Population oscillations, synchronization, and range expansion in a bacterial cross-protection mutualism

Abstract

Cooperation between microbes can enable microbial communities to survive in harsh environments. Enzymatic deactivation of antibiotics is a cooperative behavior that can allow resistant cells to protect sensitive cells from antibiotics. The prevalence of this mechanism of antibiotic resistance in clinical isolates and in soil bacteria makes it important both clinically and ecologically. Here, we show that two Escherichia coli strains can form a cross-protection mutualism, protecting each other in the presence of two antibiotics (ampicillin and chloramphenicol) so that the coculture can survive in antibiotic concentrations that inhibit growth of either strain alone. Moreover, we find that daily dilutions of the coculture lead to large oscillations in the relative abundance of the two strains, with the ratio of abundances varying by nearly four orders of magnitude over the course of the 3-day period of the oscillation. A simple mechanistic model is consistent with our experimental results. Next, we explore how this mutualism responds to a spatially structured environment where migration connects population patches. We find that intermediate migration rates maximize the probability of survival in harsh environments, whereas high migration rates lead to synchronization and thus risk simultaneous extinction. Interestingly, the increased stability is a result of the perturbed population dynamics that emerge in this regime, rather than ecological rescue. In addition, we explore the spatial expansion of the bacterial mutualism when subject to discrete space (a patchy environment) and discrete time (periodic growth cycles). Theoretical predictions suggest that range expansion of populations with an Allee effect (when average individual fitness increases with population size or density) in these conditions can exhibit pinning (inability to expand at low dispersal rates) and pulsed expansion (periodic or step-like expansion into new territory). Preliminary modeling and experimental results indicate that these phenomena can occur in our system. Our results may help elucidate the impact of migration on microbial population dynamics in spatially structured environments; more broadly, these studies may have implications on how migration influences large networks such as those studied in conservation biology and epidemiology.