Dataset Information

Context-Specific Requirement of Forty-Four Two-Component Loci in Pseudomonas aeruginosa Swarming.

ABSTRACT: Swarming in Pseudomonas aeruginosa is a coordinated movement of bacteria over semisolid surfaces (0.5%-0.7% agar). On soft agar, P. aeruginosa exhibits a dendritic swarm pattern, with multiple levels of branching. However, the swarm patterns typically vary depending upon the experimental design. In the present study, we show that the pattern characteristics of P. aeruginosa swarm are highly environment dependent. We define several quantifiable, macroscale features of the swarm to study the plasticity of the swarm, observed across different nutrient formulations. Furthermore, through a targeted screen of 113 two-component system (TCS) loci of the P. aeruginosa strain PA14, we show that forty-four TCS genes regulate swarming in PA14 in a contextual fashion. However, only four TCS genes-fleR, fleS, gacS, and PA14_59770-were found essential for swarming. Notably, many swarming-defective TCS mutants were found highly efficient in biofilm formation, indicating opposing roles for many TCS loci.

SUBMITTER: Kollaran AM

PROVIDER: S-EPMC6423354 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Context-Specific Requirement of Forty-Four Two-Component Loci in Pseudomonas aeruginosa Swarming.

Kollaran Ameen M AM Joge Shubham S Kotian Harshitha S HS Badal Divakar D Prakash Deep D Mishra Ayushi A Varma Manoj M Singh Varsha V

iScience 20190301

Swarming in Pseudomonas aeruginosa is a coordinated movement of bacteria over semisolid surfaces (0.5%-0.7% agar). On soft agar, P. aeruginosa exhibits a dendritic swarm pattern, with multiple levels of branching. However, the swarm patterns typically vary depending upon the experimental design. In the present study, we show that the pattern characteristics of P. aeruginosa swarm are highly environment dependent. We define several quantifiable, macroscale features of the swarm to study the plast ...[more]

PMID: 30877999

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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.

Project description:Pseudomonas aeruginosa is an opportunistic pathogen that can cause problematic infections at different sites throughout the human body. P. aeruginosa encodes a large suite of over 60 two-component signaling systems that enable cells to rapidly sense and respond to external signals. Previous work has shown that some of these sensory systems contribute to P. aeruginosa pathogenesis, but the virulence-associated processes and phenotypic traits that each of these systems controls are still largely unclear. To aid investigations of these sensory systems, we have generated deletion strains for each of 64 genes encoding histidine kinases and one histidine phosphotransferase in P. aeruginosa PA14. We carried out initial phenotypic characterizations of this collection by assaying these mutants for over a dozen virulence-associated traits, and we found that each of these phenotypes is regulated by multiple sensory systems. Our work highlights the usefulness of this collection for further studies of P. aeruginosa two-component signaling systems and provides insight into how these systems may contribute to P. aeruginosa infection.IMPORTANCEPseudomonas aeruginosa can grow and survive under a wide range of conditions, including as a human pathogen. As such, P. aeruginosa must be able to sense and respond to diverse signals and cues in its environment. This sensory capability is endowed in part by the hundreds of two-component signaling proteins encoded in the P. aeruginosa genome, but the precise roles of each remain poorly defined. To facilitate systematic study of the signaling repertoire of P. aeruginosa PA14, we generated a library of deletion strains, each lacking one of the 64 histidine kinases. By subjecting these strains to a battery of phenotypic assays, we confirmed the functions of many and unveiled roles for dozens of previously uncharacterized histidine kinases in controlling various traits, many of which are associated with P. aeruginosa virulence. Thus, this work provides new insight into the functions of two-component signaling proteins and provides a resource for future investigations.

Dataset Information

Context-Specific Requirement of Forty-Four Two-Component Loci in Pseudomonas aeruginosa Swarming.

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Context-Specific Requirement of Forty-Four Two-Component Loci in Pseudomonas aeruginosa Swarming.

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