Evolving a plant-beneficial bacterium in soil vs. nutrient-rich liquid culture has contrasting effects on in-soil fitness.

Inoculation of plant-beneficial microbes into agricultural soils can improve crop growth, but such outcomes depend on microbial survival. Here, we assessed how exposure to prior environmental conditions impacts microbial in-soil fitness, particularly focusing on incubation in liquid culture as an unavoidable phase of inoculant production and on pre-incubation in target soils as a potential method to improve performance. We conducted experimental evolution on a phosphorus-solubilizing bacterial species, IMPORTANCE: Innovative solutions are needed to address emerging challenges in agriculture while reducing its environmental footprint. Management of soil microbiomes could contribute to this effort, as plant growth-promoting microorganisms provide key ecosystem services that support crops. Yet, inoculating beneficial microbes into farm soils yields unreliable results. We require a greater knowledge of the ecology of these taxa to improve their functioning in sustainable agroecosystems. In this report, we demonstrate that exposure to laboratory media and lingering adaptation to another soil can negatively impact the in-soil survival of a phosphorus-solubilizing bacterial species. We go further to highlight the underlying mutations that give rise to these patterns. These insights can be leveraged to improve our understanding of how soil-dwelling beneficial microorganisms adapt to different evolutionary pressures.