Directional reversals enableMyxococcus xanthuscells to produce collective one-dimensional streams during fruiting-body formation

Abstract

The formation of a collectively moving group benefits individuals within a population in a variety of ways. The surface-dwelling bacterium Myxococcus xanthus forms dynamic collective groups both to feed on prey and to aggregate during times of starvation. The latter behaviour, termed fruiting-body formation, involves a complex, coordinated series of density changes that ultimately lead to three-dimensional aggregates comprising hundreds of thousands of cells and spores. How a loose, two-dimensional sheet of motile cells produces a fixed aggregate has remained a mystery as current models of aggregation are either inconsistent with experimental data or ultimately predict unstable structures that do not remain fixed in space. Here, we use high-resolution microscopy and computer vision software to spatiotemporally track the motion of thousands of individuals during the initial stages of fruiting-body formation. We find that cells undergo a phase transition from exploratory flocking, in which unstable cell groups move rapidly and coherently over long distances, to a reversal-mediated localization into onedimensional growing streams that are inherently stable in space. These observations identify a new phase of active collective behaviour and answer a long-standing open question in Myxococcus development by describing how motile cell groups can remain statistically fixed in a spatial location.

Data-driven modeling reveals cell behaviors controlling self-organization during Myxococcus xanthus development

“…Previous observations indicated that cells increase their movement when aggregation initiates (20,22,23). To quantify these effects, the mean and 95% confidence intervals for distance, duration, and speed of persistent state runs were calculated in a 20-min sliding window over the length of the experiment (Fig.…”

“…Few data exist on the cues and cell behaviors that lead to these emergent behaviors. Cell-tracking experiments revealed that motility increases outside aggregates (20,22,23) and decreases inside (23, 24) whereas statistical image analysis revealed that the area of the aggregate solely determines whether an aggregate will disappear or mature into a fruiting body (19). On their own, Significance Coordinated cell movement is critical for a broad range of multicellular phenomena, including microbial self-organization, embryogenesis, wound healing, and cancer metastasis.…”

Low-noise phase of a two-dimensional active nematic system

“…Unlike its polar counterpart, where the appearance of macroscopic polar order results in collective directed motion or flocking [3,4], the active nematic involves driven apolar constituents, which means on average the system goes nowhere [5] making its properties far more subtle. Examples of active nematics include monolayers of melanocytes [6,7], fibroblasts [8], neural progenitors [9], myxobacteria [10,11], swimming filamentous bacteria [12][13][14], vibrated rods [15] and microtubule-kinesin suspensions [16].…”

Collective motion of bacteria in two dimensions

“…A similar function may be conferred by directional reversal in swarming of flagellated bacteria [17]. Notably, Myxobacteria were found to regulate reversal period using an internal biochemical clock when predating prey bacteria or during starvation [79], and the changes of reversal behavior lead to the formation of rippling waves [80], streams [81,82], as well as 3D fruiting bodies [83]. Short-ranged contact-mediated interactions are the primary interactions between gliding bacteria, as suggested by a number of cell-based biomechanical models that have successfully explained some key aspects of collective motion of gliding bacteria [59,77,81,[83][84][85][86][87][88].…”

“…For example, variation of directional reversal frequencies in Myxobacteria can change collective behavior from swarming to rippling [80] or to streaming [82]. On the other hand, models of self-propelled particle systems and active fluids suggest that behavioral parameters of individuals are often critical to collective dynamics [11,15,16,18] A growing number of techniques have become available to control the behavior of bacteria.…”