Single-cell morphology dictates bacterial growth dynamics under 3D confinement

Can physical properties of the microenvironment act as selection pressures at the population-level? Our current understanding of factors that exert such effect on population growth dynamics implicates genetic mutations and chemical cues, based on experimental assays performed using homogeneous liquid or 2D cultures. However, in their natural niche, bacteria inhabit complex and disordered 3D microenvironments with diverse mechanical properties. Here, to test if the physical microenvironment can selectively favor the collective growth of certain microbial strains under 3D confinement, we design transparent porous 3D growth media that match the viscoelastic properties of natural microbial habitats. Combining optical density-based growth measurements, 3D confocal microscopy, and agent-based simulations, we find that the shape anisotropy of high-aspect-ratio bacteria provides them with a selective advantage to grow more efficiently under increased 3D confinement as opposed to spherical bacteria. More precisely, under 3D confinement, high aspect ratio bacteria produce elongated colonies with larger surface areas allowing them to access nutrients more effectively. Our work provides an example of how the alteration in the physical of the microenvironment can dictate the microbiome composition in 3D disordered materials. This will help in understanding and modeling population dynamics within microbial communities inhabiting diverse biological niches using elementary physical principles.