Adaptive benefits of motility in cross-feeding mutualisms

Cross-feeding mutualisms, in which partner species exchange essential metabolites, are ubiquitous in microbial communities. In spatially structured environments, motility can improve access to partner-produced resources but also impose metabolic costs and displace cells from nutrient-rich regions, so its net benefit depends on the spatial dynamics of the interaction. Here, we combine competition experiments in a cross-feeding mutualism between Escherichia coli and Salmonella enterica with a spatially explicit consumer-resource model to determine what drives selection on motility. Spatial structure imposes asymmetric selection between partners i.e. S. enterica benefits from motility regardless of partner motility, whereas selection on E. coli switches from favourable to unfavourable depending on whether its partner can move. Competition in well-mixed culture suggests that this reversal reflects the loss of a spatial benefit rather than an increased cost. Our model attributes the asymmetry to three interacting factors: the ratio of metabolite production to consumption which sets whether the cross-fed resource is scarce or abundant; the number of growth-limiting resources which determines whether an alternative gradient can rescue the benefit of motility; and partner motility and growth rate, which shape where metabolites are produced. When a metabolite is scarce, motile cells gain by dispersing into regions it has reached but not yet been depleted from. When it accumulates, this gradient is eroded, and the motility costs offset any benefit it provides. Selection on motility therefore depends on the metabolic structure of the interaction and the spatial behaviour of partners.