Feng Liu

Oxygenic photosynthesis generates ATP and NADPH via linear electron flow from water to NADP ⁺ , a process thought to require photosystem I (PSI) for reductant formation. Here we demonstrate that oxygenic photosynthesis can operate without PSI in the cyanobacterium Synechocystis sp. PCC 6803. Using genetic engineering and adaptive laboratory evolution, we obtained PSI-deficient lineages capable of photoautotrophic growth, inorganic carbon fixation, and light-driven oxygen evolution. PSI-independent photoautotrophy arose from co-mutations in at least two proteins, including the translation elongation factor G (FusA), and required a functional NDH-1 complex. We propose that the light-driven electron transport in the evolved strains is reorganised in two branches: one involving terminal oxidases to generate proton motive force, and a second in which reverse NDH-1 activity exploits this gradient to produce reductant. These findings uncover unexpected plasticity in the thylakoid electron transport network and prompt a reassessment of the canonical requirement for PSI in oxygenic photosynthesis.

Oxygenic photosynthesis in cyanobacteria, algae, and plants fixes carbon dioxide and releases oxygen. This process depends on ATP and NADPH generated by light-driven reactions involving multi-protein complexes and mobile electron carriers. Central to these reactions are Photosystem II (PSII) and Photosystem I (PSI), which enable linear electron flow (LEF) from water to NADP ⁺ molecules ¹ . LEF both drives proton gradient formation for ATP synthesis and supports NADP ⁺ reduction via ferredoxin-mediated electron transfer from PSI ^2–4 . According to prevailing models, LEF cannot occur without PSI, as its absence would block NADP⁺ reduction. Here we show that oxygenic photosynthesis can take place independently of PSI in the cyanobacterium Synechocystis PCC 6803. Through adaptive laboratory evolution, we obtained PSI-deficient lineages capable of photoautotrophic growth, inorganic carbon fixation, and light-dependent oxygen evolution. PSI-independent photoautotrophy emerged following co-mutations in at least two proteins, including the translation elongation factor G (FusA), and was abolished when the NDH-1 complex was disrupted. These results suggest that NDH-1 can substitute for PSI by operating in reverse to transfer electrons from plastoquinone to ferredoxin. Our findings reveal an unanticipated plasticity in the thylakoid electron transport network of cyanobacteria and compel a revision of existing models of oxygenic photosynthesis.

Bio-nanohybrid devices featuring natural photocatalysts bound to a nanostructure hold great promise in the search for sustainable energy conversion. One of the major challenges of integrating biological systems is protecting them against harsh environmental conditions while retaining, or ideally enhancing, their photophysical properties. In this mainly computational work we investigate an assembly of cyanobacterial photosystem I (PS I) embedded in a metal-organic framework (MOF), namely the zeolitic imidazolate framework ZIF-8. This complex has been reported experimentally [Bennett et al., Nanoscale Adv., 2019, 1, 94.] but so far the molecular interactions between PS I and the MOF remained elusive. We show via absorption spectroscopy that PS I remains intact throughout the encapsulation-release cycle. Molecular dynamics (MD) simulations further confirm that the encapsulation has no noticeable structural impact on the photosystem. However, the MOF building blocks frequently coordinate to the Mg²⁺ ions of chlorophylls in the periphery of the antenna complex. High-level quantum mechanical calculations reveal charge-transfer interactions, which affect the excitonic network and thereby may reversibly change the fluorescence properties of PS I. Nevertheless, our results highlight the stability of PS I in the MOF, as the reaction center remains unimpeded by the heterogeneous environment, paving the way for applications in the foreseeable future.