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Hydration-Controlled Bacterial Motility and Dispersal on Surfaces

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Hydration-Controlled Bacterial Motility and Dispersal on Surfaces Hydration-controlled bacterial motility and dispersal on surfaces Arnaud Dechesnea, Gang Wangb, Gamze Güleza, Dani Orb, and Barth F. Smetsa,1 aDepartment of Environmental Engineering, Technical University of Denmark, DK-2800 Kgs. Lyngby, Denmark; and bDepartment of Environmental Sciences, Swiss Federal Institute of Technology, 8092 Zurich, Switzerland Communicated by James M. Tiedje, Center for Microbial Ecology, East Lansing, MI, June 14, 2010 (received for review October 5, 2009) Flagellar motility, a mode of active motion shared by many pro- from direct observation of bacterial dispersal at both individual karyotic species, is recognized as a key mechanism enabling pop- and population scales under conditions of controlled hydration, ulation dispersal and resource acquisition in microbial communities we used the porous-surface model (PSM) (12). In this experi- living in marine, freshwater, and other liquid-replete habitats. By mental system, bacteria are grown on a porous ceramic surface in contrast, its role in variably hydrated habitats, where water dynamics thin aqueous films, whose effective thickness is controlled by result in fragmented aquatic habitats connected by micrometric films, applying a prescribed suction similar to how matric potential is debated. Here, we quantify the spatial dynamics of Pseudomonas controls hydration in soils. The system allowed a quantitative putida KT2440 and its nonflagellated isogenic mutant as affected assessment of the dispersal rate and competition of Pseudomo- by the hydration status of a rough porous surface using an experi- nas putida KT2240 and a nonflagellated ΔfliM isogenic mutant as mental system that mimics aquatic habitats found in unsaturated influenced by water potential at the colony and individual scales. soils. The flagellar motility of the model soil bacterium decreased sharply within a small range of water potential (0 to −2 kPa) and nearly Results and Discussion ceased in liquid films of effective thickness smaller than 1.5 μm. How- At the colony scale, we observed constant front expansion rates, in ever, bacteria could rapidly resume motility in response to periodic accordance with the model proposed by Skellam (13) for a pop- increases in hydration. We propose a biophysical model that captures ulation dispersing by random walk and exponential growth. The key effects of hydration and liquid-film thickness on individual cell average rate of colony expansion for both the wild type and non- velocity and use a simple roughness network model to simulate colony flagellated mutant decreased with decreasing matric potential MICROBIOLOGY expansion. Model predictions match experimental results reasonably (Fig. 1). The most significant differences in expansion rates be- well, highlighting the role of viscous and capillary pinning forces in tween the strains were apparent at −0.5 and −1.2 kPa, where the hindering flagellar motility. Although flagellar motility seems to be wild type, capable of flagellar motility, dispersed more than 15 restricted to a narrow range of very wet conditions, fitness gains con- times faster than the mutant, which dispersed by cell shoving and ferred by fast surface colonization during transient favorable periods Brownian motion only. This clearly shows the potential of flagellar might offset the costs associated with flagella synthesis and explain motility for fast population dispersal on wet surfaces. A role of the sustained presence of flagellated prokaryotes in partially satu- swarming motility, which, in P. putida KT2440, relies on short pili rated habitats such as soil surfaces. rather than flagella, is unlikely in our experiments, because it is expressed only under specific conditions (14) and manifests itself flagella | biophysics | liquid film | fitness | motility by en masse cell movements, which we did not observe. The colony-expansion rate of the wild type decreased exponen- ispersal is recognized as a key ecological process enabling tially from an average of 521 μm/h for the wettest conditions (−0.5 Dpopulations’ access to new sites and pools of resources (1), kPa) to 14 μm/h at −2.0 kPa (Fig. 1). After this sharp decrease, thereby affecting structure and productivity of ecosystems (2, 3). the colonization rate leveled, suggesting that, on the PSM, −2.0 Active bacterial motion (motility) takes on many forms that require kPa marks a threshold, below which the contribution of flagellar various appendages (4). If surface-associated modes of motility motility to population dispersal becomes insignificant. Under drier such as twitching, gliding, or swarming seem restricted to some conditions, we expect both types of bacteria to disperse by cell species (5), the ability to swim by rotating one or more flagella is shoving only and thus, their colonies to expand at similar rates. The shared by a large diversity of prokaryotes. This swimming motility slightly faster expansion of the wild-type colonies observed at −3.6 has attracted considerable attention, primarily aimed at resolving kPa (Fig. 1) is attributed to the higher intrinsic-growth rate of the biophysical functioning of flagella and to a lesser degree, ex- this organism. Indeed, although the only difference between mu- ploring its adaptive value. In marine environments, a large fraction tant and wild type resides in the fliM knock-out, the former presents of bacterial populations are flagellated (6), and swimming motility asignificantly reduced growth rate. This was evidenced in compe- is often coupled with chemotaxis, conferring a clear benefit to these tition experiments in stirred liquid medium where the fitness of cells by allowing them to outswim diffusion and exploit transient the mutant relative to that of the wild type was significantly smaller substrate gradients (7, 8). than 1 (0.82, SD = 0.04, n =3,P = 0.016, two-tailed t test). In contrast to water-replete environments where flagellar mo- The mild matric potential that we prescribed does not per se tility is essentially unrestricted, there exists strong physical limi- restrict bacterial motion (12), but it acts through its control of tations to flagellar motility in partially saturated media where the effective liquid-film thickness on the ceramic-plate surface. The 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, long been posited Author contributions: A.D., D.O., and B.F.S. designed research; A.D., G.W., and G.G. per- but never directly quantified or described biophysically beyond the formed research; A.D. made and analyzed single-cell observations; G.W. implemented the fl motility model, ran the simulations, and analyzed the results; G.G. made and analyzed general notion that agellar motility requires hydrated pathways. population-scale observations and competition experiments; and A.D., D.O., and B.F.S. In addition, the fitness benefit associated with flagellar motility in wrote the paper. partially saturated soils has been debated because of conflicting The authors declare no conflict of interest. experimental data (10, 11). 1To whom correspondence should be addressed. E-mail: [email protected]. Here, to avoid the complexity inherent to natural partially This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. saturated microbial habitats such as soil matrixes and benefit 1073/pnas.1008392107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1008392107 PNAS Early Edition | 1of4 Downloaded by guest on September 27, 2021 onset of normal capillary pressure, and introduction of a capillary pinning force (FC) (19). We combine hydration-dependent re- sistive forces into a simple model where attainable bacterial cell velocity is proportional to the residual force available for flagellar FM − Fλ − FC V ¼ V V FM − Fλ − FC < propulsion: 0 FM , with = 0 for 0. This model component provides estimates of the potential cell velocity for local hydration conditions (which may vary spatially over a natural surface) that may then be directed by local che- motactic gradient and a random component (tumble-like) to define the actual direction and extent of displacement during a single run (or time step). These modifications are implemented Fig. 1. Matric potential affects colony-expansion rates of P. putida KT2440 wild type (flagellated) and its ΔfliM isogenic mutant (nonflagellated) mea- by combining the random component (tumble-like change of run sured as radial expansion of colonies initiated from single cells. More neg- direction) and local chemotactic gradients by weighing these by ative matric potentials correspond to thinner surface liquid films. Error bars a factor of (1 − ξ)andξ, respectively, depending on normalized mark 1 SD (n varies from 6 to 14). Simulated colony-expansion rates are local chemoattractant gradient, ξ (defined as the ratio of local to depicted by the line and shaded area (representing 1 SD). maximal chemotactic gradient and calculated as the concentra- tion difference across the local bond divided by the boundary concentration). The cellular motion is evaluated every 1.1 s (an fi relationship between matric potential and liquid- lm thickness assumed duration of a run and tumble cycle) (20), and the actual depends solely on surface wettability and roughness (15). At −2.0 * * * * run velocity is obtained as: V ¼ðRð1 − ξÞþNξÞV,withR de- kPa, which we identified as the limit beyond which the contribution * of flagellar motility to colony expansion is negligible on the ceramic scribing a random direction
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