Biofilms regulate critical processes in porous ecosystems. However, the biophysical underpinnings of the ecological success of these biofilms are poorly understood. Combining experiments with fluidic devices, sequencing and modeling, we reveal that architectural plasticity enhances space exploitation by multispecies biofilms in porous environments. Biofilms consistently differentiated into an annular base biofilm coating the grains and into streamers protruding from the grains into the pore space. Although different flow-related processes governed the differentiation of these architectures, both BB and streamers were composed of similar bacterial assemblages. This is evidence for architectural plasticity. Architectural plasticity allowed for complementary use of the space provided by the grain–pore complexes, which increased biofilm carrying capacity at the larger scale of the porous system. This increase comes potentially at the cost of a tradeoff. Contrasting time scales of oxygen replenishment and consumption, we show that streamers locally inhibit the growth of the BB downstream from the grains. Our study provides first insights into the biophysical underpinnings to the success of multispecies biofilms in porous environments.

Natural porous systems, such as soil, membranes, and biological tissues comprise disordered structures characterized by dead-end pores connected to a network of percolating channels. The release and dispersion of particles, solutes, and microorganisms from such features is key for a broad range of environmental and medical applications including soil remediation, filtration and drug delivery. Yet, owing to the stagnant and opaque nature of these disordered systems, the role of microscopic structure and flow on the dispersion of particles and solutes remains poorly understood. Here, we use a microfluidic model system that features a pore structure characterized by distributed dead-ends to determine how particles are transported, retained and dispersed. We observe strong tailing of arrival time distributions at the outlet of the medium characterized by power-law decay with an exponent of 2/3. Using numerical simulations and an analytical model, we link this behavior to particles initially located within dead-end pores, and explain the tailing exponent with a hopping across and rolling along the streamlines of vortices within dead-end pores. We quantify such anomalous dispersal by a stochastic model that predicts the full evolution of arrival times. Our results demonstrate how microscopic flow structures can impact macroscopic particle transport.

The dispersal of organisms controls the structure and dynamics of populations and communities, and can regulate ecosystem functioning. Predicting dispersal patterns across scales is important to understand microbial life in heterogeneous porous environments such as soils and sediments. We developed a multi-scale approach, combining experiments with microfluidic devices and time-lapse microscopy to track individual bacterial trajectories and measure the overall breakthrough curves and bacterial deposition profiles: we, then, linked the two scales with a novel stochastic model. We show that motile cells of Pseudomonas putida disperse more efficiently than non-motile mutants through a designed heterogeneous porous system. Motile cells can evade flow-imposed trajectories, enabling them to explore larger pore areas than non-motile cells. While transported cells exhibited a rotation in response to hydrodynamic shear, motile cells were less susceptible to the torque, maintaining their body oriented towards the flow direction and thus changing the population velocity distribution with a significant impact on the overall transport properties. We also found, in a separate set of experiments, that if the suspension flows through a porous system already colonized by a biofilm, P. putida cells are channelled into preferential flow paths and the cell attachment rate is increased. These two effects were more pronounced for non-motile than for motile cells. Our findings suggest that motility coupled with heterogeneous flows can be beneficial to motile bacteria in confined environments as it enables them to actively explore the space for resources or evade regions with unfavourable conditions. Our study also underlines the benefit of a multi-scale approach to the study of bacterial dispersal in porous systems.

In streams and rivers, ecosystem metabolism (primary production and respiration) that is carried out by multitrophic microbial communities residing mainly in the streambed is shaped by the master variable flow (