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Title: Impact of the lipid bilayer on energy transfer kinetics in the photosynthetic protein LH2

Abstract

Photosynthetic purple bacteria convert solar energy to chemical energy with near unity quantum efficiency. The light-harvesting process begins with absorption of solar energy by an antenna protein called Light-Harvesting Complex 2 (LH2). Energy is subsequently transferred within LH2 and then through a network of additional light-harvesting proteins to a central location, termed the reaction center, where charge separation occurs. The energy transfer dynamics of LH2 are highly sensitive to intermolecular distances and relative organizations. As a result, minor structural perturbations can cause significant changes in these dynamics. Previous experiments have primarily been performed in two ways. One uses non-native samples where LH2 is solubilized in detergent, which can alter protein structure. The other uses complex membranes that contain multiple proteins within a large lipid area, which make it difficult to identify and distinguish perturbations caused by protein–protein interactions and lipid–protein interactions. Here, we introduce the use of the biochemical platform of model membrane discs to study the energy transfer dynamics of photosynthetic light-harvesting complexes in a near-native environment. We incorporate a single LH2 from Rhodobacter sphaeroides into membrane discs that provide a spectroscopically amenable sample in an environment more physiological than detergent but less complex than traditional membranes. This providesmore » a simplified system to understand an individual protein and how the lipid–protein interaction affects energy transfer dynamics. We compare the energy transfer rates of detergent-solubilized LH2 with those of LH2 in membrane discs using transient absorption spectroscopy and transient absorption anisotropy. For one key energy transfer step in LH2, we observe a 30% enhancement of the rate for LH2 in membrane discs compared to that in detergent. Based on experimental results and theoretical modeling, we attribute this difference to tilting of the peripheral bacteriochlorophyll in the B800 band. These results highlight the importance of well-defined systems with near-native membrane conditions for physiologically-relevant measurements.« less

Authors:
 [1];  [1];  [1];  [1];  [2];  [2];  [1]; ORCiD logo [1]
  1. Department of Chemistry, Massachusetts Institute of Technology, Cambridge, USA
  2. Department of Biology and Chemistry, Washington University in St. Louis, St. Louis, USA
Publication Date:
Research Org.:
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1421875
Alternate Identifier(s):
OSTI ID: 1505514
Grant/Contract Number:  
SC0018097
Resource Type:
Published Article
Journal Name:
Chemical Science
Additional Journal Information:
Journal Name: Chemical Science Journal Volume: 9 Journal Issue: 12; Journal ID: ISSN 2041-6520
Publisher:
Royal Society of Chemistry
Country of Publication:
United Kingdom
Language:
English
Subject:
14 SOLAR ENERGY; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Ogren, John I., Tong, Ashley L., Gordon, Samuel C., Chenu, Aurélia, Lu, Yue, Blankenship, Robert E., Cao, Jianshu, and Schlau-Cohen, Gabriela S. Impact of the lipid bilayer on energy transfer kinetics in the photosynthetic protein LH2. United Kingdom: N. p., 2018. Web. doi:10.1039/C7SC04814A.
Ogren, John I., Tong, Ashley L., Gordon, Samuel C., Chenu, Aurélia, Lu, Yue, Blankenship, Robert E., Cao, Jianshu, & Schlau-Cohen, Gabriela S. Impact of the lipid bilayer on energy transfer kinetics in the photosynthetic protein LH2. United Kingdom. doi:10.1039/C7SC04814A.
Ogren, John I., Tong, Ashley L., Gordon, Samuel C., Chenu, Aurélia, Lu, Yue, Blankenship, Robert E., Cao, Jianshu, and Schlau-Cohen, Gabriela S. Mon . "Impact of the lipid bilayer on energy transfer kinetics in the photosynthetic protein LH2". United Kingdom. doi:10.1039/C7SC04814A.
@article{osti_1421875,
title = {Impact of the lipid bilayer on energy transfer kinetics in the photosynthetic protein LH2},
author = {Ogren, John I. and Tong, Ashley L. and Gordon, Samuel C. and Chenu, Aurélia and Lu, Yue and Blankenship, Robert E. and Cao, Jianshu and Schlau-Cohen, Gabriela S.},
abstractNote = {Photosynthetic purple bacteria convert solar energy to chemical energy with near unity quantum efficiency. The light-harvesting process begins with absorption of solar energy by an antenna protein called Light-Harvesting Complex 2 (LH2). Energy is subsequently transferred within LH2 and then through a network of additional light-harvesting proteins to a central location, termed the reaction center, where charge separation occurs. The energy transfer dynamics of LH2 are highly sensitive to intermolecular distances and relative organizations. As a result, minor structural perturbations can cause significant changes in these dynamics. Previous experiments have primarily been performed in two ways. One uses non-native samples where LH2 is solubilized in detergent, which can alter protein structure. The other uses complex membranes that contain multiple proteins within a large lipid area, which make it difficult to identify and distinguish perturbations caused by protein–protein interactions and lipid–protein interactions. Here, we introduce the use of the biochemical platform of model membrane discs to study the energy transfer dynamics of photosynthetic light-harvesting complexes in a near-native environment. We incorporate a single LH2 from Rhodobacter sphaeroides into membrane discs that provide a spectroscopically amenable sample in an environment more physiological than detergent but less complex than traditional membranes. This provides a simplified system to understand an individual protein and how the lipid–protein interaction affects energy transfer dynamics. We compare the energy transfer rates of detergent-solubilized LH2 with those of LH2 in membrane discs using transient absorption spectroscopy and transient absorption anisotropy. For one key energy transfer step in LH2, we observe a 30% enhancement of the rate for LH2 in membrane discs compared to that in detergent. Based on experimental results and theoretical modeling, we attribute this difference to tilting of the peripheral bacteriochlorophyll in the B800 band. These results highlight the importance of well-defined systems with near-native membrane conditions for physiologically-relevant measurements.},
doi = {10.1039/C7SC04814A},
journal = {Chemical Science},
number = 12,
volume = 9,
place = {United Kingdom},
year = {2018},
month = {1}
}

Journal Article:
Free Publicly Available Full Text
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DOI: 10.1039/C7SC04814A

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Cited by: 1 work
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