Nonlocal interactions through hydrodynamics drive biofilm development and microbial competition in porous media

Abstract Microorganisms predominantly exist within soil-like environments as sessile communities called biofilms, where fluid dynamics critically shape their development and dispersal. Despite their central role in diverse systems, from biogeochemical processes to industrial filtration, oil recovery, groundwater contamination, and carbon sequestration, the mechanisms underlying biofilm-flow interactions in porous media remain poorly understood. Here, we combine microfluidic experiments with mathematical modeling to demonstrate that nonlocal interactions through hydrodynamic effects mediate intricate spatiotemporal dynamics and drive exploitative competition within porous media. Our results show that biofilms self-organize into clusters of biologically clogged channels interspersed with preferential flow paths (PFPs). PFP formation and stability result from feedbacks between local changes in hydraulic conductivity and global reorganization of flow patterns and pressure distribution. We reveal that PFPs tend to be unstable, with detachment of biofilm triggered when pressure differentials exceed critical thresholds. Based on simulations of competing populations, we suggest that these large-scale detachment events could be interpreted as an evolutionary trade-off, whereby bacterial matrices are sufficiently robust to withstand continuous shear stress while remaining sensitive to pressure-induced failure, thereby enabling nutrient access and avoiding redirection of resources toward competitors. The nonlocal nature of these hydrodynamic interactions shows that fitness in porous media must be thought of as a multiscale concept and provides new insights into bacterial adaptation strategies in porous environments. These findings further suggest targeted approaches for biofilm control in both natural and engineered systems.