Redox-enabled electronic interrogation and feedback control of hierarchical and networked biological systems

• Published in: Nature communications 2023-12, Vol.14 (1), p.8514-8514, Article 8514
• Main Authors: Wang, Sally, Chen, Chen-Yu, Rzasa, John R., Tsao, Chen-Yu, Li, Jinyang, VanArsdale, Eric, Kim, Eunkyoung, Zakaria, Fauziah Rahma, Payne, Gregory F., Bentley, William E.
• Format: Article
• Language: English
• Subjects: 14/19; 14/35; 38/22; 38/23; 38/35; 38/39; 38/44; 38/77; 38/88; 38/90; 631/61/185; 631/61/350; 631/80/86; 639/301/54; 639/925/350/1057; Algorithms; Biology; Chemical communication; Closed loops; Consortia; Control systems; Data transmission; E coli; Electrodes; Electronic control; Electronics; Enzymatic activity; Enzyme activity; Escherichia coli - genetics; Escherichia coli - metabolism; Feedback; Feedback control; Gene expression; Horseradish peroxidase; Humanities and Social Sciences; Hydrogen peroxide; Interrogation; multidisciplinary; Oxidation-Reduction; Peroxidase; Proteins; Proteins - metabolism; Quorum sensing; Real time; Redox reactions; Science; Science (multidisciplinary); Synthetic biology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-023-44223-w

Microelectronic devices can directly communicate with biology, as electronic information can be transmitted via redox reactions within biological systems. By engineering biology’s native redox networks, we enable electronic interrogation and control of biological systems at several hierarchical levels: proteins, cells, and cell consortia. First, electro-biofabrication facilitates on-device biological component assembly. Then, electrode-actuated redox data transmission and redox-linked synthetic biology allows programming of enzyme activity and closed-loop electrogenetic control of cellular function. Specifically, horseradish peroxidase is assembled onto interdigitated electrodes where electrode-generated hydrogen peroxide controls its activity. E. coli ’s stress response regulon, oxyRS , is rewired to enable algorithm-based feedback control of gene expression, including an eCRISPR module that switches cell-cell quorum sensing communication from one autoinducer to another—creating an electronically controlled ‘bilingual’ cell. Then, these disparate redox-guided devices are wirelessly connected, enabling real-time communication and user-based control. We suggest these methodologies will help us to better understand and develop sophisticated control for biology. With redox-linked synthetic biology and electrobiofabrication, electronic information can be transmitted in a bidirectional manner between biology and electronics. Here the authors design an electrogenetic platform that allows real time electronic control of biological functions from proteins and gene circuits to cell consortia.