Scale-dependent tipping points of bacterial colonization resistance

Abstract

Bacteria are efficient colonizers of a wide range of secluded microhabitats, such as soil pores, skin follicles, or intestinal crypts. How the structural diversity of these habitats modulates microbial self-organization remains poorly understood, in part because of the difficulty to precisely manipulate the physical structure of microbial environments. Using a microfluidic device to grow bacteria in crypt-like incubation chambers of systematically varied lengths, we show that small variations in the physical structure of the microhabitat can drastically alter bacterial colonization success and resistance against invaders. Small crypts are uncolonizable; intermediately sized crypts can stably support dilute populations, while beyond a second critical length scale, populations phase separate into a dilute region and a jammed region. The jammed state is characterized by extreme colonization resistance, even if the resident strain is suppressed by an antibiotic. Combined with a flexible biophysical model, we demonstrate that colonization resistance and associated priority effects can be explained by a crowding-induced phase transition, which results from a competition between proliferation and density-dependent cell leakage. The emerging sensitivity to scale underscores the need to control for scale in microbial ecology experiments. Systematic flow-adjustable length-scale variations may serve as a promising strategy to elucidate further scale-sensitive tipping points and to rationally modulate the stability and resilience of microbial colonizers.

Ecological Stability Emerges at the Level of Strains in the Human Gut Microbiome

“…How and why closely related strains coexist in the human gut are two of the central biological questions raised by our results. Spatial segregation between strains, perhaps occupying different colonic crypts, or partitioning luminal and mucosal niches, could contribute to the observed pattern of strain coexistence ( 44 – 46 ), much as it does among Cutibacterium acnes strains inhabiting different pores on the facial microbiome ( 25 ). However, the spatial structure is far from the only mechanism that can foster coexistence between strains.…”

Self-consistent dispersal puts tight constraints on the spatiotemporal organization of species-rich metacommunities

“…This allows us to use much more specific spatiotemporal data to verify or falsify our model and to test the proximity of species to global extinction. It will further be interesting to apply our theoretical approach to experiments specifically designed to disentangle colonization and local competition in metacommunities, such as recently proposed with coupled microfluidic chambers ( 94 ).…”

Proliferating active matter

“…However, proliferation can also induce phase separation even when cells are only passively diffusing, provided they are near a reflecting boundary. For example, a mixture of jammed and gas-like bacterial phases spontaneously form in pores beyond a critical size 124 (Fig. 4 ).…”