , 1973 .

[45]  Th. Förster Zwischenmolekulare Energiewanderung und Fluoreszenz , 1948 .

[46]  G.,et al.  On the Theory of Relaxation Processes * , 2022 .