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Title: Robust light harvesting by a noisy antenna

Abstract

Photosynthetic light harvesting can be very efficient in solar energy conversion while taking place in a highly disordered and noisy physiological environment. This efficiency is achieved by the ultrafast speed of the primary photosynthetic processes, which is enabled by a delicate interplay of quantum effects, thermodynamics and environmental noise. The primary processes take place in light-harvesting antennas built from pigments bound to a fluctuating protein scaffold. Here, we employ ultrafast single-molecule spectroscopy to follow fluctuations of the femtosecond energy transfer times in individual LH2 antenna complexes of purple bacteria. By combining single molecule results with ensemble spectroscopy through a unified theoretical description of both, we show how the protein fluctuations alter the excitation energy transfer dynamics. We find that from the thirteen orders of magnitude of possible timescales from picoseconds to minutes, the relevant fluctuations occur predominantly on a biological timescale of seconds, i.e. in the domain of slow protein motion. The measured spectra and dynamics can be explained by the protein modulating pigment excitation energies only. Moreover, we find that the small spread of pigment mean energies allows for excitation delocalization between the coupled pigments to survive. These unique features provide fast energy transport even in the presence ofmore » disorder. We conclude that this is the mechanism that enables LH2 to operate as a robust light-harvester, in spite of its intrinsically noisy biological environment.« less

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [2];  [1]; ORCiD logo [3]
  1. Department of Biophysics, Faculty of Sciences, Vrije Universiteit Amsterdam, 1081HV Amsterdam, The Netherlands
  2. Institute of Molecular, Cellular and Systems Biology, College of Medical, Veterinary and Life Sciences, University of Glasgow
  3. Faculty of Mathematics and Physics, Charles University, 121 16 Prague, Czech Republic
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) (SC-22)
OSTI Identifier:
1418068
Alternate Identifier(s):
OSTI ID: 1470100
Grant/Contract Number:  
SC 0001035; SC0001035
Resource Type:
Published Article
Journal Name:
Physical Chemistry Chemical Physics
Additional Journal Information:
Journal Name: Physical Chemistry Chemical Physics Journal Volume: 20 Journal Issue: 6; Journal ID: ISSN 1463-9076
Publisher:
Royal Society of Chemistry (RSC)
Country of Publication:
United Kingdom
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

Malý, Pavel, Gardiner, Alastair T., Cogdell, Richard J., van Grondelle, Rienk, and Mančal, Tomáš. Robust light harvesting by a noisy antenna. United Kingdom: N. p., 2018. Web. doi:10.1039/C7CP06139K.
Malý, Pavel, Gardiner, Alastair T., Cogdell, Richard J., van Grondelle, Rienk, & Mančal, Tomáš. Robust light harvesting by a noisy antenna. United Kingdom. doi:10.1039/C7CP06139K.
Malý, Pavel, Gardiner, Alastair T., Cogdell, Richard J., van Grondelle, Rienk, and Mančal, Tomáš. Mon . "Robust light harvesting by a noisy antenna". United Kingdom. doi:10.1039/C7CP06139K.
@article{osti_1418068,
title = {Robust light harvesting by a noisy antenna},
author = {Malý, Pavel and Gardiner, Alastair T. and Cogdell, Richard J. and van Grondelle, Rienk and Mančal, Tomáš},
abstractNote = {Photosynthetic light harvesting can be very efficient in solar energy conversion while taking place in a highly disordered and noisy physiological environment. This efficiency is achieved by the ultrafast speed of the primary photosynthetic processes, which is enabled by a delicate interplay of quantum effects, thermodynamics and environmental noise. The primary processes take place in light-harvesting antennas built from pigments bound to a fluctuating protein scaffold. Here, we employ ultrafast single-molecule spectroscopy to follow fluctuations of the femtosecond energy transfer times in individual LH2 antenna complexes of purple bacteria. By combining single molecule results with ensemble spectroscopy through a unified theoretical description of both, we show how the protein fluctuations alter the excitation energy transfer dynamics. We find that from the thirteen orders of magnitude of possible timescales from picoseconds to minutes, the relevant fluctuations occur predominantly on a biological timescale of seconds, i.e. in the domain of slow protein motion. The measured spectra and dynamics can be explained by the protein modulating pigment excitation energies only. Moreover, we find that the small spread of pigment mean energies allows for excitation delocalization between the coupled pigments to survive. These unique features provide fast energy transport even in the presence of disorder. We conclude that this is the mechanism that enables LH2 to operate as a robust light-harvester, in spite of its intrinsically noisy biological environment.},
doi = {10.1039/C7CP06139K},
journal = {Physical Chemistry Chemical Physics},
number = 6,
volume = 20,
place = {United Kingdom},
year = {2018},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1039/C7CP06139K

Citation Metrics:
Cited by: 4 works
Citation information provided by
Web of Science

Figures / Tables:

Fig. 1 Fig. 1: Structure of the excited state manifold in the LH2 antenna complex. (A) The lines represent individual excitonic states, with energies (position) and oscillator strength (line thickness) averaged over the static pigment energetic disorder. Initial (B) and final (D) light harvesting states in LH2, measured by absorption and fluorescence,more » respectively. Experimental data (black) are compared to the theoretical model (orange). (C) The structure of the LH2 antenna, with the B850 (red) and B800 (orange) bacteriochlorophyll rings. Black: protein helices, yellow: carotenoids. The picture was rendered in VMD based on the 2FKW structure used for calculations.« less

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    Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.