Motile subpopulations in microbial communities are believed to be important for dispersal, quest for food, and material transport. Here, we show that motile cells in sessile colonies of peritrichously flagellated bacteria can self-organize into two adjacent, centimeter-scale motile rings surrounding the entire colony. The motile rings arise from spontaneous segregation of a homogeneous swimmer suspension that mimics a phase separation; the process is mediated by intercellular interactions and shear-induced depletion. As a result of this self-organization, cells drive fluid flows that circulate around the colony at a constant peak speed of ~30 µm s-1, providing a stable and high-speed avenue for directed material transport at the macroscopic scale. Our findings present a unique form of bacterial self-organization that influences population structure and material distribution in colonies.