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.