Redox cycling of extracellular electron shuttles can enable the metabolic activity of subpopulations within multicellular bacterial biofilms that lack direct access to electron acceptors or donors. How these shuttles catalyze extracellular electron transfer (EET) within biofilms without being lost to the environment has been a long-standing question. Here, we show that phenazines mediate efficient EET through interactions with extracellular DNA (eDNA) in Pseudomonas aeruginosa biofilms. Retention of pyocyanin (PYO) and phenazine carboxamide in the biofilm matrix is facilitated by eDNA binding. In vitro, different phenazines can exchange electrons in the presence or absence of DNA and can participate directly in redox reactions through DNA. In vivo, biofilm eDNA can also support rapid electron transfer between redox active intercalators. Together, these results establish that PYO:eDNA interactions support an efficient redox cycle with rapid EET that is faster than the rate of PYO loss from the biofilm.

细胞外电子穿梭的氧化还原循环可以使缺乏直接接触电子受体或供体的多细胞细菌生物膜内亚群的代谢活动成为可能。这些穿梭机如何在不丢失到环境中的情况下催化生物膜内的细胞外电子转移 (EET) 一直是一个长期存在的问题。在这里，我们表明吩嗪通过与铜绿假单胞菌生物膜中的细胞外 DNA (eDNA) 相互作用来介导有效的 EET 。eDNA 结合促进了绿脓素 (PYO) 和吩嗪甲酰胺在生物膜基质中的保留。在体外，不同吩嗪可以在DNA存在或不存在的情况下交换电子，并可以通过DNA直接参与氧化还原反应。体内，生物膜 eDNA 还可以支持氧化还原活性嵌入剂之间的快速电子转移。总之，这些结果表明 PYO:eDNA 相互作用支持有效的氧化还原循环，快速 EET 比 PYO 从生物膜中的损失速度更快。