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Title: Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells

Abstract

Photosynthesis transfers energy efficiently through a series of antenna complexes to the reaction center where charge separation occurs. Energy transfer in vivo is primarily monitored by measuring fluorescence signals from the small fraction of excitations that fail to result in charge separation. Here, we use two-dimensional electronic spectroscopy to follow the entire energy transfer process in a thriving culture of the purple bacteria, Rhodobacter sphaeroides. By removing contributions from scattered light, we extract the dynamics of energy transfer through the dense network of antenna complexes and into the reaction center. Simulations demonstrate that these dynamics constrain the membrane organization into small pools of core antenna complexes that rapidly trap energy absorbed by surrounding peripheral antenna complexes. The rapid trapping and limited back transfer of these excitations lead to transfer efficiencies of 83% and a small functional light-harvesting unit.

Authors:
 [1];  [1]; ORCiD logo [1];  [1];  [2]; ORCiD logo [2]; ORCiD logo [1]
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  1. The Univ. of Chicago, Chicago, IL (United States)
  2. Univ. of Sheffield, Sheffield (United Kingdom)
Publication Date:
Research Org.:
Energy Frontier Research Centers (EFRC), Washington, D.C. (United States). Photosynthetic Antenna Research Center (PARC); Washington Univ., St. Louis, MO (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1469984
Alternate Identifier(s):
OSTI ID: 1545601
Grant/Contract Number:  
SC0001035
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal Issue: 1; 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 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
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

Dahlberg, Peter D., Ting, Po -Chieh, Massey, Sara C., Allodi, Marco A., Martin, Elizabeth C., Hunter, C. Neil, and Engel, Gregory S. Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells. United States: N. p., 2017. Web. doi:10.1038/s41467-017-01124-z.
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Dahlberg, Peter D., Ting, Po -Chieh, Massey, Sara C., Allodi, Marco A., Martin, Elizabeth C., Hunter, C. Neil, & Engel, Gregory S. Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells. United States. https://doi.org/10.1038/s41467-017-01124-z
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Dahlberg, Peter D., Ting, Po -Chieh, Massey, Sara C., Allodi, Marco A., Martin, Elizabeth C., Hunter, C. Neil, and Engel, Gregory S. Tue . "Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells". United States. https://doi.org/10.1038/s41467-017-01124-z. https://www.osti.gov/servlets/purl/1469984.
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@article{osti_1469984,
title = {Mapping the ultrafast flow of harvested solar energy in living photosynthetic cells},
author = {Dahlberg, Peter D. and Ting, Po -Chieh and Massey, Sara C. and Allodi, Marco A. and Martin, Elizabeth C. and Hunter, C. Neil and Engel, Gregory S.},
abstractNote = {Photosynthesis transfers energy efficiently through a series of antenna complexes to the reaction center where charge separation occurs. Energy transfer in vivo is primarily monitored by measuring fluorescence signals from the small fraction of excitations that fail to result in charge separation. Here, we use two-dimensional electronic spectroscopy to follow the entire energy transfer process in a thriving culture of the purple bacteria, Rhodobacter sphaeroides. By removing contributions from scattered light, we extract the dynamics of energy transfer through the dense network of antenna complexes and into the reaction center. Simulations demonstrate that these dynamics constrain the membrane organization into small pools of core antenna complexes that rapidly trap energy absorbed by surrounding peripheral antenna complexes. The rapid trapping and limited back transfer of these excitations lead to transfer efficiencies of 83% and a small functional light-harvesting unit.},
doi = {10.1038/s41467-017-01124-z},
journal = {Nature Communications},
number = 1,
volume = 8,
place = {United States},
year = {2017},
month = {10}
}
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Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1038/s41467-017-01124-z
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Citation Metrics:
Cited by: 19 works
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Figures / Tables:

Fig. 1 Fig. 1: Annihilation reveals a highly connected network of light-harvesting complexes in vivo. a, Crystal structures of LH2 and RC-LH1-PufX (PDB 1KZU and PDB 4JC9, respectively) with the carotenoids and Bchl a phytyl tails removed for clarity. LH2 contains two bands of Bchl a, the B800 (blue) and the B850more » (green). LH1 contains a single band of Bchl a, B875 (red) that transfers energy to the special pair of the RC (orange). b, Absorption spectra in a 200 μm path length of cells containing only LH2, cells containing only LH1, and wild-type (WT) cells. The large offset from zero optical density is due to optical scattering. The 2DES excitation spectrum is shown in gray and is produced by super continuum generation in argon gas. The spectrum is broad enough to interrogate the entire energy transfer process from LH2→LH1→RC. c, Absorptive 2DES spectrum of LH2-only cells taken with 17.6 μJ cm−2 at T = 1 ps. d, Waiting time traces acquired at different powers from the maximum of the GSB/SE feature. The traces are the average of three scans and the shaded background is the mean ± the standard deviation. The change in dynamics with power is indicative of exciton-exciton annihilation. The dashed traces are the population of excited LH2 from a random walk simulation with a lifetime for energy transfer between LH2s of 2.7 ps, a domain size of 64 LH2, and a fluorescence lifetime of 250 ps« less
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    Works referencing / citing this record:

    Spatially-resolved fluorescence-detected two-dimensional electronic spectroscopy probes varying excitonic structure in photosynthetic bacteria
    journal, October 2018

    • Tiwari, Vivek; Matutes, Yassel Acosta; Gardiner, Alastair T.
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-018-06619-x

    Quantum coherences reveal excited-state dynamics in biophysical systems
    journal, June 2019

    Turning the challenge of quantum biology on its head: biological control of quantum optical systems
    journal, January 2019

    • Lishchuk, Anna; Vasilev, Cvetelin; Johnson, Matthew P.
    • Faraday Discussions, Vol. 216
    • DOI: 10.1039/c8fd00241j

    Dissecting the cytochrome c2–reaction centre interaction in bacterial photosynthesis using single molecule force spectroscopy
    journal, August 2019

    • Vasilev, Cvetelin; Mayneord, Guy E.; Brindley, Amanda A.
    • Biochemical Journal, Vol. 476, Issue 15
    • DOI: 10.1042/bcj20170519

    Geometry Effects on Light‐Harvesting Complex's Light Absorption and Energy Transfer in Purple Bacteria
    journal, July 2019

    • Zeng, Lingyu; Liao, Zeyang; Wang, Xue‐hua
    • Photochemistry and Photobiology, Vol. 95, Issue 6
    • DOI: 10.1111/php.13129
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