Cell-to-cell bacterial interactions promoted by drier conditions on soil surfaces

Bacterial cell-to-cell interactions are in the core of evolutionary and ecological processes in soil and other environments. Under most conditions, natural soils are unsaturated where the fragmented aqueous habitats and thin liquid films confine bacterial cells within small volumes and close proximity for prolonged periods. We report effects of a range of hydration conditions on bacterial cell-level interactions that are marked by plasmid transfer between donor and recipient cells within populations of the soil bacterium Pseudomonas putida. Using hydration-controlled sand microcosms, we demonstrate that the frequency of cell-to-cell contacts under prescribed hydration increases with lowering water potential values (i.e., under drier conditions where the aqueous phase shrinks and fragments). These observations were supported using a mechanistic individual-based model for linking macroscopic soil water potential to microscopic distribution of liquid phase and explicit bacterial cell interactions in a simplified porous medium. Model results are in good agreement with observations and inspire confidence in the underlying mechanisms. The study highlights important physical factors that control short-range bacterial cell interactions in soil and on surfaces, specifically, the central role of the aqueous phase in mediating bacterial interactions and conditions that promote genetic information transfer in support of soil microbial diversity.