Nutrient-rich spatial refuges buffer against extinction and promote evolutionary rescue in evolving microbial populations

Microbial populations are often exposed to long-term abiotic disturbances, which can reduce population viability and cause local extinction. Eco-evolutionary theory suggests that spatial refuges can facilitate persistence and evolutionary rescue. However, one drawback of spatial refuges is reduced exposure to nutrients such as carbon and oxygen, suggesting the protective effect of refuges depends on the interplay between environmental conditions and the degree of stress. Here, we test this general idea using mathematical modelling, and experimental evolution of the model bacterium Pseudomonas fluorescens SBW25 under salinity stress. As our model predicted, we find that the ability of spatial refuges to rescue evolving populations from extinction crucially depends on nutrient availability. Populations evolving under salinity stress where nutrient-rich spatial refuges were available, harboured clones that displayed enhanced salt resistance, indicating that nutrient-rich spatial refuges can facilitate evolutionary rescue. Furthermore, while control-salinity-evolved populations adapted to spatial structure by evolving enhanced motility (likely through parallel mutations in PFLU_4551, a predicted aerotaxis response regulator), this phenotype was constrained under high salinity, because increased motility negates the benefits of a spatial refuge. Our results reveal a general interplay between spatial refuges and nutrient availability that could be leveraged to reduce extinction risk in natural populations.