Quorum-Sensing-Mediated Extracellular Electron Transfer Enables Hydrogel Morphogenesis

Abstract

Engineered living materials seek to capture the sensitivity, responsiveness, and programmable characteristics of biological systems. One emergent property of living systems is genetically driven spatial patterning, which controls cell differentiation and the development of complex multicellular organisms. Inspired by this capability, we use bacteria to spatially control material assembly. In our system, extracellular electron transfer (EET) flux from Shewanella oneidensis drives hydrogel synthesis via copper-catalyzed radical polymerization. We first construct a recombinant quorum sensing system in S. oneidensis that allows for cell-cell communication between "sender" and "receiver" cells through an autoinducer. We then examine controlled gene expression and EET-driven chemical transformation in various synthetic consortia. Via diffusion through agarose, we examine 2D patterns of gene expression relative to localized sender cell populations and demonstrate controlled hydrogel crosslinking in predictable patterns. Finally, we apply computational methods and NOT logic in "receiver" cells towards more complex patterns of gene expression. Our results highlight the potential of bacteria to program material systems with life-like properties including self-assembly, environmental responsiveness, and patterned differentiation.