The unique extracellular electron transfer (EET) ability has positioned electroactive bacteria (EAB) as a major class of cellular chassis for genetic engineering aimed at favorable environmental, energy, and geoscience applications. However, previous efforts to genetically enhance EET ability have often impaired the basal metabolism and cellular growth due to the competition for the limited cellular resource. Here, we design a quorum sensing-based population-state decision (PSD) system for intelligently reprogramming the EET regulation system, which allows the rebalanced allocation of the cellular resource upon the bacterial growth state. We demonstrate that the electron output from Shewanella oneidensis MR-1 could be greatly enhanced by the PSD system via shifting the dominant metabolic flux from initial bacterial growth to subsequent EET enhancement (i.e., after reaching a certain population-state threshold). The strain engineered with this system achieved up to 4.8-fold EET enhancement and exhibited a substantially improved pollutant reduction ability, increasing the reduction efficiencies of methyl orange and hexavalent chromium by 18.8- and 5.5-fold, respectively. Moreover, the PSD system outcompeted the constant expression system in managing EET enhancement, resulting in considerably enhanced electron output and pollutant bioreduction capability. The PSD system provides a powerful tool for intelligently managing extracellular electron transfer and may inspire the development of new-generation smart bioelectrical devices for various applications.

独特的细胞外电子转移（EET）能力已将电活性细菌（EAB）定位为基因工程的主要细胞底盘类别，旨在有利于环境，能源和地球科学的应用。然而，由于竞争有限的细胞资源，先前在遗传上增强EET能力的努力常常损害了基础代谢和细胞生长。在这里，我们设计了一种基于群体感应的种群状态决策（PSD）系统，用于智能地对EET调节系统进行重新编程，从而可以根据细菌的生长状态重新分配细胞资源。我们证明了Shewanella oneidensis的电子输出PSD系统可以通过将主要的代谢通量从最初的细菌生长转移到随后的EET增强（即，在达到一定的种群状态阈值之后）来大大增强MR-1。用该系统设计的菌株可实现高达4.8倍的EET增强，并显示出显着改善的污染物还原能力，从而使甲基橙和六价铬的还原效率分别提高了18.8和5.5倍。此外，PSD系统在管理EET增强方面胜过了恒定表达系统，从而显着增强了电子输出和污染物的生物还原能力。