Intracellular–Extracellular Synergistic Biohybrid System Boosts Photosynthetic Carbon Fixation

Biotic-abiotic hybrid systems offer a promising approach for converting CO₂ into energy-rich organic matter and addressing rising CO₂ levels. Prevailing research indicates that intracellular or extracellular biomineralization enhances photosynthesis and carbon fixation, with limited attention to the potential and mechanisms of intracellular-extracellular synergy. Here, we report that electroactive cyanobacteria (<i>Synechococcus</i>, <i>Syne</i>) construct an intracellular-extracellular synergistic biohybrid system by biomineralizing Zn(II) into intracellular Zn(II)-OM and extracellular ZnO-OM. The photoexcited electrons from ZnO-OM transfer to the photosynthetic electron transport chain and promote photosynthesis in this biohybrid system. Meanwhile, Zn(II)-OM plays essential roles in photosynthesis and cellular metabolism, upregulating key genes involved in light-dependent reactions (e.g., <i>PsbA</i>, <i>PsbD</i>, <i>PsaA</i>, and <i>PsaB</i>) and light-independent reactions (e.g., <i>rbcL</i> and <i>rbcS</i>) to increase CO₂ capture and fixation. Compared to untreated <i>Syne</i> cells, this biohybrid system, formed by treating <i>Syne</i> cells with Zn(II), exhibits a combined 120.9% increase in protein and lipid production efficiency. This work reveals the complexity of biomineralization both intracellularly and extracellularly, proposes the concept of an intracellular-extracellular synergistic biohybrid system that boosts photosynthetic carbon fixation, and provides comprehensive insights into the mechanisms of self-assembled hybrid systems.