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Title: Augmenting light coverage for photosynthesis through YFP-enhanced charge separation at the Rhodobacter sphaeroides reaction centre

Abstract

Photosynthesis uses a limited range of the solar spectrum, so enhancing spectral coverage could improve the efficiency of light capture. Here, we show that a hybrid reaction centre (RC)/yellow fluorescent protein (YFP) complex accelerates photosynthetic growth in the bacterium Rhodobacter sphaeroides. The structure of the RC/YFP-light-harvesting 1 (LH1) complex shows the position of YFP attachment to the RC-H subunit, on the cytoplasmic side of the RC complex. Fluorescence lifetime microscopy of whole cells and ultrafast transient absorption spectroscopy of purified RC/YFP complexes show that the YFP–RC intermolecular distance and spectral overlap between the emission of YFP and the visible-region (Q X) absorption bands of the RC allow energy transfer via a Fo¨rster mechanism, with an efficiency of 40±10%. Finally, this proof-of-principle study demonstrates the feasibility of increasing spectral coverage for harvesting light using non-native genetically-encoded light-absorbers, thereby augmenting energy transfer and trapping in photosynthesis.

Authors:
ORCiD logo [1];  [2];  [1];  [1];  [2];  [1];  [1];  [1];  [2]; ORCiD logo [2];  [1];  [2];  [2]; ORCiD logo [1]
  1. Univ. of Sheffield, Sheffield (United Kingdom)
  2. Washington Univ., St. Louis, MO (United States)
Publication Date:
Research Org.:
Washington Univ., St. Louis, MO (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1345997
Grant/Contract Number:
SC0001035
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; bioenergetics; devices for energy harvesting; photosynthesis; synthetic biology

Citation Formats

Grayson, Katie J., Faries, Kaitlyn M., Huang, Xia, Qian, Pu, Dilbeck, Preston, Martin, Elizabeth C., Hitchcock, Andrew, Vasilev, Cvetelin, Yuen, Jonathan M., Niedzwiedzki, Dariusz M., Leggett, Graham J., Holten, Dewey, Kirmaier, Christine, and Hunter, C. Neil. Augmenting light coverage for photosynthesis through YFP-enhanced charge separation at the Rhodobacter sphaeroides reaction centre. United States: N. p., 2017. Web. doi:10.1038/ncomms13972.
Grayson, Katie J., Faries, Kaitlyn M., Huang, Xia, Qian, Pu, Dilbeck, Preston, Martin, Elizabeth C., Hitchcock, Andrew, Vasilev, Cvetelin, Yuen, Jonathan M., Niedzwiedzki, Dariusz M., Leggett, Graham J., Holten, Dewey, Kirmaier, Christine, & Hunter, C. Neil. Augmenting light coverage for photosynthesis through YFP-enhanced charge separation at the Rhodobacter sphaeroides reaction centre. United States. doi:10.1038/ncomms13972.
Grayson, Katie J., Faries, Kaitlyn M., Huang, Xia, Qian, Pu, Dilbeck, Preston, Martin, Elizabeth C., Hitchcock, Andrew, Vasilev, Cvetelin, Yuen, Jonathan M., Niedzwiedzki, Dariusz M., Leggett, Graham J., Holten, Dewey, Kirmaier, Christine, and Hunter, C. Neil. Thu . "Augmenting light coverage for photosynthesis through YFP-enhanced charge separation at the Rhodobacter sphaeroides reaction centre". United States. doi:10.1038/ncomms13972. https://www.osti.gov/servlets/purl/1345997.
@article{osti_1345997,
title = {Augmenting light coverage for photosynthesis through YFP-enhanced charge separation at the Rhodobacter sphaeroides reaction centre},
author = {Grayson, Katie J. and Faries, Kaitlyn M. and Huang, Xia and Qian, Pu and Dilbeck, Preston and Martin, Elizabeth C. and Hitchcock, Andrew and Vasilev, Cvetelin and Yuen, Jonathan M. and Niedzwiedzki, Dariusz M. and Leggett, Graham J. and Holten, Dewey and Kirmaier, Christine and Hunter, C. Neil},
abstractNote = {Photosynthesis uses a limited range of the solar spectrum, so enhancing spectral coverage could improve the efficiency of light capture. Here, we show that a hybrid reaction centre (RC)/yellow fluorescent protein (YFP) complex accelerates photosynthetic growth in the bacterium Rhodobacter sphaeroides. The structure of the RC/YFP-light-harvesting 1 (LH1) complex shows the position of YFP attachment to the RC-H subunit, on the cytoplasmic side of the RC complex. Fluorescence lifetime microscopy of whole cells and ultrafast transient absorption spectroscopy of purified RC/YFP complexes show that the YFP–RC intermolecular distance and spectral overlap between the emission of YFP and the visible-region (QX) absorption bands of the RC allow energy transfer via a Fo¨rster mechanism, with an efficiency of 40±10%. Finally, this proof-of-principle study demonstrates the feasibility of increasing spectral coverage for harvesting light using non-native genetically-encoded light-absorbers, thereby augmenting energy transfer and trapping in photosynthesis.},
doi = {10.1038/ncomms13972},
journal = {Nature Communications},
number = ,
volume = 8,
place = {United States},
year = {Thu Jan 05 00:00:00 EST 2017},
month = {Thu Jan 05 00:00:00 EST 2017}
}

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  • Femtosecond transient absorption spectroscopy has been used to investigate the excitation wavelength dependence of energy transfer and initial charge separation processes in reaction centers of the purple nonsulfur photosynthetic bacterium Rhodobacter sphaeroides (R-26) at room temperature. The Q{sub Y} transition bands of the bacteriopheophytins (H), bacteriochlorophyll monomers (B), and special pair (P) were selectively excited with pulses of 150 fs duration and 5 nm spectral bandwidth. Absorbance changes were analyzed over the entire wavelength region from 700 to 1000 nm. From this analysis we concluded the following: (1) As seen by others, energy transfer between H, B, and P ismore » extremely fast, occurring on the 100-300 fs time scale. (2) The spectral evolution of the system is excitation wavelength dependent for picoseconds after excitation, implying that vibrational relaxation is not complete on the time scale of either energy transfer or charge separation and suggesting that the pathway of charge separation may be excitation wavelength dependent. (3) The absorbance change spectra of the initial excited states of B and H are not consistent with intensity borrowing between these bands, reopening the question of what gives rise to the complex absorbance changes normally associated with the H{sub A}{sup -} state. (4) The 10-20 ps component of the stimulated emission decay is excitation wavelength dependent and spectrally different from the dominant 2-3 ps decay of the stimulated emission. 67 refs., 8 figs.« less
  • Ubiquinone forms an integral part of the electron transport chain in cellular respiration and photosynthesis across a vast number of organisms. Prior experimental results have shown that the photosynthetic reaction center (RC) from Rhodobacter sphaeroides is only fully functional with a limited set of methoxy-bearing quinones, suggesting that specific interactions with this substituent are required to drive electron transport and the formation of quinol. The nature of these interactions has yet to be determined. Through parameterization of a CHARMM-compatible quinone force field and subsequent molecular dynamics simulations of the quinone-bound RC, in this paper we have investigated and characterized themore » interactions of the protein with the quinones in the Q A and Q B sites using both equilibrium simulation and thermodynamic integration. In particular, we identify a specific interaction between the 2-methoxy group of ubiquinone in the Q B site and the amide nitrogen of GlyL225 that we implicate in locking the orientation of the 2-methoxy group, thereby tuning the redox potential difference between the quinones occupying the Q A and Q B sites. Finally, disruption of this interaction leads to weaker binding in a ubiquinone analogue that lacks a 2-methoxy group, a finding supported by reverse electron transfer electron paramagnetic resonance experiments of the Q A–Q B– biradical and competitive binding assays.« less