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      Photocurrent Generation by Plant Light-Harvesting Complexes is Enhanced by Lipid-Linked Chromophores in a Self-Assembled Lipid Membrane

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          Abstract

          The light-harvesting pigment–protein complex II (LHCII) from plants can be used as a component for biohybrid photovoltaic devices, acting as a photosensitizer to increase the photocurrent generated when devices are illuminated with sunlight. LHCII is effective at photon absorption in the red and blue regions of the visible spectrum, however, it has low absorption in the green region (550–650 nm). Previous studies have shown that synthetic chromophores can be used to fill this spectral gap and transfer additional energy to LHCII, but it was uncertain whether this would translate into an improved performance for photovoltaics. In this study, we demonstrate amplified photocurrent generation from LHCII under green light illumination by coupling this protein to Texas Red (TR) chromophores that are coassembled into a lipid bilayer deposited onto electrodes. Absorption spectroscopy shows that LHCII and lipid-linked TR are successfully incorporated into lipid membranes and maintained on electrode surfaces. Photocurrent action spectra show that the increased absorption due to TR directly translates into a significant increase of photocurrent output from LHCII. However, the absolute magnitude of the photocurrent appears to be limited by the lipid bilayer acting as an insulator and the TR enhancement effect reaches a maximum due to protein, lipid or substrate-related quenching effects. Future work should be performed to optimize the use of extrinsic chromophores within novel biophotovoltaic devices.

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          Most cited references66

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          Nonphotochemical Chlorophyll Fluorescence Quenching: Mechanism and Effectiveness in Protecting Plants from Photodamage.

          We review the mechanism underlying nonphotochemical chlorophyll fluorescence quenching (NPQ) and its role in protecting plants against photoinhibition. This review includes an introduction to this phenomenon, a brief history of major milestones in our understanding of NPQ, definitions, and a discussion of quantitative measurements of NPQ We discuss the current knowledge and unknown aspects in the NPQ scenario, including the following: ΔpH, the proton gradient (trigger); light-harvesting complex II (LHCII), PSII light harvesting antenna (site); and changes in the antenna induced by ΔpH (change), which lead to the creation of the quencher We conclude that the minimum requirements for NPQ in vivo are ΔpH, LHCII complexes, and the PsbS protein. We highlight the most important unknown in the NPQ scenario, the mechanism by which PsbS acts upon the LHCII antenna. Finally, we describe a novel, emerging technology for assessing the photoprotective "power" of NPQ and the important findings obtained through this technology.
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            Solid supported lipid bilayers: From biophysical studies to sensor design

            The lipid bilayer is one of the most eloquent and important self-assembled structures in nature. It not only provides a protective container for cells and sub-cellular compartments, but also hosts much of the machinery for cellular communication and transport across the cell membrane. Solid supported lipid bilayers provide an excellent model system for studying the surface chemistry of the cell. Moreover, they are accessible to a wide variety of surface-specific analytical techniques. This makes it possible to investigate processes such as cell signaling, ligand–receptor interactions, enzymatic reactions occurring at the cell surface, as well as pathogen attack. In this review, the following membrane systems are discussed: black lipid membranes, solid supported lipid bilayers, hybrid lipid bilayers, and polymer cushioned lipid bilayers. Examples of how supported lipid membrane technology is interfaced with array based systems by photolithographic patterning, spatial addressing, microcontact printing, and microfluidic patterning are explored. Also, the use of supported lipid bilayers in microfluidic devices for the development of lab-on-a-chip based platforms is examined. Finally, the utility of lipid bilayers in nanotechnology and future directions in this area are discussed.
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              Mechanisms of photoprotection and nonphotochemical quenching in pea light-harvesting complex at 2.5 A resolution.

              The plant light-harvesting complex of photosystem II (LHC-II) collects and transmits solar energy for photosynthesis in chloroplast membranes and has essential roles in regulation of photosynthesis and in photoprotection. The 2.5 A structure of pea LHC-II determined by X-ray crystallography of stacked two-dimensional crystals shows how membranes interact to form chloroplast grana, and reveals the mutual arrangement of 42 chlorophylls a and b, 12 carotenoids and six lipids in the LHC-II trimer. Spectral assignment of individual chlorophylls indicates the flow of energy in the complex and the mechanism of photoprotection in two close chlorophyll a-lutein pairs. We propose a simple mechanism for the xanthophyll-related, slow component of nonphotochemical quenching in LHC-II, by which excess energy is transferred to a zeaxanthin replacing violaxanthin in its binding site, and dissipated as heat. Our structure shows the complex in a quenched state, which may be relevant for the rapid, pH-induced component of nonphotochemical quenching.
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                Author and article information

                Journal
                J Phys Chem B
                J Phys Chem B
                jp
                jpcbfk
                The Journal of Physical Chemistry. B
                American Chemical Society
                1520-6106
                1520-5207
                09 January 2025
                23 January 2025
                : 129
                : 3
                : 900-910
                Affiliations
                []Department of Life Science and Applied Chemistry, Graduate School of Engineering, Nagoya Institute of Technology , Gokiso-cho, Showa-ku, Nagoya 466-8555, Japan
                []School of Physics and Astronomy, University of Leeds , Leeds LS2 9JT, U.K.
                [§ ]Astbury Centre for Structural Molecular Biology, University of Leeds , Leeds LS2 9JT, U.K.
                []Department of Nanopharmaceutical Sciences, Nagoya Institute of Technology , Gokiso-cho, Showa-ku, Nagoya 4668-8555, Japan
                Author notes
                Author information
                https://orcid.org/0000-0002-3940-8770
                https://orcid.org/0000-0002-9786-3114
                Article
                10.1021/acs.jpcb.4c07402
                11770764
                39782489
                50c91807-5fed-4fc3-b79c-25f550149c56
                © 2025 The Authors. Published by American Chemical Society

                Permits the broadest form of re-use including for commercial purposes, provided that author attribution and integrity are maintained ( https://creativecommons.org/licenses/by/4.0/).

                History
                : 31 October 2024
                : 27 December 2024
                : 20 December 2024
                Funding
                Funded by: Engineering and Physical Sciences Research Council, doi 10.13039/501100000266;
                Award ID: EP/T013958/1
                Funded by: Japan Society for the Promotion of Science, doi 10.13039/501100001691;
                Award ID: 24H01128
                Funded by: Japan Society for the Promotion of Science, doi 10.13039/501100001691;
                Award ID: 22H05416
                Funded by: Japan Society for the Promotion of Science, doi 10.13039/501100001691;
                Award ID: 21KK0088
                Funded by: Japan Society for the Promotion of Science, doi 10.13039/501100001691;
                Award ID: 21H01985
                Categories
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                jp4c07402
                jp4c07402

                Physical chemistry
                Physical chemistry

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