Spatial dynamics of synthetic microbial hypercycles and their parasites

Abstract

Early theoretical work revealed that the simplest class of autocatalytic cycles, known as hypercycles, provide an elegant framework for understanding the evolution of mutualism. Furthermore, hypercycles are highly susceptible to parasites, spatial structure constituting a key protection against them. However, there is an insufficient experimental validation of these theoretical predictions, in addition to little knowledge on how environmental conditions could shape the spatial dynamics of hypercycles. Here, we constructed spatially extended hypercycles by using synthetic biology as a way to design mutualistic and parasitic {\em E. coli} strains. A mathematical model of the hypercycle front expansion is developed, providing analytic estimates of front speed propagation. Moreover, we explore how the environment affects the mutualistic consortium during range expansions. Interestingly, moderate improvements in environmental conditions (namely, increasing the availability of growth-limiting amino acids) can lead to a slowing-down of the front speed. Our agent-based simulations suggest that opportunistic depletion of environmental amino acids can lead to subsequent high fractions of stagnant cells at the front, and thus to the slow-down of the front speed. Moreover, environmental deterioration can also shape the interaction of the parasitic strain towards the hypercycle. On the one hand, the parasite is excluded from the population during range expansions in which the two species mutualism can thrive (in agreement with a classical theoretical prediction). On the other hand, environmental deterioration (e.g., associated with toxic chemicals) can lead to the survival of the parasitic strain, while reshaping the interactions within the three-species. The evolutionary and ecological implications for the design of synthetic consortia are outlined.