Hitchhiking, collapse and contingency in phage infections of migrating bacterial populations

Abstract

Natural bacterial populations are subject to constant predation pressure by phages. Bacteria use a variety of well-studied molecular mechanisms to defend themselves from phage predation. However, since phage are non-motile, perhaps the simplest defense against phage would be for bacteria to outrun their predators. In particular, chemotaxis, the active migration of bacteria up attractant gradients, may help the bacteria escape slowly diffusing phages. Here we study phage infection dynamics in migrating bacterial populations driven by chemotaxis through low viscosity agar plates. We find that expanding phage-bacteria populations support two migrating fronts, an outermost “bacterial” front driven by nutrient uptake and chemotaxis and an inner “phage” front at which bacterial population collapses due to phage predation. We show that with increasing adsorption rate and initial phage population, the rate of migration of the phage front increases, eventually overtaking the bacterial front and driving the system across a “phage transition” from a regime where bacteria outrun a phage infection to one where they must evolve phage resistance to survive. We confirm experimentally that this process requires phages to “surf” the bacterial front by repeatedly reinfecting the fastest moving bacteria. A deterministic model recapitulates the transition. Macroscopic fluctuations in bacterial densities at the phage front suggest that a feedback mechanism, possibly due to growth rate dependent phage infection rates, drives millimeter scale spatial structure in phage-bacteria populations. Our work opens a new, spatiotemporal, line of investigation into the eco-evolutionary struggle between bacteria and their phage predators.