Breathe in, breathe out: Bacterial density determines collective migration in aerotaxis

Abstract

Bacteria navigate their environment by biasing their swimming direction toward beneficial chemicals and away from harmful ones. Out of all the chemicals bacteria respond to, oxygen stands out due to its ubiquitous presence, distinct influence on bacterial metabolism and motility, and historical role in chemotaxis research. However, a coherent understanding of bacterial motility in oxygen gradients, known as aerotaxis, remains elusive, as evidenced by conflicting reports on the migration direction of the model organism Escherichia coli in self-generated oxygen gradients. Here, by combining experiments, simulations, and theory, we provide a unified framework elucidating the fundamental biophysical principle governing bacterial aerotaxis. We track the migration of bacteria in a capillary channel under self-generated oxygen gradients and show that the migration direction depends on the overall bacterial density. At high densities, bacteria migrate toward regions of higher oxygen concentration, whereas at low densities, they move in the opposite direction. We identify a critical bacterial density at which collective migration ceases, despite the presence of oxygen gradients. A kinetic theory, based on the assumption that bacteria seek an optimal oxygen concentration, is then developed to quantitatively explain our experimental findings. We validate this hypothesis by demonstrating the biased movement of individual bacteria in a dense suspension and proposing a signaling pathway that enables this behavior. Thus, by bridging the molecular level understanding of the signaling pathway, the motility of single bacteria in oxygen gradients, and the collective population dynamics shaped by oxygen diffusion and consumption, our study provides a comprehensive understanding of aerotaxis, addressing the long-standing controversy over how bacteria response to non-uniform oxygen distributions pervasive in microbial habitats.