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Title: Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo

Abstract

In photosynthetic organisms, the pigment-protein complexes that comprise the light-harvesting antenna exhibit complex electronic structures and ultrafast dynamics due to the coupling among the chromophores. In this work, we present absorptive two-dimensional (2D) electronic spectra from living cultures of the purple bacterium, Rhodobacter sphaeroides, acquired using gradient assisted photon echo spectroscopy. Diagonal slices through the 2D lineshape of the LH1 stimulated emission/ground state bleach feature reveal a resolvable higher energy population within the B875 manifold. The waiting time evolution of diagonal, horizontal, and vertical slices through the 2D lineshape shows a sub-100 fs intra-complex relaxation as this higher energy population red shifts. The absorption (855 nm) of this higher lying sub-population of B875 before it has red shifted optimizes spectral overlap between the LH1 B875 band and the B850 band of LH2. Access to an energetically broad distribution of excitonic states within B875 offers a mechanism for efficient energy transfer from LH2 to LH1 during photosynthesis while limiting back transfer. Two-dimensional lineshapes reveal a rapid decay in the ground-state bleach/stimulated emission of B875. This signal, identified as a decrease in the dipole strength of a strong transition in LH1 on the red side of the B875 band, is assigned tomore » the rapid localization of an initially delocalized exciton state, a dephasing process that frustrates back transfer from LH1 to LH2.« less

Authors:
 [1];  [2]; ORCiD logo [1]; ORCiD logo [1];  [1];  [3];  [3]; ORCiD logo [1]
  1. Univ. of Chicago, IL (United States). Dept. of Chemistry, Inst. for Biophysical Dynamics, and The James Franck Inst.
  2. Univ. of Chicago, IL (United States). Graduate Program in the Biophysical Sciences, Inst. for Biophysical Dynamics, and The James Franck Inst.
  3. Univ. of Sheffield (United Kingdom). Dept. of Molecular Biology and Biotechnology
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1469878
Alternate Identifier(s):
OSTI ID: 1396635
Grant/Contract Number:  
SC0001035; SC 0001035
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Journal of Chemical Physics
Additional Journal Information:
Journal Volume: 147; Journal Issue: 13; Related Information: PARC partners with Washington University in St. Louis (lead); University of California, Riverside; University of Glasgow, UK; Los Alamos National Laboratory; University of New Mexico; New Mexico Corsortium; North Carolina State University; Northwestern University; Oak Ridge National Laboratory; University of Pennsylvania; Sandia National Laboratories; University of Sheffield, UK; Journal ID: ISSN 0021-9606
Publisher:
American Institute of Physics (AIP)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 14 SOLAR ENERGY; solar (fuels); photosynthesis (natural and artificial); biofuels (including algae and biomass); bio-inspired; charge transport; membrane; synthesis (novel materials); synthesis (self-assembly)

Citation Formats

Sohail, Sara H., Dahlberg, Peter D., Allodi, Marco A., Massey, Sara C., Ting, Po-Chieh, Martin, Elizabeth C., Hunter, C. Neil, and Engel, Gregory S. Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo. United States: N. p., 2017. Web. doi:10.1063/1.4999057.
Sohail, Sara H., Dahlberg, Peter D., Allodi, Marco A., Massey, Sara C., Ting, Po-Chieh, Martin, Elizabeth C., Hunter, C. Neil, & Engel, Gregory S. Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo. United States. https://doi.org/10.1063/1.4999057
Sohail, Sara H., Dahlberg, Peter D., Allodi, Marco A., Massey, Sara C., Ting, Po-Chieh, Martin, Elizabeth C., Hunter, C. Neil, and Engel, Gregory S. Wed . "Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo". United States. https://doi.org/10.1063/1.4999057. https://www.osti.gov/servlets/purl/1469878.
@article{osti_1469878,
title = {Communication: Broad manifold of excitonic states in light-harvesting complex 1 promotes efficient unidirectional energy transfer in vivo},
author = {Sohail, Sara H. and Dahlberg, Peter D. and Allodi, Marco A. and Massey, Sara C. and Ting, Po-Chieh and Martin, Elizabeth C. and Hunter, C. Neil and Engel, Gregory S.},
abstractNote = {In photosynthetic organisms, the pigment-protein complexes that comprise the light-harvesting antenna exhibit complex electronic structures and ultrafast dynamics due to the coupling among the chromophores. In this work, we present absorptive two-dimensional (2D) electronic spectra from living cultures of the purple bacterium, Rhodobacter sphaeroides, acquired using gradient assisted photon echo spectroscopy. Diagonal slices through the 2D lineshape of the LH1 stimulated emission/ground state bleach feature reveal a resolvable higher energy population within the B875 manifold. The waiting time evolution of diagonal, horizontal, and vertical slices through the 2D lineshape shows a sub-100 fs intra-complex relaxation as this higher energy population red shifts. The absorption (855 nm) of this higher lying sub-population of B875 before it has red shifted optimizes spectral overlap between the LH1 B875 band and the B850 band of LH2. Access to an energetically broad distribution of excitonic states within B875 offers a mechanism for efficient energy transfer from LH2 to LH1 during photosynthesis while limiting back transfer. Two-dimensional lineshapes reveal a rapid decay in the ground-state bleach/stimulated emission of B875. This signal, identified as a decrease in the dipole strength of a strong transition in LH1 on the red side of the B875 band, is assigned to the rapid localization of an initially delocalized exciton state, a dephasing process that frustrates back transfer from LH1 to LH2.},
doi = {10.1063/1.4999057},
url = {https://www.osti.gov/biblio/1469878}, journal = {Journal of Chemical Physics},
issn = {0021-9606},
number = 13,
volume = 147,
place = {United States},
year = {2017},
month = {10}
}

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Works referenced in this record:

Femtosecond spectroscopy of photosynthetic light-harvesting systems
journal, October 1997


Exciton Delocalization and Initial Dephasing Dynamics of Purple Bacterial LH2
journal, August 2000


Two-dimensional spectroscopy of electronic couplings in photosynthesis
journal, March 2005


Structural model and excitonic properties of the dimeric RC–LH1–PufX complex from Rhodobacter sphaeroides
journal, February 2009


Integration of energy and electron transfer processes in the photosynthetic membrane of Rhodobacter sphaeroides
journal, October 2014


Energy Transfer Observed in Live Cells Using Two-Dimensional Electronic Spectroscopy
journal, October 2013


Coherent Two-Dimensional Optical Spectroscopy
journal, April 2008


Vibronic coherence in oxygenic photosynthesis
journal, July 2014


Hydrogen bonds in liquid water are broken only fleetingly
journal, August 2005


Real-time mapping of electronic structure with single-shot two-dimensional electronic spectroscopy
journal, September 2010


Two-dimensional spectroscopy using diffractive optics based phased-locked photon echoes
journal, March 2004


T WO -D IMENSIONAL F EMTOSECOND S PECTROSCOPY
journal, October 2003


Two-dimensional Fourier transform electronic spectroscopy
journal, October 2001


In situ mapping of the energy flow through the entire photosynthetic apparatus
journal, May 2016


Two-Dimensional Line Shapes Derived from Coherent Third-Order Nonlinear Spectroscopy
journal, May 2000


Experimental Implementations of Two-Dimensional Fourier Transform Electronic Spectroscopy
journal, April 2015


Two-dimensional electronic spectroscopy and photosynthesis: Fundamentals and applications to photosynthetic light-harvesting
journal, July 2011


Communication: Coherences observed in vivo in photosynthetic bacteria using two-dimensional electronic spectroscopy
journal, September 2015


Intra- and Interband Transfers in the B800−B850 Antenna of Rhodospirillum m olischianum :  Redfield Theory Modeling of Polarized Pump−Probe Kinetics
journal, October 2003


Three-Pulse Photon Echo Measurements on LH1 and LH2 Complexes of Rhodobacter sphaeroides :  A Nonlinear Spectroscopic Probe of Energy Transfer
journal, September 1997


Independent phasing of rephasing and non-rephasing 2D electronic spectra
journal, August 2013


Förster Energy Transfer Theory as Reflected in the Structures of Photosynthetic Light‐Harvesting Systems
journal, February 2011


Single-Shot Gradient-Assisted Photon Echo Electronic Spectroscopy
journal, April 2011


Energy transfer in photosynthesis: experimental insights and quantitative models
journal, January 2006


Characterization of spectral diffusion from two-dimensional line shapes
journal, August 2006


Electronic Structure and Dynamics of Higher-Lying Excited States in Light Harvesting Complex 1 from Rhodobacter sphaeroides
journal, June 2016


Time-Resolved Absorption Difference Spectroscopy of the LH-1 Antenna of Rhodopseudomonas viridis
journal, June 1998


Two-Dimensional Electronic Spectroscopy Reveals Ultrafast Energy Diffusion in Chlorosomes
journal, July 2012