Division of Biology and Biological Engineering, Caltech, Pasadena, CA, USA.
Division of Chemistry and Chemical Engineering, Caltech, Pasadena, CA, USA; Department of Chemistry, University of Hong Kong, Hong Kong SAR, China.
Cell. 2020 Aug 20;182(4):919-932.e19. doi: 10.1016/j.cell.2020.07.006. Epub 2020 Aug 6.
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电子受体或供体的多细胞细菌生物膜内的亚群具有代谢活性。这些穿梭物如何在不向环境中损失的情况下在生物膜内催化细胞外电子转移 (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 结合促进了生物膜基质中绿脓菌素 (PYO) 和吩嗪羧酰胺的保留。在体外,不同的吩嗪可以在有或没有 DNA 的情况下交换电子,并且可以直接通过 DNA 参与氧化还原反应。在体内,生物膜 eDNA 还可以支持在氧化还原活性嵌入剂之间进行快速电子转移。总之,这些结果表明 PYO:eDNA 相互作用支持快速 EET 的有效氧化还原循环,其速度比 PYO 从生物膜中损失的速度还要快。