Self-generated environmental feedback drives traveling waves of gene expression in bacterial colonies

Bacterial colonies grow within microenvironments that they continuously reshape through nutrient uptake, metabolism and mechanical interaction. However, in colonies carrying engineered gene circuits, how these self-generated environmental changes feed back on gene expression to produce spatiotemporal organization remains poorly understood. Here we show that growth and gene expression are dynamically coupled during the maturation of founding colonies, with growth-driven environmental changes organizing gene expression into traveling waves. By combining quantitative time-lapse microscopy, mathematical modeling and image-based parameter inference, we demonstrate that edge-dominated colony expansion consistent with mechanical constraints on growth is followed by density-dependent growth arrest in which the total area occupied by colonies does not converge to a fixed carrying capacity of the shared growth environment. We then find that colonies form two distinct traveling waves of gene expression. An intra-colony wave emerges only after growth arrest and is observed in both constitutive genes and distinct regulated circuit architectures, indicating that it is not a result of circuit topology. Our observations are consistent with nutrient depletion during growth followed by subsequent recovery after growth arrest. At later times, an inter-colony wave emerges that is consistent with a colony-produced diffusible factor spreading through the shared medium. Together, these findings reveal that the colony environment is not a passive background but an active and intrinsic component of spatiotemporal gene regulatory dynamics, in which self-generated environmental feedback couples mechanical constraints, nutrient dynamics and gene expression across spatial scales.