Abstract
Bacteria often live in complex communities in which they interact with other organisms. Soil microbial communities are responsible for important ecological functions, such as nutrient cycling, soil fertility, and plant health. The wealth of studies on microbial communities has revealed the complexity and dynamics of the composition of communities in many ecological settings. However, we lack a mechanistic understanding of interspecies interactions within these communities. The study of community interactions is essential for gaining a more holistic understanding of microbial community functions, as these functions may not be fully revealed by characterizing the individuals. Consideration of the social environment of bacteria can uncover emergent traits and behaviors that would be overlooked by studying bacteria in isolation. Here we characterize a behavior which emerges upon interaction between the distantly related soil bacteria Pseudomonas fluorescens Pf0-1 and Pedobacter sp. strain V48. Our experimental settings are not permissive for motility of either species, but co-culture reveals an emergent phenotype we term ‘interspecies social spreading,’ where the mixed colony spreads across a hard agar surface. Investigation of this interaction revealed that (1) initiation of social spreading requires close association between the two species of bacteria, and both species remain associated throughout the spreading colony, with reproducible and non-homogenous patterns of distribution, (2) The phenotype is prevalent among related isolates, and we have found interactions mediated by diffusible signals, (3) Pseudomonas flagella are part of the motility mechanism underlying social spreading, (4) Environmental factors influence the decision to engage in social spreading, as high-nutrient conditions preclude emergence of the phenotype, but low-nutrient conditions are insufficient to promote social spreading without high salt concentrations, and (5) Pedobacter mutants that have evolved the ability to spread faster in coculture likely overproduce exopolysaccharides, which could hydrate the local environment of the spreading colony, and can potentiate evolution of the Pseudomonas partner to further enhance motility. This simple two-species consortium provides a tractable model system that will facilitate mechanistic investigations of interspecies interactions and provide insight into emergent properties of communities of interacting species. Observation of emergent traits suggests there may be many functions of a community that are not predicted based on a priori knowledge of the individual community members. This research will enable us to connect information about community composition with behaviors determined by interspecific interactions, contributing to the broader knowledge of how bacterial interactions influence the functions of communities they inhabit. Ultimately, these studies will provide a more holistic understanding of microbial communities in natural environments.