Trait-specific dispersal of bacteria in heterogeneous porous environments: from pore to porous medium scale

Abstract

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.

The influence of motility on bacterial accumulation in a microporous channel

“…This is, for example, the case in the fields of pollution reduction, 1,2 oil recovery [3][4][5] biocalcification for soil reinforcement, 6,7 or to heal cement cracks. 8,9 However, one of the problems researchers face when trying to optimize these processes is the limited understanding of the role that bacterial motility plays at the pore scale [10][11][12][13][14] and its coupling to local chemical gradients. 15 Indeed, we now know that flagellated microorganisms such as E. coli, or sperm cells display a great variety of swimming behaviors like upstream motions, [16][17][18] drift trajectories on surfaces 19,20 or helicoidal trajectories in a flow.…”

“…21,22 These motions contribute significantly to the trapping of bacteria in pores as well as in determining their localization in a channeled flow 23 and their hydrodynamic dispersion. 14,24,25 One of the consequences is an enhanced attachment and colonization of surfaces 23,[26][27][28] which influences the biofilm formation 29 and therefore the overall fluid flow. 29,30 The aim of this work is to elucidate the important role that motility and geometric confinement play at the pore scale for the accumulation of bacteria on surfaces in a complex geometry.…”

Challenges and approaches in assessing the interplay between microorganisms and their physical micro-environments

“…This example illustrates the new insights attainable by introducing physical structures within microfluidic chambers, as the interaction between the mixed genotypes was only evident in the structured chambers. In another example, microbial migration through a similar microfluidics structure was used to help demonstrate that motile Pseudomonas putidi cells could disperse more efficiently than non-motile mutants and were better able to navigate against the direction of flow across different scales [43] . This allowed the motile cells to explore more pore space relative to non-motile cells…”

Controlling pore-scale processes to tame subsurface biomineralization

“…The distribution of single cells within porous media is far from uniform and most likely affects the spatial distribution of biomineralization products. Chemotaxis, the ability to sense and move towards a chemical source (Matthäus et al 2009 ; Ahmed et al 2010 ), enables bacteria to position themselves along gradients within a fully or partially saturated porous matrix (Godány et al 2017 ; Creppy et al 2019 ; Ebrahimi and Or 2015 ; Scheidweiler et al 2020 ). Chemotactic bacteria can accumulate in a region of high nutrient concentration and then disperse as the nutrient concentration is decreased by diffusion, flow or microbial metabolism.…”