Cooperation controls partners spatial intermixing in a synthetic bacterial consortium

Abstract

Microbes are essential actors in all environments (nutrients cycling, pollutants bioremediation, and more), and their functions depend on multispecies communities that possess intricate interspecies interactions and high degree of spatial organization. Due to the complexity of natural microbial systems, mechanistic understanding of community spatial assembly and activity remains fragmentary. Here, we used a synthetic ecology approach to ask how simple factors such as carbon utilization control spatial patterns of a two-partner bacterial consortium grown on surfaces. The experimental model consortium consisted of two mutant strains of Pseudomonas putida that cooperate to degrade and utilize toluene. Strains tagging with different autofluorescent proteins allowed for microscopic visualization and pattern quantification by image analysis. We showed that trophic cooperation (toluene degradation) led to convergence of partner abundance (1:1) regardless of the initial ratio, and to strong strain intermixing at the microscale (10-100 m). In contrast, competition for a carbon source (benzoate) degraded independently by both strains resulted in distinct segregation patterns. The consortium productivity (cell growth) on toluene was affected by the initial partner ratio on surfaces but not in liquid cultures. This study pinpoints general principles of microbial community spatial organization with potential applications for natural and engineered microbial systems.