Extracellular DNA Promotes Efficient Extracellular Electron Transfer by Pyocyanin in Pseudomonas aeruginosa Biofilms

• Published in: Cell 2020-08, Vol.182 (4), p.919-932.e19
• Main Authors: Saunders, Scott H., Tse, Edmund C.M., Yates, Matthew D., Otero, Fernanda Jiménez, Trammell, Scott A., Stemp, Eric D.A., Barton, Jacqueline K., Tender, Leonard M., Newman, Dianne K.
• Format: Article
• Language: English
• Subjects: bacterial metabolism; biofilm; biofilm matrix; Biofilms - growth & development; DNA - chemistry; DNA - metabolism; DNA charge transfer; Electrochemical Techniques; Electrodes; Electron Transport - drug effects; extracellular DNA; extracellular electron transfer; Fluorescent Dyes - chemistry; Hydrogen-Ion Concentration; Oxidation-Reduction; phenazine; Phenazines - chemistry; Phenazines - metabolism; Phenazines - pharmacology; Pseudomonas aeruginosa; Pseudomonas aeruginosa - physiology; pyocyanin; Pyocyanine - chemistry; Pyocyanine - metabolism
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2020.07.006

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. [Display omitted] •PYO and PCN bind extracellular DNA, which facilitates their retention in biofilms•Electrode biofilms support fast PYO electron transfer and slow PYO loss•Phenazines rapidly exchange electrons and are capable of DNA charge transfer in vitro Phenazines are retained in biofilms through binding to extracellular DNA, and together these biofilm components mediate efficient extracellular electron transfer to support bacterial metabolism