Weak synchronization and large-scale collective oscillation in dense bacterial suspensions

Abstract

Collective oscillatory behaviour is ubiquitous in nature, having a vital role in many biological processes from embryogenesis and organ development to pace-making in neuron networks. Elucidating the mechanisms that give rise to synchronization is essential to the understanding of biological self-organization. Collective oscillations in biological multicellular systems often arise from long-range coupling mediated by diffusive chemicals, by electrochemical mechanisms, or by biomechanical interaction between cells and their physical environment. In these examples, the phase of some oscillatory intracellular degree of freedom is synchronized. Here, in contrast, we report the discovery of a weak synchronization mechanism that does not require long-range coupling or inherent oscillation of individual cells. We find that millions of motile cells in dense bacterial suspensions can self-organize into highly robust collective oscillatory motion, while individual cells move in an erratic manner, without obvious periodic motion but with frequent, abrupt and random directional changes. So erratic are individual trajectories that uncovering the collective oscillations of our micrometre-sized cells requires individual velocities to be averaged over tens or hundreds of micrometres. On such large scales, the oscillations appear to be in phase and the mean position of cells typically describes a regular elliptic trajectory. We found that the phase of the oscillations is organized into a centimetre-scale travelling wave. We present a model of noisy self-propelled particles with strictly local interactions that accounts faithfully for our observations, suggesting that self-organized collective oscillatory motion results from spontaneous chiral and rotational symmetry breaking. These findings reveal a previously unseen type of long-range order in active matter systems (those in which energy is spent locally to produce non-random motion). This mechanism of collective oscillation may inspire new strategies to control the self-organization of active matter and swarming robots.

Collective motion of bacteria and their dynamic assembly behavior

“…Chen et al [41] found that with increasing bacterial concentration the velocity of E. coli within the plane exhibited a weak synchronization behavior, which lasted at least half an hour. It is interesting that the probability of quasi clockwise movement in different colonies is almost equal.…”

Coupling between distant biofilms and emergence of nutrient time-sharing

“…Specifically, we modeled the biofilms as two coupled phase oscillators (20–24) to represent their growth dynamics (fig. S3 and supplementary text).…”

The 3D architecture of a bacterial swarm has implications for antibiotic tolerance

“…Swarming not only helps bacteria to colonize new niches, but has also been demonstrated to facilitate their survival on antibiotic concentrations that are lethal to the same bacteria while swimming in liquid 15–19 . Dense suspensions of swimming bacteria, obtained by artificially concentrating the cells to high volume fractions, exhibit collective motion as well 20–26 , but these bacteria are not equivalent to the swarm collective because swarming bacteria have an altered physiology 5,6 . How bacteria move within the swarm, if they respond to chemical gradients, and whether their motion contributes to their survival, is poorly understood compared to their swimming counterparts.…”