Shear Stress Increases the Residence Time of Adhesion of Pseudomonas aeruginosa

Lecuyer, Sigolène; Rusconi, Roberto; Shen, Yi; Forsyth, Alison M.; Vlamakis, Hera; Kolter, Roberto; Stone, Howard A.

doi:10.1016/j.bpj.2010.11.078

Cited by 163 publications

(142 citation statements)

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“…Whereas previous research on surface attachment focused on the effects of high shear rates (10 3 -10 5 s −1 ; ref. 22) and post-attachment dynamics including surface residence time 23 and catch-bond adhesion strength 24 , our results demonstrate that attachment can be enhanced by lower, commonly occurring shear rates with a mechanism virtually independent from specific adhesion properties. For example, P. aeruginosa biofilms are a frequent cause of infection in catheters 3 , where typical shear rates are of the order of 15 s −1 (ref.…”

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confidence: 75%

Bacterial transport suppressed by fluid shear

2014

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Bacteria often live in dynamic fluid environments 1-3 and flow can a ect fundamental microbial processes such as nutrient uptake 1,4 and infection 5 . However, little is known about the consequences of the forces and torques associated with fluid flow on bacteria. Through microfluidic experiments, we show that fluid shear produces strong spatial heterogeneity in suspensions of motile bacteria, characterized by up to 70% cell depletion from low-shear regions due to 'trapping' in high-shear regions. Two mathematical models and a scaling analysis accurately capture these observations, including the maximal depletion at mean shear rates of 2.5-10 s −1 , and reveal that trapping by shear originates from the competition between the cell alignment with the flow and the stochasticity in the swimming orientation. We show that this shear-induced trapping directly impacts widespread bacterial behaviours, by hampering chemotaxis and promoting surface attachment. These results suggest that the hydrodynamic environment may directly a ect bacterial fitness and should be carefully considered in the study of microbial processes.We investigated the effect of flow on motile bacteria by tracking them in precisely controlled laminar flows generated in a microfluidic channel (Fig. 1a). To ensure that the dominant velocity gradients occurred in the horizontal observation plane, at the channel mid-depth, we used a microchannel with aspect ratio H /W > 1 (height H = 750 µm; width W = 425 µm). In that plane, the velocity profile, u(y) = U [1 − 4(y/W ) 2 ], where U is the flow velocity at the channel centreline, is parabolic, and, thus, the shear rate S(y) = du/dy = −8yU /W 2 varies linearly with distance y across the channel and is zero at the centreline (Fig. 1b). In this flow, smooth-swimming Bacillus subtilis bacteria swam unperturbed in straight paths (Fig. 1c) when near the centre of the channel, where the local shear rate was small. Conversely, in high-shear-rate regions, trajectories exhibited frequent loops resulting from rotation of the swimming bacteria by the hydrodynamic torque imparted by the local shear (Fig. 1d). The opposite handedness of the loops on either side of the channel centreline reflects the opposite sign of the shear rate (Fig. 1c,d and Supplementary Movie 1). As shown below, these looping trajectories resulted in bacteria becoming trapped in the high-shear region of the channel.At the population scale, this trapping effect resulted in a marked depletion of cells from the central, low-shear region of the flow, and consequently, in an accumulation in the flanking regions of higher shear. When the flow was impulsively started from rest, the initially uniform distribution of cells over the imaging region across the channel width (Fig. 1e) rapidly (5-10 s) evolved into a distribution characterized by considerably fewer cells in the central part of the channel (Fig. 1f-h). The magnitude of the depletion was severe, with local cell concentrations dropping by 70% (Fig. 1h). The absence of depletion in control experime...

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Bacterial transport suppressed by fluid shear

2014

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“…Previous studies have shown that shear stress increases the duration of adhesion of both P. aeruginosa and Escherichia coli biofilms to coated surfaces. 30,31 This reduction in the amount of bacteria seen on the ETTs in the in vitro model could be an effect of changes in the physical properties of the biofilm in reaction to shear stress. 32 High shear forces have been shown in the literature to favor the creation of tight, rounded microcolonies of bacteria.…”

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Decreased <em>Pseudomonas aeruginosa</em> biofilm formation on nanomodified endotracheal tubes: a dynamic lung model

Machado¹,

Webster²

2016

IJN

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Ventilator-associated pneumonia (VAP) is a serious complication of mechanical ventilation that has been shown to be associated with increased mortality rates and medical costs in the pediatric intensive care unit. Currently, there is no cost-effective solution to the problems posed by VAP. Endotracheal tubes (ETTs) that are resistant to bacterial colonization and that inhibit biofilm formation could provide a novel solution to the problems posed by VAP. The objective of this in vitro study was to evaluate differences in the growth of Pseudomonas aeruginosa on unmodified polyvinyl chloride (PVC) ETTs and on ETTs etched with a fungal lipase, Rhizopus arrhizus , to create nanoscale surface features. These differences were evaluated using an in vitro model of the pediatric airway to simulate a ventilated patient in the pediatric intensive care unit. Each experiment was run for 24 hours and was supported by computational models of the ETT. Dynamic conditions within the ETT had an impact on the location of bacterial growth within the tube. These conditions also quantitatively affected bacterial growth especially within the areas of tube curvature. Most importantly, experiments in the in vitro model revealed a 2.7 log reduction in the number (colony forming units/mL) of P. aeruginosa on the nanoroughened ETTs compared to the untreated PVC ETTs after 24 hours. This reduction in total colony forming units/mL along the x -axis of the tube was similar to previous studies completed for Staphylococcus aureus . Thus, this dynamic study showed that lipase etching can create surface features of nanoscale roughness on PVC ETTs that decrease bacterial attachment of P. aeruginosa without the use of antibiotics and may provide clinicians with an effective and inexpensive tool to combat VAP.

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“…There is precedence for mechanotransduction in eukaryotes, in which surface substrate recognition is an important regulator of development and behavior (11). In prokaryotes, surface mechanical forces affect the binding affinity of cells to substrates (12,13) and alter the rotation of flagella (14,15). However, the effects of mechanical forces on cell behaviors other than motility are not understood, and the regulation of virulence by mechanical cues has not been explored.…”

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Surface attachment inducesPseudomonas aeruginosavirulence

Siryaporn

Kuchma

O’Toole

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

197

264

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Pseudomonas aeruginosa infects every type of host that has been examined by deploying multiple virulence factors. Previous studies of virulence regulation have largely focused on chemical cues, but P. aeruginosa may also respond to mechanical cues. Using a rapid imaging-based virulence assay, we demonstrate that P. aeruginosa activates virulence in response to attachment to a range of chemically distinct surfaces, suggesting that this bacterial species responds to mechanical properties of its substrates. Surface-activated virulence requires quorum sensing, but activating quorum sensing does not induce virulence without surface attachment. The activation of virulence by surfaces also requires the surface-exposed protein PilY1, which has a domain homologous to a eukaryotic mechanosensor. Specific mutation of the putative PilY1 mechanosensory domain is sufficient to induce virulence in non-surface-attached cells, suggesting that PilY1 mediates surface mechanotransduction. Triggering virulence only when cells are both at high density and attached to a surface-two host-nonspecific cues-explains how P. aeruginosa precisely regulates virulence while maintaining broad host specificity.T he bacterium Pseudomonas aeruginosa is a metabolically versatile pathogen that inhabits diverse environments and infects a remarkable range of hosts, including mammals, insects, worms, amoeba, fungi, and other bacteria. P. aeruginosa produces a large number of secreted and cell-associated virulence factors that are redundant and multifactorial (1, 2). Many of P. aeruginosa's virulence factors-including pyocyanin, elastase, and hydrogen cyanide-are host-nonspecific (3-5), bolstering the ability of P. aeruginosa to attack a large range of hosts. Although many of the virulence factors in P. aeruginosa have been identified, the cues that regulate their activity are less understood. Because many of the virulence factors are host-nonspecific, we explored whether virulence in P. aeruginosa is regulated by host-nonspecific cues.Host cell membranes and cell surfaces are the first line of defense against bacterial toxins and invasion. P. aeruginosa attaches to host cell surfaces early during the infection process. The presence of a surface could thus act as a cue for P. aeruginosa, signaling the presence of a host. Surface attachment is also a critical initial step that enables the establishment of biofilms (6-8). Although biofilms are clearly important for pathogenesis, it remains unclear whether they directly promote host cell killing or mediate other important processes such as long-term colonization.One host-nonspecific cue that could regulate virulence is the mechanical force that bacteria experience upon surface attachment. P. aeruginosa performs surface-associated behaviors (7, 8) such as swarming and twitching (9, 10), but it remains unclear whether P. aeruginosa senses the chemical or mechanical properties of surfaces. There is precedence for mechanotransduction in eukaryotes, in which surface substrate recognition is an important regulat...

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Shear Stress Increases the Residence Time of Adhesion of Pseudomonas aeruginosa

Cited by 163 publications

References 40 publications

Bacterial transport suppressed by fluid shear

Bacterial transport suppressed by fluid shear

Decreased <em>Pseudomonas aeruginosa</em> biofilm formation on nanomodified endotracheal tubes: a dynamic lung model

Surface attachment inducesPseudomonas aeruginosavirulence

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