(319f) Getting in Shape—Unraveling the Morphodynamics of Microbial Communities

In nature, microbial organisms often self-organize into spatially structured communities, with distinct groups of cells occupying distinct spatial domains in 3D space. This spatial arrangement significantly influences diverse biological functions, including stability, nutrient access, and diversity; and yet, how exactly multicellular microbial communities get their shape and spatial structure remain poorly understood. Here, we first study how growing 3D bacterial colonies get their shape, a morphodynamical process that remains underexplored despite the prevalence of 3D environments in nature, e.g., soils and hosts. Using experiments in transparent 3D granular hydrogel matrices, we show that dense colonies generically become morphologically unstable and roughen as they consume nutrients and grow beyond a critical size—eventually adopting a characteristic broccoli-like morphology independent cell type and environmental conditions. This behavior reflects a key difference between 2D and 3D: while a 2D colony may access the nutrients needed for growth from the third dimension, a 3D colony inevitably becomes nutrient limited in its interior, driving a transition to unstable growth. We elucidate this instability using a continuum model that treats the colony as an “active fluid” whose dynamics are driven by nutrient-dependent cellular growth. We find that when all dimensions of the colony substantially exceed the nutrient penetration length, nutrient-limited growth drives a 3D morphological instability that recapitulates essential features of the experimental observations. Additionally, we extend our work to unveil the morphodynamics of multispecies communities, in which different microbes form monoclonal domains that compete for space and resources. What determines the shape of the interface between such domains—which in turn influences the interactions between cells and overall community function? Using a related model, we establish quantitative principles describing when different interfacial behaviors arise, and find good agreement both with the results of previous experimental reports as well as new experiments performed here. Altogether, our work thus provides a framework to predict and control the organization of proliferating colonies—as well as other forms of growing active matter, such as tumors and engineered living materials—in 2D and 3D environments.