Chemotactic smoothing of collective migration

Elife. 2022 Mar 8:11:e71226. doi: 10.7554/eLife.71226.

Abstract

Collective migration-the directed, coordinated motion of many self-propelled agents-is a fascinating emergent behavior exhibited by active matter with functional implications for biological systems. However, how migration can persist when a population is confronted with perturbations is poorly understood. Here, we address this gap in knowledge through studies of bacteria that migrate via directed motion, or chemotaxis, in response to a self-generated nutrient gradient. We find that bacterial populations autonomously smooth out large-scale perturbations in their overall morphology, enabling the cells to continue to migrate together. This smoothing process arises from spatial variations in the ability of cells to sense and respond to the local nutrient gradient-revealing a population-scale consequence of the manner in which individual cells transduce external signals. Altogether, our work provides insights to predict, and potentially control, the collective migration and morphology of cellular populations and diverse other forms of active matter.

Keywords: E. coli; chemotaxis; collective migration; computational biology; motility; physics of living systems; systems biology.

Plain language summary

Flocks of birds, schools of fish and herds of animals are all good examples of collective migration, where individuals co-ordinate their behavior to improve survival. This process also happens on a cellular level; for example, when bacteria consume a nutrient in their surroundings, they will collectively move to an area with a higher concentration of food via a process known as chemotaxis. Several studies have examined how disturbing collective migration can cause populations to fall apart. However, little is known about how groups withstand these interferences. To investigate, Bhattacharjee, Amchin, Alert et al. studied bacteria called Escherichia coli as they moved through a gel towards nutrients. The E. coli were injected into the gel using a three-dimensional printer, which deposited the bacteria into a wiggly shape that forces the cells apart, making it harder for them to move as a collective group. However, as the bacteria migrated through the gel, they smoothed out the line and gradually made it straighter so they could continue to travel together over longer distances. Computer simulations revealed that this smoothing process is achieved by differences in how the cells respond to local nutrient levels based on their position. Bacteria towards the front of the group are exposed to more nutrients, causing them to become oversaturated and respond less effectively to the nutrient gradient. As a result, they move more slowly, allowing the cells behind them to eventually catch-up. These findings reveal a general mechanism in which limitations in how individuals sense and respond to an external signal (in this case local nutrient concentrations) allows them to continue migrating together. This mechanism may apply to other systems that migrate via chemotaxis, as well as groups whose movement is directed by different external factors, such as temperature and light intensity.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Bacteria
  • Chemotaxis / physiology
  • Escherichia coli* / physiology
  • Models, Biological*

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.