Dataset Information

Multiple Environmental Factors Influence the Importance of the Phosphodiesterase DipA upon Pseudomonas aeruginosa Swarming.

ABSTRACT: Pseudomonas aeruginosa exhibits flagellum-mediated swimming in liquid and swarming on hydrated surfaces under diverse nutrient conditions. Prior studies have implicated a phosphodiesterase, DipA, in regulating these flagellum-mediated motilities, but collectively, the necessity for DipA was unclear. In this study, we find that the medium composition conditionally constrains the influence of DipA on flagellar motility. We show that DipA exhibits more influence on minimal medium supplemented with glutamate or glucose, where flagellar motility was negated for the dipA mutant. Conversely, a dipA-deficient mutant exhibits flagellar motility when growing with LB Lennox broth and minimal medium supplemented with Casamino Acids. Swarming under these rich medium conditions occurs under elevated levels of c-di-GMP. We also demonstrate that the influence of DipA upon swimming often differs from that upon swarming, and we conclude that a direct comparison of the motility phenotypes is generally valid only when characterizing motility assay results from the same medium composition. Our results are consistent with the explanation that DipA is one of several phosphodiesterases responding to the nutrient environment sensed by P. aeruginosa On minimal medium with glutamate or glucose, DipA is dominant; however, on rich medium, the necessity of DipA is fully negated.IMPORTANCE Motile and ubiquitous bacteria such as Pseudomonas aeruginosa can quickly colonize surfaces and form biofilms in numerous environments such as water distribution systems, soil, and the human lung. To effectively disrupt bacterial colonization, it is imperative to understand how bacteria regulate motility in these different growth environments. Here, we show that the phosphodiesterase DipA is not required for flagellar motility under all nutrient conditions. Thus, the maintenance of intracellular c-di-GMP levels to promote flagellar motility or biofilm development must be conditionally regulated by differing phosphodiesterases in variation with select nutrient cues.

SUBMITTER: Mattingly AE

PROVIDER: S-EPMC5861829 | biostudies-other | 2018 Apr

REPOSITORIES: biostudies-other

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Multiple Environmental Factors Influence the Importance of the Phosphodiesterase DipA upon Pseudomonas aeruginosa Swarming.

Mattingly Anne E AE Kamatkar Nachiket G NG Morales-Soto Nydia N Borlee Bradley R BR Borlee Bradley R BR Shrout Joshua D JD

Applied and environmental microbiology 20180319 7

<i>Pseudomonas aeruginosa</i> exhibits flagellum-mediated swimming in liquid and swarming on hydrated surfaces under diverse nutrient conditions. Prior studies have implicated a phosphodiesterase, DipA, in regulating these flagellum-mediated motilities, but collectively, the necessity for DipA was unclear. In this study, we find that the medium composition conditionally constrains the influence of DipA on flagellar motility. We show that DipA exhibits more influence on minimal medium supplemente ...[more]

PMID: 29427430

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Project description:BackgroundThe bacterium Pseudomonas aeruginosa is capable of three types of motilities: swimming, twitching and swarming. The latter is characterized by a fast and coordinated group movement over a semi-solid surface resulting from intercellular interactions and morphological differentiation. A striking feature of swarming motility is the complex fractal-like patterns displayed by migrating bacteria while they move away from their inoculation point. This type of group behaviour is still poorly understood and its characterization provides important information on bacterial structured communities such as biofilms. Using GeneChip® Affymetrix microarrays, we obtained the transcriptomic profiles of both bacterial populations located at the tip of migrating tendrils and swarm center of swarming colonies and compared these profiles to that of a bacterial control population grown on the same media but solidified to not allow swarming motility.ResultsMicroarray raw data were corrected for background noise with the RMA algorithm and quantile normalized. Differentially expressed genes between the three conditions were selected using a threshold of 1.5 log2-fold, which gave a total of 378 selected genes (6.3% of the predicted open reading frames of strain PA14). Major shifts in gene expression patterns are observed in each growth conditions, highlighting the presence of distinct bacterial subpopulations within a swarming colony (tendril tips vs. swarm center). Unexpectedly, microarrays expression data reveal that a minority of genes are up-regulated in tendril tip populations. Among them, we found energy metabolism, ribosomal protein and transport of small molecules related genes. On the other hand, many well-known virulence factors genes were globally repressed in tendril tip cells. Swarm center cells are distinct and appear to be under oxidative and copper stress responses.ConclusionsResults reported in this study show that, as opposed to swarm center cells, tendril tip populations of a swarming colony displays general down-regulation of genes associated with virulence and up-regulation of genes involved in energy metabolism. These results allow us to propose a model where tendril tip cells function as «scouts» whose main purpose is to rapidly spread on uncolonized surfaces while swarm center population are in a state allowing a permanent settlement of the colonized area (biofilm-like).

Project description:The opportunistic human pathogen Pseudomonas aeruginosa is known for exhibiting diverse forms of collective behaviors, like swarming motility and biofilm formation. Swarming in P. aeruginosa is a collective movement of the bacterial population over a semisolid surface, but specific swarming signals are not clear. We hypothesize that specific environmental signals induce swarming in P. aeruginosa. We show that under nutrient-limiting conditions, a low concentration of ethanol provides a strong ecological motivation for swarming in P. aeruginosa strain PA14. Ethanol serves as a signal and not a source of carbon under these conditions. Moreover, ethanol-driven swarming relies on the ability of the bacteria to metabolize ethanol to acetaldehyde using a periplasmic quinoprotein alcohol dehydrogenase, ExaA. We found that ErdR, an orphan response regulator linked to ethanol oxidation, is necessary for the transcriptional regulation of a cluster of 17 genes, including exaA, during swarm lag. Further, we show that P. aeruginosa displays characteristic foraging motility on a lawn of Cryptococcus neoformans, a yeast species, in a manner dependent on the ethanol dehydrogenase ErdR and on rhamnolipids. Finally, we show that ethanol, as a volatile, could induce swarming in P. aeruginosa at a distance, suggesting long-range spatial effects of ethanol as a signaling molecule. IMPORTANCE P. aeruginosa, a Gram-negative opportunistic pathogen, can adapt to diverse ecological niches and exhibits several forms of social behavior. Swarming (flagellum-driven collective motility) is a collective behavior of P. aeruginosa exclusively over semisolid surfaces. However, the ecological motivations for swarming are not known. Here, we demonstrate the importance of a specific environmental cue, ethanol, produced by many microbes, in inducing swarming in the P. aeruginosa population during starvation. We show that ethanol is a signal for swarming in P. aeruginosa. Our study provides a framework to understand swarming as a chemotactic response of bacterium to a food source via a foraging signal, ethanol.

Dataset Information

Multiple Environmental Factors Influence the Importance of the Phosphodiesterase DipA upon Pseudomonas aeruginosa Swarming.

Publications

Multiple Environmental Factors Influence the Importance of the Phosphodiesterase DipA upon Pseudomonas aeruginosa Swarming.

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