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Title: Correlated fluorescence quenching and topographic mapping of Light-Harvesting Complex II within surface-assembled aggregates and lipid bilayers

Abstract

Light-Harvesting Complex II (LHCII) is a chlorophyll-protein antenna complex that efficiently absorbs solar energy and transfers electronic excited states to photosystems I and II. Under excess light intensity LHCII can adopt a photoprotective state in which excitation energy is safely dissipated as heat, a process known as Non-Photochemical Quenching (NPQ). In vivo NPQ is triggered by combinatorial factors including transmembrane ΔpH, PsbS protein and LHCII-bound zeaxanthin, leading to dramatically shortened LHCII fluorescence lifetimes. In vitro, LHCII in detergent solution or in proteoliposomes can reversibly adopt an NPQ-like state, via manipulation of detergent/protein ratio, lipid/protein ratio, pH or pressure. Previous spectroscopic investigations revealed changes in exciton dynamics and protein conformation that accompany quenching, however, LHCII-LHCII interactions have not been extensively studied. Here, we correlated fluorescence lifetime imaging microscopy (FLIM) and atomic force microscopy (AFM) of trimeric LHCII adsorbed to mica substrates and manipulated the environment to cause varying degrees of quenching. AFM showed that LHCII self-assembled onto mica forming 2D-aggregates (25–150 nm width). FLIM determined that LHCII in these aggregates were in a quenched state, with much lower fluorescence lifetimes (~0.25 ns) compared to free LHCII in solution (2.2–3.9 ns). LHCII-LHCII interactions were disrupted by thylakoid lipids or phospholipids, leading tomore » intermediate fluorescent lifetimes (0.6–0.9 ns). To our knowledge, this is the first in vitro correlation of nanoscale membrane imaging with LHCII quenching. Our findings suggest that lipids could play a key role in modulating the extent of LHCII-LHCII interactions within the thylakoid membrane and so the propensity for NPQ activation.« less

Authors:
; ; ;
Publication Date:
Research Org.:
Washington Univ., St. Louis, MO (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); Biotechnology and Biological Sciences Research Council (BBSRC UK); European Research Council (ERC)
OSTI Identifier:
1615096
Alternate Identifier(s):
OSTI ID: 1566429
Grant/Contract Number:  
SC 0001035; SC0001035; BB/M013723/1; BB/M000265/1; 338895
Resource Type:
Published Article
Journal Name:
Biochimica et Biophysica Acta - Bioenergetics
Additional Journal Information:
Journal Name: Biochimica et Biophysica Acta - Bioenergetics Journal Volume: 1859 Journal Issue: 10; Journal ID: ISSN 0005-2728
Publisher:
Elsevier
Country of Publication:
Netherlands
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; solar (fuels); photosynthesis (natural and artificial); biofuels (including algae and biomass); bio-inspired; charge transport; membrane; synthesis (novel materials); synthesis (self-assembly)

Citation Formats

Adams, Peter G., Vasilev, Cvetelin, Hunter, C. Neil, and Johnson, Matthew P. Correlated fluorescence quenching and topographic mapping of Light-Harvesting Complex II within surface-assembled aggregates and lipid bilayers. Netherlands: N. p., 2018. Web. doi:10.1016/j.bbabio.2018.06.011.
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Adams, Peter G., Vasilev, Cvetelin, Hunter, C. Neil, & Johnson, Matthew P. Correlated fluorescence quenching and topographic mapping of Light-Harvesting Complex II within surface-assembled aggregates and lipid bilayers. Netherlands. https://doi.org/10.1016/j.bbabio.2018.06.011
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Adams, Peter G., Vasilev, Cvetelin, Hunter, C. Neil, and Johnson, Matthew P. Mon . "Correlated fluorescence quenching and topographic mapping of Light-Harvesting Complex II within surface-assembled aggregates and lipid bilayers". Netherlands. https://doi.org/10.1016/j.bbabio.2018.06.011.
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@article{osti_1615096,
title = {Correlated fluorescence quenching and topographic mapping of Light-Harvesting Complex II within surface-assembled aggregates and lipid bilayers},
author = {Adams, Peter G. and Vasilev, Cvetelin and Hunter, C. Neil and Johnson, Matthew P.},
abstractNote = {Light-Harvesting Complex II (LHCII) is a chlorophyll-protein antenna complex that efficiently absorbs solar energy and transfers electronic excited states to photosystems I and II. Under excess light intensity LHCII can adopt a photoprotective state in which excitation energy is safely dissipated as heat, a process known as Non-Photochemical Quenching (NPQ). In vivo NPQ is triggered by combinatorial factors including transmembrane ΔpH, PsbS protein and LHCII-bound zeaxanthin, leading to dramatically shortened LHCII fluorescence lifetimes. In vitro, LHCII in detergent solution or in proteoliposomes can reversibly adopt an NPQ-like state, via manipulation of detergent/protein ratio, lipid/protein ratio, pH or pressure. Previous spectroscopic investigations revealed changes in exciton dynamics and protein conformation that accompany quenching, however, LHCII-LHCII interactions have not been extensively studied. Here, we correlated fluorescence lifetime imaging microscopy (FLIM) and atomic force microscopy (AFM) of trimeric LHCII adsorbed to mica substrates and manipulated the environment to cause varying degrees of quenching. AFM showed that LHCII self-assembled onto mica forming 2D-aggregates (25–150 nm width). FLIM determined that LHCII in these aggregates were in a quenched state, with much lower fluorescence lifetimes (~0.25 ns) compared to free LHCII in solution (2.2–3.9 ns). LHCII-LHCII interactions were disrupted by thylakoid lipids or phospholipids, leading to intermediate fluorescent lifetimes (0.6–0.9 ns). To our knowledge, this is the first in vitro correlation of nanoscale membrane imaging with LHCII quenching. Our findings suggest that lipids could play a key role in modulating the extent of LHCII-LHCII interactions within the thylakoid membrane and so the propensity for NPQ activation.},
doi = {10.1016/j.bbabio.2018.06.011},
journal = {Biochimica et Biophysica Acta - Bioenergetics},
number = 10,
volume = 1859,
place = {Netherlands},
year = {Mon Oct 01 00:00:00 EDT 2018},
month = {Mon Oct 01 00:00:00 EDT 2018}
}
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https://doi.org/10.1016/j.bbabio.2018.06.011
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