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 (Synechococcus, Syne) 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., PsbA, PsbD, PsaA, and PsaB) and light-independent reactions (e.g., rbcL and rbcS) to increase CO₂ capture and fixation. Compared to untreated Syne cells, this biohybrid system, formed by treating Syne 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.