Temperature and pyoverdine‐mediated iron acquisition control surface motility of <i>Pseudomonas putida</i>

Matilla, Miguel A.; Ramos, Juan L.; Duque, Estrella; Alché, Juan de Dios; Espinosa‐Urgel, Manuel; Ramos-González, Marı́a Isabel

doi:10.1111/j.1462-2920.2007.01286.x

Cited by 67 publications

(80 citation statements)

References 54 publications

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“…This clearly shows the potential of flagellar motility for fast population dispersal on wet surfaces. A role of swarming motility, which, in P. putida KT2440, relies on short pili rather than flagella, is unlikely in our experiments, because it is expressed only under specific conditions (14) and manifests itself by en masse cell movements, which we did not observe.…”

Section: Resultscontrasting

confidence: 66%

Hydration-controlled bacterial motility and dispersal on surfaces

Dechesne

Wang

Gulez

et al. 2010

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

181

240

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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...

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Section: Resultscontrasting

confidence: 66%

Hydration-controlled bacterial motility and dispersal on surfaces

Dechesne

Wang

Gulez

et al. 2010

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

181

240

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“…It was shown previously that siderophores play an important role in surface motility in P. aeruginosa (17). Since our microarray experiments revealed the downregulation of several genes involved in the synthesis and function of the two siderophores pyoverdine and pyochelin in the PA4398…”

Section: Fig 4 Relative Intracellular C-di-gmp Levels Of Pa14 Wild-tysupporting

confidence: 53%

“…Swarming is characterized by rapid, coordinated migration of bacterial cells across semisolid surfaces (12,13) and is highly dependent on cell-to-cell signaling and the production and secretion of rhamnolipids, which are proposed to act as biosurfactants that lower the strong surface tension between bacterial cells and the surrounding environment (11,14,15). Previously, studies by us and others were able to show that swarming in P. aeruginosa is more than just a form of locomotion: it is a complex adaptation process resulting in cellular changes, such as cell elongation or hyperflagellation, as well as increased virulence gene expression and antibiotic resistance (11,13,16,17).…”

mentioning

confidence: 99%

Sensor Kinase PA4398 Modulates Swarming Motility and Biofilm Formation in Pseudomonas aeruginosa PA14

Strehmel

Neidig

Nusser

et al. 2015

Appl Environ Microbiol

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Pseudomonas aeruginosa is an opportunistic human pathogen that is able to sense and adapt to numerous environmental stimuli by the use of transcriptional regulators, including two-component regulatory systems. In this study, we demonstrate that the sensor kinase PA4398 is involved in the regulation of swarming motility and biofilm formation in P. aeruginosa PA14. A PA4398 ؊ mutant strain was considerably impaired in swarming motility, while biofilm formation was increased by approximately 2-fold. The PA4398؊ mutant showed no changes in growth rate, rhamnolipid synthesis, or the production of the Pel exopolysaccharide but exhibited levels of the intracellular second messenger cyclic dimeric GMP (c-di-GMP) 50% higher than those in wild-type cells. The role of PA4398 in gene regulation was investigated by comparing the PA4398 ؊ mutant to the wildtype strain by using microarray analysis, which demonstrated that 64 genes were up-or downregulated more than 1.5-fold (P < 0.05) under swarming conditions. In addition, more-sensitive real-time PCR studies were performed on genes known to be involved in c-di-GMP metabolism. Among the dysregulated genes were several involved in the synthesis and degradation of c-di-GMP or in the biosynthesis, transport, or function of the iron-scavenging siderophores pyoverdine and pyochelin, in agreement with the swarming phenotype observed. By analyzing additional mutants of selected pyoverdine-and pyochelin-related genes, we were able to show that not only pvdQ but also pvdR, fptA, pchA, pchD, and pchH are essential for the normal swarming behavior of P. aeruginosa PA14 and may also contribute to the swarming-deficient phenotype of the PA4398؊ mutant in addition to elevated c-di-GMP levels.

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“…Because iron acquisition is reported to play an important role in the surface movement of bacteria (18,31), the motilities of the WT and pyoverdine-related mutants were investigated on an MG plate containing 0.25% agar for swimming and on an MG plate containing 0.4% agar and an SWM plate containing 0.5% agar for swarming. All of the strains showed similar swimming motilities under this condition (data not shown), whereas mutant strains, especially the ⌬pvdJ and ⌬pvdL mutants, exhibited a hyperswarming phenotype (Fig.…”

Section: Resultsmentioning

confidence: 99%

The Siderophore Pyoverdine of Pseudomonas syringae pv. tabaci 6605 Is an Intrinsic Virulence Factor in Host Tobacco Infection

et al. 2010

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To investigate the role of iron uptake mediated by the siderophore pyoverdine in the virulence of the plant pathogen Pseudomonas syringae pv. tabaci 6605, three predicted pyoverdine synthesis-related genes, pvdJ, pvdL, and fpvA, were mutated. The pvdJ, pvdL, and fpvA genes encode the pyoverdine side chain peptide synthetase III L-Thr-L-Ser component, the pyoverdine chromophore synthetase, and the TonB-dependent ferripyoverdine receptor, respectively. The ⌬pvdJ and ⌬pvdL mutants were unable to produce pyoverdine in mineral saltsglucose medium, which was used for the iron-depleted condition. Furthermore, the ⌬pvdJ and ⌬pvdL mutants showed lower abilities to produce tabtoxin, extracellular polysaccharide, and acyl homoserine lactones (AHLs), which are quorum-sensing molecules, and consequently had reduced virulence on host tobacco plants. In contrast, all of the mutants had accelerated swarming ability and increased biosurfactant production, suggesting that swarming motility and biosurfactant production might be negatively controlled by pyoverdine. Scanning electron micrographs of the surfaces of tobacco leaves inoculated with the mutant strains revealed only small amounts of extracellular polymeric matrix around these mutants, indicating disruption of the mature biofilm. Tolerance to antibiotics was drastically increased for the ⌬pvdL mutant, as for the ⌬psyI mutant, which is defective in AHL production. These results demonstrated that pyoverdine synthesis and the quorum-sensing system of Pseudomonas syringae pv. tabaci 6605 are indispensable for virulence in host tobacco infection and that AHL may negatively regulate tolerance to antibiotics.Phytopathogenic bacteria employ a variety of virulence mechanisms to overcome the defense systems of plants. Pseudomonas syringae pv. tabaci 6605 is a gram-negative bacterium that causes wildfire disease on host tobacco plants. Previously, we demonstrated that flagellin, a component of the flagellar filament of this organism, is a major elicitor of the hypersensitive reaction and is posttranslationally modified by glycosylation (26,(28)(29)(30). A genetic region composed of three open reading frames (ORFs), namely, fgt1, fgt2, and orf3, was previously identified in a flagellum gene cluster. fgt1 and fgt2 encode flagellin glycosyltransferase, and orf3 shows significant homology to the 3-oxoacyl-(acyl carrier protein [ACP]) synthase III in the fatty acid elongation cycle, required for the synthesis of acyl homoserine lactones (AHLs) (11,30,31). Analysis of an orf3 deletion (⌬orf3) mutant revealed that orf3 played no role in the glycosylation of flagellin, although the virulence of the ⌬orf3 mutant on tobacco plants was remarkably reduced.Many virulence factors of bacteria have been reported to be under the regulation of a cell density-dependent system called quorum sensing. AHLs are synthesized by the coupling of the homoserine lactone ring from S-adenosylmethionine and acyl chains from the acyl-ACP by PsyI in P. syringae (9, 11). P. syringae pv. tabaci 6605 secretes three type...

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Temperature and pyoverdine‐mediated iron acquisition control surface motility of Pseudomonas putida

Cited by 67 publications

References 54 publications

Hydration-controlled bacterial motility and dispersal on surfaces

Hydration-controlled bacterial motility and dispersal on surfaces

Sensor Kinase PA4398 Modulates Swarming Motility and Biofilm Formation in Pseudomonas aeruginosa PA14

The Siderophore Pyoverdine of Pseudomonas syringae pv. tabaci 6605 Is an Intrinsic Virulence Factor in Host Tobacco Infection

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