Molecular dynamics of photosynthetic electron flow in a biophotovoltaic system

Biophotovoltaics (BPV) represents an innovative biohybrid technology that couples electrochemistry with oxygenic photosynthetic microbes to harness solar energy and convert it into electricity. Central to BPV systems is the ability of microbes to perform extracellular electron transfer (EET), utiliz...

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Main Authors: Jianqi Yuan, Jens Appel, Kirstin Gutekunst, Bin Lai, Jens Olaf Krömer
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Environmental Science and Ecotechnology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2666498424001339
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author Jianqi Yuan
Jens Appel
Kirstin Gutekunst
Bin Lai
Jens Olaf Krömer
author_facet Jianqi Yuan
Jens Appel
Kirstin Gutekunst
Bin Lai
Jens Olaf Krömer
author_sort Jianqi Yuan
collection DOAJ
description Biophotovoltaics (BPV) represents an innovative biohybrid technology that couples electrochemistry with oxygenic photosynthetic microbes to harness solar energy and convert it into electricity. Central to BPV systems is the ability of microbes to perform extracellular electron transfer (EET), utilizing an anode as an external electron sink. This process simultaneously serves as an electron sink and enhances the efficiency of water photolysis compared to conventional electrochemical water splitting. However, optimizing BPV systems has been hindered by a limited understanding of EET pathways and their impacts on cellular physiology. Here we show photosynthetic electron flows in Synechocystis sp. PCC 6803 cultivated in a ferricyanide-mediated BPV system. By monitoring carbon fixation rates and photosynthetic oxygen exchange, we reveal that EET does not significantly affect cell growth, respiration, carbon fixation, or photosystem II efficiency. However, EET competes for electrons with the flavodiiron protein flv1/3, influencing Mehler-like reactions. Our findings suggest that the ferricyanide mediator facilitates photosynthetic electron extraction from ferredoxins downstream of photosystem I. Additionally, the mediator induces a more reduced plastoquinone pool, an effect independent of EET. At very high ferricyanide concentrations, the electron transport chain exhibits responses resembling the impact of trace cyanide. These insights provide a molecular-level understanding of EET pathways in Synechocystis within BPV systems, offering a foundation for the future refinement of BPV technologies.
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spelling doaj-art-9a2be7ff3c4a443eaeff5d581754be252025-08-20T03:01:11ZengElsevierEnvironmental Science and Ecotechnology2666-49842025-01-012310051910.1016/j.ese.2024.100519Molecular dynamics of photosynthetic electron flow in a biophotovoltaic systemJianqi Yuan0Jens Appel1Kirstin Gutekunst2Bin Lai3Jens Olaf Krömer4Systems Biotechnology Group, Department of Microbial Biotechnology, Helmholtz Centre for Environmental Research - UFZ, 04318, Leipzig, GermanyMolecular Plant Physiology, University Kassel, 34132, Kassel, GermanyMolecular Plant Physiology, University Kassel, 34132, Kassel, GermanyBMBF Junior Research Group Biophotovoltaics, Department of Microbial Biotechnology, Helmholtz Centre for Environmental Research - UFZ, 04318, Leipzig, Germany; Corresponding author. Helmholtz Centre for Environmental Research – UFZ, Permoserstraße 15, 04318, Leipzig, Germany.Systems Biotechnology Group, Department of Microbial Biotechnology, Helmholtz Centre for Environmental Research - UFZ, 04318, Leipzig, GermanyBiophotovoltaics (BPV) represents an innovative biohybrid technology that couples electrochemistry with oxygenic photosynthetic microbes to harness solar energy and convert it into electricity. Central to BPV systems is the ability of microbes to perform extracellular electron transfer (EET), utilizing an anode as an external electron sink. This process simultaneously serves as an electron sink and enhances the efficiency of water photolysis compared to conventional electrochemical water splitting. However, optimizing BPV systems has been hindered by a limited understanding of EET pathways and their impacts on cellular physiology. Here we show photosynthetic electron flows in Synechocystis sp. PCC 6803 cultivated in a ferricyanide-mediated BPV system. By monitoring carbon fixation rates and photosynthetic oxygen exchange, we reveal that EET does not significantly affect cell growth, respiration, carbon fixation, or photosystem II efficiency. However, EET competes for electrons with the flavodiiron protein flv1/3, influencing Mehler-like reactions. Our findings suggest that the ferricyanide mediator facilitates photosynthetic electron extraction from ferredoxins downstream of photosystem I. Additionally, the mediator induces a more reduced plastoquinone pool, an effect independent of EET. At very high ferricyanide concentrations, the electron transport chain exhibits responses resembling the impact of trace cyanide. These insights provide a molecular-level understanding of EET pathways in Synechocystis within BPV systems, offering a foundation for the future refinement of BPV technologies.http://www.sciencedirect.com/science/article/pii/S2666498424001339MediatorExtracellular electron transportFlavodiiron proteinMehler-like reactionMembrane inlet mass spectrometry
spellingShingle Jianqi Yuan
Jens Appel
Kirstin Gutekunst
Bin Lai
Jens Olaf Krömer
Molecular dynamics of photosynthetic electron flow in a biophotovoltaic system
Environmental Science and Ecotechnology
Mediator
Extracellular electron transport
Flavodiiron protein
Mehler-like reaction
Membrane inlet mass spectrometry
title Molecular dynamics of photosynthetic electron flow in a biophotovoltaic system
title_full Molecular dynamics of photosynthetic electron flow in a biophotovoltaic system
title_fullStr Molecular dynamics of photosynthetic electron flow in a biophotovoltaic system
title_full_unstemmed Molecular dynamics of photosynthetic electron flow in a biophotovoltaic system
title_short Molecular dynamics of photosynthetic electron flow in a biophotovoltaic system
title_sort molecular dynamics of photosynthetic electron flow in a biophotovoltaic system
topic Mediator
Extracellular electron transport
Flavodiiron protein
Mehler-like reaction
Membrane inlet mass spectrometry
url http://www.sciencedirect.com/science/article/pii/S2666498424001339
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