Spatiotemporal dynamics of bacterial collective migration

Abstract

Collective migration is a highly ordered collective behavior exhibited by species in response to a stimulus. Such behavior can help a population to gain a competitive advantage ahead of environmental changes. However, the process that shapes collective migration is complicated by the involvement of multiple factors, including genetics, phenotypic diversity, and the environment. In the last 50 years, mathematical models, computerized simulations, and quantitative experiments have all contributed to significant progress in the study of spatiotemporal dynamics in bacterial population migration. In this review, we first summarize the fundamental research on single-cell behavior of bacteria and collective migration, then overview recent work on the spatiotemporal dynamics of bacterial population migration and the applications of quantitative synthetic biology in collective migration research. Common bacteria such as Escherichia coli undergo random walks when grown in suspension in bulk liquid, consisting of successions of “runs” and “tumbles”. To find favorable environments for survival, bacteria process chemical stimuli by swimming towards (or away from) the sources of attractants (or repellents). Bacteria evaluate changes in signal concentrations by a well-characterized chemotaxis pathway, and then modulate the tumble frequency accordingly. Increasing levels of a chemoattractant decrease the tumble frequency, allowing the bacteria to approach the source of chemoattractant. Bacteria tend to live in groups in the natural environment and exhibit collective migration. Two forms of bacterial collective migration, chemotactic migration and swarming, have been extensively studied. In a capillary or semisolid medium containing a chemoattractant, the bacterial population consumes the attractant to form a gradient. Such a gradient attracts more bacteria to concentrate at the location of higher attractant concentration, allowing the population to re-establish the gradient. The attractant-consumption loop results in chemotactic collective migration of bacteria. By contrast, on the moist surface of a solid medium, highly compact bacteria swim on a thin layer above the surface to form a swarm. The population growth and collision between bacterial cells pushes the groups to expand and results in swarming. To understand the spatiotemporal dynamics of bacterial collective motion, mathematical models were developed together with single-cell tracking techniques. Based on the classic Keller-Segel model, which describes the macroscopic movement of chemotactic collective migration, recent studies have incorporated the chemotaxis pathway of single cells or have examined the effects of phenotypic diversity. The details of chemotactic collective migration in bacteria are becoming increasingly clear. Using another approach, recent studies of bacterial swarming combined the Vichek model of collective motion with fluid dynamics to reveal coordinated behaviors within the swarm. Furthermore, interactions between bacteria and physical obstacles were found to have significant impacts on bacterial motion. Developments in synthetic biology have provided tools to alter bacterial behavior through synthetic gene circuits. Scientists can then alter bacterial motility quantitatively to better understand bacterial collective migration, or to create collective patterns using specially designed gene circuits. These studies show great potential for the application of synthetic biology in studies of bacterial collective migration.