Radial and Spiral Stream Formation in Proteus mirabilis Colonies

The enteric bacterium Proteus mirabilis, which is a pathogen that forms biofilms in vivo, can swarm over hard surfaces and form a variety of spatial patterns in colonies. Colony formation involves two distinct cell types: swarmer cells that dominate near the surface and the leading edge, and swimmer cells that prefer a less viscous medium, but the mechanisms underlying pattern formation are not understood. New experimental investigations reported here show that swimmer cells in the center of the colony stream inward toward the inoculation site and in the process form many complex patterns, including radial and spiral streams, in addition to previously-reported concentric rings. These new observations suggest that swimmers are motile and that indirect interactions between them are essential in the pattern formation. To explain these observations we develop a hybrid model comprising cell-based and continuum components that incorporates a chemotactic response of swimmers to a chemical they produce. The model predicts that formation of radial streams can be explained as the modulation of the local attractant concentration by the cells, and that the chirality of the spiral streams results from a swimming bias of the cells near the surface of the substrate. The spatial patterns generated from the model are in qualitative agreement with the experimental observations. Author Summary: Bacteria frequently colonize surfaces and grow as biofilm communities embedded in a gel-like polysaccharide matrix, and when this occurs on catheters, heart valves and other medical implants, it can lead to serious, hard-to-treat infections. Proteus mirabilis is an enteric bacterium that forms biofilms on urinary catheters, but in laboratory experiments it can swarm over hard surfaces and form a variety of spatial patterns. Understanding these patterns is a first step toward understanding biofilm formation, and here we describe new experimental results and mathematical models of pattern formation in Proteus. The experiments show that swimmer cells in the center of the colony stream inward toward the inoculation site and in the process form many complex patterns, including radial and spiral streams, in addition to concentric rings. To explain these observations we develop a model that incorporates a chemotactic response of swimmers to a chemical they produce. The model predicts that formation of radial streams can be explained as the modulation of the local attractant concentration by the cells, and that the chirality of the spiral streams can be predicted by incorporating a swimming bias of the cells near the surface of the substrate.