Hydration-controlled bacterial motility and dispersal on surfaces

Abstract

Flagellar motility, a mode of active motion shared by many prokaryotic species, is recognized as a key mechanism enabling population dispersal and resource acquisition in microbial communities living in marine, freshwater, and other liquid-replete habitats. By contrast, its role in variably hydrated habitats, where water dynamics result in fragmented aquatic habitats connected by micrometric films, is debated. Here, we quantify the spatial dynamics of Pseudomonas putida KT2440 and its nonflagellated isogenic mutant as affected by the hydration status of a rough porous surface using an experimental system that mimics aquatic habitats found in unsaturated soils. The flagellar motility of the model soil bacterium decreased sharply within a small range of water potential (0 to −2 kPa) and nearly ceased in liquid films of effective thickness smaller than 1.5 μm. However, bacteria could rapidly resume motility in response to periodic increases in hydration. We propose a biophysical model that captures key effects of hydration and liquid-film thickness on individual cell velocity and use a simple roughness network model to simulate colony expansion. Model predictions match experimental results reasonably well, highlighting the role of viscous and capillary pinning forces in hindering flagellar motility. Although flagellar motility seems to be restricted to a narrow range of very wet conditions, fitness gains conferred by fast surface colonization during transient favorable periods might offset the costs associated with flagella synthesis and explain the sustained presence of flagellated prokaryotes in partially saturated habitats such as soil surfaces.flagella | biophysics | liquid film | fitness | motility D ispersal is recognized as a key ecological process enabling populations' access to new sites and pools of resources (1), thereby affecting structure and productivity of ecosystems (2, 3). Active bacterial motion (motility) takes on many forms that require various appendages (4). If surface-associated modes of motility such as twitching, gliding, or swarming seem restricted to some species (5), the ability to swim by rotating one or more flagella is shared by a large diversity of prokaryotes. This swimming motility has attracted considerable attention, primarily aimed at resolving the biophysical functioning of flagella and to a lesser degree, exploring its adaptive value. In marine environments, a large fraction of bacterial populations are flagellated (6), and swimming motility is often coupled with chemotaxis, conferring a clear benefit to these cells by allowing them to outswim diffusion and exploit transient substrate gradients (7,8).In contrast to water-replete environments where flagellar motility is essentially unrestricted, there exists strong physical limitations to flagellar motility in partially saturated media where aquatic microhabitats are often fragmented and connected only by thin liquid films of bacterial size or smaller (9). The limitations to bacterial motility in thin liquid films have, thus, l...

Microbial dispersal in unsaturated porous media: Characteristics of motile bacterial cell motions in unsaturated angular pore networks

“…For given geometry and cell size, the results depicted in Figure 5 show that cell flagellated velocity was relatively constant under saturated condition, and following air entry, the velocity gradually decreased with matric potential until it reached a critical value where capillary forces pin bacterial cells behind air-water interfaces rendering cells nonmotile [Dechesne et al, 2010;Wang and Or, 2010]. The results indicate that cell velocity never achieves to cell velocity in bulk solution due to cell-wall hydrodynamic interactions (see equation (6)).…”

“…However, in unsaturated porous media, heterogeneous geometry and hydration conditions restrict the motility of bacteria to a thin aqueous film due to the cell-wall viscous drag and capillary pinning forces [Dechesne et al, 2010;Wang and Or, 2010]. In the pore network model, we consider each corner of triangular-shaped bonds as a separate pathway for bacterial motion with own effective water film thickness, dðuÞ.…”

“…Dispersal and self-motion play an important role in many biological and ecological processes, including the cycling of soil organic matter [Azam, 1998;Bardgett, 2011;Philippot et al, 2013], bioremediation of contaminated soils and aquifers [Hams and Bosma, 1997;Harms and Wick, 2006;Banitz et al, 2011], promoting the plant rhizosphere and root function, controlling the spread of pathogenic bacteria [Beattie and Lindow, 1995;Beattie, 2011;Van der Wal et al, 2013], and numerous other functions continuously being discovered. Despite the significant role of microbial dispersal in unsaturated soil, based mechanisms and rates remain unclear due to limited experimental data, soil opacity, and complex pore spaces all leading to conflicting reports concerning rates and modes of soil microbial dispersion [Boelens et al, 1994;Turnbull et al, 2001;Dechesne et al, 2010].…”

Hydration dynamics promote bacterial coexistence on rough surfaces

“…Hydration status and pore-space characteristics are critical factors shaping nutrient fields and bacterial motility, and are thus key to understanding bacterial interactions in soil and other porous media such as dry food products (Barton and Ford, 1997;Dens and Van Impe, 2000;Wilson et al, 2002;Chang and Halverson, 2003;Or et al, 2007;Chen and Jin, 2011). Although motility has long been argued as a key factor for survival in heterogeneous environments and for biodiversity maintenance (Fenchel, 2002;Reichenbach et al, 2007;Vos and Velicer, 2008), it is only recently that crucial processes regulating bacterial motility within liquid films forming on partially hydrated rough surfaces have been quantified (Dechesne et al, 2010;Wang and Or, 2010). These studies have shown that surface roughness and aqueous-phase configuration impose capillary and hydrodynamic constraints limiting bacterial motility, and defined a surprisingly narrow range of hydration conditions where motility could confer ecological advantage on rough surfaces.…”

“…We employed a hybrid model that couples individual-based description of cell growth, motion and interactions within a nutrient field described by a (continuum-based) reaction À diffusion model (Kreft et al, 1998;Dechesne et al, 2010). The model resolves spatial and temporal nutrient diffusion fields subjected to prescribed boundary conditions, heterogeneity and local nutrient interception by individual cells.…”