Abstract Ecosystem processes result from interaction between organisms. When interactions are local, the spatial organization of organisms defines their network of interactions, and thus influences the system’s functioning. This can be especially relevant for microbial systems, which often consist of spatially structured communities of cells connected by a dense interaction network. Here we measured the spatial interaction network between cells in microbial systems and identify the factors that determine it. Combining quantitative single-cell analysis of synthetic bacterial communities with mathematical modeling, we find that cells only interact with other cells in their immediate neighbourhood. This short interaction range impacts the functioning of the whole system by reducing its ability to perform metabolic processes collectively. Our experiments and models demonstrate that the spatial scale of cell-to-cell interaction plays a fundamental role in understanding and controlling natural communities, and in engineering microbial systems for specific purposes. Significance Statement Communities of interacting microbes perform fundamental processes on earth. We do not understand well how these processes emerge from the interactions between individual microbial cells. Our work investigates how strongly individual cells interact and how the strength of the interaction depends on the distance between cells. The discovery that individual cells ‘live in a small world’, i.e. they only interact with a small number of cells around them, changes our understanding of how cells in natural microbial communities are metabolically coupled and how their spatial arrangement determines emergent properties at the community level. Our quantitative single-cell approach allows to address central questions on systems composed of interacting genotypes and to increase our understanding and ability to control microbial communities.

Short-range interactions govern cellular dynamics in microbial multi-genotype systems