Habitat Adaptation Drives Speciation of a Streptomyces Species with Distinct Habitats and Disparate Geographic Origins

Microbial diversification is driven by geographic and ecological factors, but how the relative importance of these factors varies among species, geographic scales, and habitats remains unclear. Streptomyces, a genus of antibiotic-producing, spore-forming, and widespread bacteria, offers a robust model for identifying the processes underlying population differentiation. We examined the population structure of 37 Streptomyces olivaceus strains isolated from various sources, showing that they diverged into two habitat-associated (free-living and insect-associated) and geographically disparate lineages. More frequent gene flow within than between the lineages confirmed genetic isolation in S. olivaceus. Geographic isolation could not explain the genetic isolation; instead, habitat type was a strong predictor of genetic distance when controlling for geographic distance. The identification of habitat-specific genetic variations, including genes involved in regulation, resource use, and secondary metabolism, suggested a significant role of habitat adaptation in the diversification process. Physiological assays revealed fitness trade-offs under different environmental conditions in the two lineages. Notably, insect-associated isolates could outcompete free-living isolates in a free-iron-deficient environment. Furthermore, substrate (e.g., sialic acid and glycogen) utilization but not thermal traits differentiated the two lineages. Overall, our results argue that adaptive processes drove ecological divergence among closely related streptomycetes, eventually leading to dispersal limitation and gene flow barriers between the lineages. S. olivaceus may best be considered a species complex consisting of two cryptic species.