Dynamic switching enables efficient bacterial colonization in flow

Significance Bacteria colonize surfaces and form dense biofilm communities in natural and infection settings where flow is present. The physical mechanisms that give rise to the spatial organization of biofilms in flow are not understood. Here, we show that the bacterium Pseudomonas aeruginosa uses a process that we have termed dynamic switching to efficiently disperse throughout a flow network and maximize spatial colonization. This process dictates the spatial organization of cells during the transition from individual cells to multicellular biofilm communities. Thus, dynamic switching establishes the initial organizational structure of biofilms. The motion of many eukaryotic cell types can be described by dynamic switching, which suggests a general role of this process in a broad range of cellular systems. Bacteria colonize environments that contain networks of moving fluids, including digestive pathways, blood vasculature in animals, and the xylem and phloem networks in plants. In these flow networks, bacteria form distinct biofilm structures that have an important role in pathogenesis. The physical mechanisms that determine the spatial organization of bacteria in flow are not understood. Here, we show that the bacterium P. aeruginosa colonizes flow networks using a cyclical process that consists of surface attachment, upstream movement, detachment, movement with the bulk flow, and surface reattachment. This process, which we have termed dynamic switching, distributes bacterial subpopulations upstream and downstream in flow through two phases: movement on surfaces and cellular movement via the bulk. The model equations that describe dynamic switching are identical to those that describe dynamic instability, a process that enables microtubules in eukaryotic cells to search space efficiently to capture chromosomes. Our results show that dynamic switching enables bacteria to explore flow networks efficiently, which maximizes dispersal and colonization and establishes the organizational structure of biofilms. A number of eukaryotic and mammalian cells also exhibit movement in two phases in flow, which suggests that dynamic switching is a modality that enables efficient dispersal for a broad range of cell types.