Bioelectronic control of a microbial community using surface-assembled electrogenetic cells to route signals

• Published in: Nature nanotechnology Vol. 16; no. 6; pp. 688 - 697
• Main Authors: Terrell, Jessica L., Tschirhart, Tanya, Jahnke, Justin P., Stephens, Kristina, Liu, Yi, Dong, Hong, Hurley, Margaret M., Pozo, Maria, McKay, Ryan, Tsao, Chen Yu, Wu, Hsuan-Chen, Vora, Gary, Payne, Gregory F., Stratis-Cullum, Dimitra N., Bentley, William E.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.06.2021; Nature Publishing Group
• Subjects: 4-Butyrolactone - analogs & derivatives; 4-Butyrolactone - metabolism; 631/61; 631/61/350; 639/925; 639/925/350/1057; 639/925/350/59; beta-Galactosidase - metabolism; Bioelectricity; Cell interactions; Cell surface; Cells, Immobilized - chemistry; Chemical communication; Chemistry and Materials Science; Communication; Communications systems; Electrodes; Electronic systems; Electronics - methods; Equipment Design; Escherichia coli - genetics; Escherichia coli - metabolism; Escherichia coli Proteins - genetics; Escherichia coli Proteins - metabolism; Gene expression; Gene Expression Regulation, Bacterial; Gold - chemistry; Granulocyte-Macrophage Colony-Stimulating Factor - biosynthesis; Green Fluorescent Proteins - chemistry; Green Fluorescent Proteins - genetics; Green Fluorescent Proteins - metabolism; GTP-Binding Proteins - genetics; GTP-Binding Proteins - metabolism; Hydrogen Peroxide - metabolism; Materials Science; Microbiomes; Microbiota; Microorganisms; Microorganisms, Genetically-Modified - genetics; Microorganisms, Genetically-Modified - metabolism; Nanotechnology; Nanotechnology and Microengineering; Oxidation-Reduction; Quorum sensing; Real time; Repressor Proteins - genetics; Repressor Proteins - metabolism; Signal Transduction
• ISSN: 1748-3387; 1748-3395
• DOI: 10.1038/s41565-021-00878-4

We developed a bioelectronic communication system that is enabled by a redox signal transduction modality to exchange information between a living cell-embedded bioelectronics interface and an engineered microbial network. A naturally communicating three-member microbial network is ‘plugged into’ an external electronic system that interrogates and controls biological function in real time. First, electrode-generated redox molecules are programmed to activate gene expression in an engineered population of electrode-attached bacterial cells, effectively creating a living transducer electrode. These cells interpret and translate electronic signals and then transmit this information biologically by producing quorum sensing molecules that are, in turn, interpreted by a planktonic coculture. The propagated molecular communication drives expression and secretion of a therapeutic peptide from one strain and simultaneously enables direct electronic feedback from the second strain, thus enabling real-time electronic verification of biological signal propagation. Overall, we show how this multifunctional bioelectronic platform, termed a BioLAN, reliably facilitates on-demand bioelectronic communication and concurrently performs programmed tasks. Living electrodes enable signalling into a microbial community, coordinating behaviour.