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Making the connections: physical and electric interactions in biohybrid photosynthetic systems.

ABSTRACT: Biohybrid photosynthesis systems, which combine biological and non-biological materials, have attracted recent interest in solar-to-chemical energy conversion. However, the solar efficiencies of such systems remain low, despite advances in both artificial photosynthesis and synthetic biology. Here we discuss the potential of conjugated organic materials as photosensitisers for biological hybrid systems compared to traditional inorganic semiconductors. Organic materials offer the ability to tune both photophysical properties and the specific physicochemical interactions between the photosensitiser and biological cells, thus improving stability and charge transfer. We highlight the state-of-the-art and opportunities for new approaches in designing new biohybrid systems. This perspective also summarises the current understanding of the underlying electron transport process and highlights the research areas that need to be pursued to underpin the development of hybrid photosynthesis systems.

SUBMITTER: Yang Y

PROVIDER: S-EPMC10566253 | biostudies-literature | 2023 Oct

REPOSITORIES: biostudies-literature

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Making the connections: physical and electric interactions in biohybrid photosynthetic systems.

Yang Ying Y Liu Lu-Ning LN Tian Haining H Cooper Andrew I AI Sprick Reiner Sebastian RS

Energy & environmental science 20230816 10

Biohybrid photosynthesis systems, which combine biological and non-biological materials, have attracted recent interest in solar-to-chemical energy conversion. However, the solar efficiencies of such systems remain low, despite advances in both artificial photosynthesis and synthetic biology. Here we discuss the potential of conjugated organic materials as photosensitisers for biological hybrid systems compared to traditional inorganic semiconductors. Organic materials offer the ability to tune ...[more]

PMID: 38013927

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Project description:Flavin chemistry is ubiquitous in biological systems with flavoproteins engaged in important redox reactions. In photosynthesis, flavin cofactors are used as electron donors/acceptors to facilitate charge transfer and accumulation for ultimate use in carbon fixation. Following light-induced charge separation in the photosynthetic transmembrane reaction center photosystem I (PSI), an electron is transferred to one of two small soluble shuttle proteins, a ferredoxin (Fd) or a flavodoxin (Fld) (the latter in the condition of Fe-deficiency), followed by electron transfer to the ferredoxin-NADP+ reductase (FNR) enzyme. FNR accepts two of these sequential one electron transfers, with its flavin adenine dinucleotide (FAD) cofactor becoming doubly reduced, forming a hydride which is then passed onto the substrate NADP+ to form NADPH. The two one-electron potentials (oxidized/semiquinone and semiquinone/hydroquinone) are similar to each other with the FNR protein stabilizing the hydroquinone, making spectroscopic detection of the intermediate semiquinone state difficult. We employed a new biohybrid-based strategy that involved truncating the native three-protein electron transfer cascade PSI → Fd → FNR to a two-protein cascade by replacing PSI with a molecular Ru(ii) photosensitizer (RuPS) which is covalently bound to Fd and Fld to form biohybrid complexes that successfully mimic PSI in light-driven NADPH formation. RuFd → FNR and RuFld → FNR electron transfer experiments revealed a notable distinction in photosynthetic charge accumulation that we attribute to the different protein cofactors [2Fe2S] and flavin. After freeze quenching the two-protein systems under illumination, an intermediate semiquinone state of FNR was readily observed with cw X-band EPR spectroscopy. The increased spectral resolution from selective deuteration allowed EPR detection of inter-flavoprotein electron transfer. This work establishes a biohybrid experimental approach for further studies of photosynthetic light-driven electron transfer chain that culminates at FNR and highlights nature's mechanisms that couple single electron transfer chemistry to charge accumulation, providing important insight for the development of photon-to-fuel schemes.

Dataset Information

Making the connections: physical and electric interactions in biohybrid photosynthetic systems.

Publications

Making the connections: physical and electric interactions in biohybrid photosynthetic systems.

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