Accelerating cell division of Shewanella oneidensis to promote extracellular electron transfer rate for efficient pollution treatment

The slow rate of extracellular electron transfer (EET) of electroactive microorganisms (EAMs) remains a predominate bottleneck that restricts practical applications of bio-electrochemical systems. Cell division has significant effects on cell cycle, morphology, growth and metabolism. However, the relation between cell division and the EET rate of Shewanella oneidensis has not been established. Here, we employed modular engineering strategy to accelerate DNA replication in the C period and divisome formation in the D period of cell cycle, which decreased cellular volume and enhanced the EET efficiency. Assembly of the C and D period modules further decreased the cell volume by 82.0 % and enhanced power density by 3.12-fold. Electrophysiological and transcriptomic analyses synergistically revealed that the programmed cell volume decrease facilitated lactate uptake and cellular metabolism due to the increased specific surface area (SSA), which consequently reinforced intracellular electron generation. Moreover, the reduced cell size facilitated electroactive biofilm formation. Furthermore, programmed increase in riboflavin biosynthesis and transport further strengthened indirect EET and boosted output power density to 1537.8 ± 116.9 mW m−2, 21.1-fold of that of the WT. The engineered strains exhibited superior abilities for Cr6+ reduction and azo dyes degradation. This study shed light on the underlying mechanism how reduced cell size impacts electrophysiology of EAMs, and indicated accelerating cell division is a promising avenue to increase the EET of EAMs for efficient environmental pollution treatment.