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The phage-encoded PIT4 protein impacts the Pseudomonas aeruginosa type IV pili by affecting different two-component systems

ABSTRACT: Two component systems (TCSs) control a large proportion of virulence factors in Pseudomonas aeruginosa. Yet, investigations on inhibitors of regulatory pathways of TCS remain scare, despite their potential in anti-virulence strategies. This work encompasses the working mechanism of PIT4, a protein derived from the lytic P. aeruginosa phage LSL4. This viral protein inhibits bacterial motility and in particular twitching motility, while reducing the virulence of P. aeruginosa towards HeLa cells. Via differential gene expression and a yeast two-hybrid screen, PIT4 was shown to interact with components of different two component systems. In one-on-one interaction assays, it was confirmed that PIT4 interacts with the histidine kinases FleS, PilS and PA2882, through interaction with the histidine kinase domain. As such, this work highlights the potential of previously unknown phage proteins in virulence regulation of multidrug resistant pathogens that might be exploited for anti-virulence strategies and biotechnological applications.

ORGANISM(S): Pseudomonas aeruginosa

PROVIDER: GSE230851 | GEO | 2023/09/25

REPOSITORIES: GEO

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Pf4 infection alters P. aeruginosa virulence

Project description:Pf4 is a filamentous bacteriophage integrated as a prophage into the genome of Pseudomonas aeruginosa PAO1. Pf4 virions can be produced without killing P. aeruginosa. Cell lysis can however occur during superinfection when Pf virions successfully infect a host lysogenized by a Pf superinfective variant. We have previously shown that infection of P. aeruginosa PAO1 with a superinfective Pf4 variant led to abolish twitching motility and to alter biofilm’s architecture. More precisely, the cells embedded into the biofilm were showing for most of them a filamentous morphology, that could be related to the activation of the cell envelope stress response involving both the AlgU and SigX extra cytoplasmic function sigma factors. Herein, we show that Pf4 variant-infection resulted also into a drastic dysregulation of 3,360 genes representing about 58% of P. aeruginosa’s genome, of which about 43% of the virulence factors encoding genes showing a down-regulation. Accordingly, Pf4 variant infection (termed Pf4*) causes in vivo reduction of P. aeruginosa virulence, decreased production of N-acyl-homoserine lactones and 2-alkyl-4-quinolones quorum sensing molecules, and related virulence factors, such as pyocyanin, elastase, and pyoverdine. In addition to virulence encoding genes, expression of genes involved in metabolism, including energy generation and iron homeostasis, was affected, suggesting further relationships between virulence and central metabolism. Altogether, these data suggest that Pf4 phage variant infection results in complex networks dysregulations, leading to reducing acute virulence in P. aeruginosa. This work contributes to the comprehension of the bacterial response to filamentous phage infection.

2022-07-05 | GSE201738 | GEO

Inhibition of Pseudomonas aeruginosa swarming motility by 1-naphthol and other bicyclic compounds bearing hydroxyl group.

Project description:Many bacteria convert bicyclic compounds, such as indole and naphthalene, to oxidized compounds, including hydroxyindoles and naphthols. Pseudomonas aeruginosa, a ubiquitous bacterium that inhabits diverse environments, shows pathogenicity against animals, plants and other microorganisms, and increasing evidence has shown that several bicyclic compounds alter the virulence-related phenotypes of P. aeruginosa. Here, we revealed that hydroxyindoles (4- and 5-hydroxyindoles) and naphthalene derivatives bearing hydroxyl groups specifically inhibit swarming motility but have minor effects on other motilities, including swimming and twitching, in P. aeruginosa. Further analyses using 1-naphthol showed that this effect is also associated with clinically isolated hyper swarming P. aeruginosa cells. Swarming motility is associated with the dispersion of cells from biofilms, and the addition of 1-naphthol maintained biofilm biomass without cell dispersion. Swarming inhibition did not mediate rhamnolipid production, which regulates swarming motility in P. aeruginosa. Transcriptome analyses revealed that 1-naphthol increases gene expression associated with multidrug efflux and represses gene expression associated with aerotaxis and pyochelin, flagellar, and pili synthesis. In the present study, we showed that several bicyclic compounds bearing hydroxyl groups inhibit the swarming motility of P. aeruginosa, and these results provide new insight into the chemical structures that inhibit the specific phenotypes of P. aeruginosa. In total 4 samples: gene expressions of P. aeruginosa with (2 samples) or without (2 samples) 1-naphthol

2015-02-20 | E-GEOD-60343 | biostudies-arrayexpress

Inhibition of Pseudomonas aeruginosa swarming motility by 1-naphthol and other bicyclic compounds bearing hydroxyl group.

2015-02-20 | GSE60343 | GEO

Definition of the AmrZ regulon under a twitching-promoting condition

2015-09-06 | GSE68066 | GEO

The phage-encoded protein PIT2 impacts bacterial quorum sensing in Pseudomonas aeruginosa by direct interaction with LasR

Project description:Quorum sensing (QS) is the cell density-dependent virulence factor regulator in Pseudomonas aeruginosa. Here, we elucidate PIT2, a phage-encoded inhibitor of the QS regulator LasR, derived from the lytic Pseudomonas phage LMA2. PIT2 inhibits the effectors PrpL and LasA of the type 2 secretion system of P. aeruginosa and attenuates bacterial virulence towards HeLa cells and in Galleria mellonella. Using RNAseq-based differential gene expression analysis, the effect of PIT2 on the LasR regulatory network was revealed. Moreover, the specific interaction between LasR and PIT2 was determined. These data expand our knowledge on phage-encoded modulators of the bacterial metabolism, as this examples an anti-virulence protein derived from a lytic phage. From an applied perspective, this phage protein reveals and exploits an interesting anti-virulence target in P. aeruginosa. As such, it lays the foundation for a new phage-inspired anti-virulence strategy to combat multidrug resistant pathogens and opens the door for SynBio applications.

2023-09-27 | GSE227677 | GEO

Pseudomonas aeruginosa lasR QS network promotes phage infection by regulating the biosynthesis of LPS and type IV pili by regulating the biosynthesis of LPS and type IV pili

Project description:Purpose: The purpose of this study was to investigate the effect of quorum sensing on phage infection. Methods: We constructed the lasR gene knockout strain of Pseudomonas aeruginosa PAO1 and performed transcriptome sequencing.

2024-04-08 | GSE246747 | GEO

Regulation of biofilm formation, twitching motility, and virulence in Galleria mellonella by AdeN protein of Acinetobacter baumannii

Project description:AdeN deletion mutant AB141 was studied for its effects on biofilm formation, twitching motility, and virulence using phenotypic methods, and the further global role of AdeN was further studied using a multiomics approach

2016-11-04 | GSE89504 | GEO

Definition of the AmrZ regulon under a twitching-promoting condition

Project description:A novel approach using cellophane sheets was designed to promote Pseudomonas aeruginosa twitching motility, as well as to provide convenience for cell harvest. The AmrZ regulon was defined under this specific growth condition by microarray analysis. WT P. aeruginosa and amrZ mutants were cultivated under this novel condition, and their transcriptional profiles were defined. WT P. aeruginosa strains include PAO1 and WFPA510 (complemented strain), while amrZ mutants include WFPA205 (ΔamrZ) and WFPA513 (AmrZV20A, DNA binding deficient). Each strain has 3 biological replicates.

2015-09-06 | E-GEOD-68066 | biostudies-arrayexpress

Impact of phage predation on bacterial transcriptome under simulated human airway conditions

Project description:Phage therapy is a promising adjunct therapeutic approach against bacterial multidrug-resistant infections, including Pseudomonas aeruginosa-derived infections. Nevertheless, the current knowledge about the phage-bacteria interaction within a human environment is limited. In this work, we performed a transcriptome analysis of phage-infected P. aeruginosa adhered to a human epithelium (Nuli-1 ATCC® CRL-4011™). To this end, we performed RNA-sequencing from a complex mixture comprising phage–bacteria–human cells at early, middle, and late infection and compared it to uninfected adhered bacteria. Overall, we demonstrated that phage genome transcription is unaltered by bacterial growth and phage employs a core strategy of predation through upregulation of prophage-associated genes, a shutdown of bacterial surface receptors, and motility inhibition. In addition, specific responses were captured under lung-simulating conditions, with the expression of genes related to spermidine syntheses, sulfate acquisition, spermidine syntheses, biofilm formation (both alginate and polysaccharide syntheses), lipopolysaccharide (LPS) modification, pyochelin expression, and downregulation of virulence regulators. These responses should be carefully studied in detail to better discern phage-induced changes from bacterial responses against phage. Our results establish the relevance of using complex settings that mimics in vivo conditions to study phage-bacteria interplay, being obvious the phage versatility on bacterial cell invasion.

2023-05-31 | GSE213159 | GEO

ChIP-seq and RNA-seq for TCSs in Pseudomonas syringae

Project description:Bacteria relies on two-component systems (TCSs) to respond to a wide range of stimuli or environmental cues for their survival and virulence. However, the functions and synergistic actions of TCSs in genomic level remains unclear. Here, in model phytopathogen Pseudomonas syringae, by integrating multiomics data, we developed a network-based PSTCSome (Pseudomonas syringae two-component systems regulome) to identify functions and crosstalk among global TCSs under either virulence suppressing (King’s B medium, KB) or activating conditions (minimal medium, MM). Transcriptome profiling identifies 2,099 differentially expressed genes (DEGs) in KB and 1,250 DEGs in MM, while ChIP-seq identifies 1,628 target genes across the whole genome. The multiomics results are applied to perform not only gene ontology (GO) analysis to detect the biological processes that TCSs involved in, but also subnetworks and co-expression analysis of 8 virulence-related pathways to decipher the TCSs regulated pathogenic behaviors. The following phenotypic experiments newly confirmed 8 TCSs that regulates type III secretion system (T3SS) (PSPPH_0253, PSPPH_2606, PSPPH_4416, and PSPPH_4451) and surface attachment (PSPPH_0253, PSPPH_3041, PSPPH_3473, PSPPH_3736, PSPPH_4001). We then compute 259 functional genes in KB and 161 in MM for those cluster TCSs. Analysis of cluster TCSs regulons led to the identification of either novel functions or 2 master regulatory TCSs (RhpS/RhpR and PSPPH_4827/4828) toward virulence. Our results show that TCSs in P. syringae dynamically adjust their regulatory networks by sensing the external environment, and then switch bacteria between pathogenic and non-pathogenic states in a sophisticated way. Furthermore, we present an online platform of PSTCSome to facilitate updating, network visualization and user-customized analyses.

2022-10-04 | GSE148104 | GEO

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