Contact-dependent communication shapes the mesoscale spatial organization of bacterial swarms

Abstract

Scientists use microscopy images to visualize and describe organisms and their interactions. Microscale visual inspections of individual cells and colonies, paired with genetic approaches, have revealed key developmental steps within microbial communities including, for example, swarms, biofilms, and fruiting bodies. However, there is a lack of formal, quantitative descriptions of these structures. This gap limits understanding of the structure and relevance of cell clusters, especially regarding development and interactions. Here, we develop biologically informed mathematical methods to formally assess cell clusters that assemble and dissolve over time in bacterial colonies. Our approaches to this analysis of the developmental stages of swarming, a type of collective migration, focus on cell length (as a proxy for developmental stage), cell-to-cell contacts, and groupings. We apply these to data from Proteus mirabilis strains with genetic disruptions in different aspects of its communication mechanisms to explore how identity signaling and cell-to-cell contact affect population structure at different scales. We found that kin recognition and contact-dependent, cell-cell communication govern population architecture during collective migration, such as swarming. This integration of microbiology with applied mathematics and computer science is a frontier for analyzing experimental data, leading to testable biological insights. SignificanceCollective behaviors are often exhibited by social organisms. Open questions regarding these behaviors include: how do communication and familial identity influence local interactions, and how do local interactions combine to create collective behaviors? Qualitative descriptions from visual examination of microbes can be useful in approaching these questions, but formal quantification of these structures will be essential if we are to understand the mechanisms that underlie organismal behavior and organization. This manuscript bridges microbiology and applied mathematics, interleaving the mathematics and the experiments in an iterative fashion. We offer critical advances to better understand, analyze, and characterize the multiscale structures that form and dissolve as a colony engages in collective migration. Our findings suggest that cell-cell communication plays an important role in population architecture, specifically that communication may "prime" cells for collective migration and prevent stagnation during life stage transitions.