In-Vivo Expression Profiling of Pseudomonas aeruginosa Infections Reveals Niche-Specific and Strain-Independent Transcriptional Programs

Bielecki, Piotr; Puchałka, Jacek; Wos‐Oxley, Melissa L.; Loessner, Holger; Glik, Justyna; Kawecki, Marek; Nowak, Mariusz; Tümmler, Burkhard; Weiß, Siegfried; Santos, Vítor A. P. Martins dos

doi:10.1371/journal.pone.0024235

Cited by 46 publications

(55 citation statements)

References 47 publications

(48 reference statements)

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“…The intercellular spaces in leaves are mostly filled with air [43] and very little is known about the mechanisms that plant pathogens utilize to obtain nutrients in this dry environment. Nitrogen limitation during P. aeruginosa infection in plants has been reported previously [44], [45]. One way that trehalose could promote nitrogen acquisition is by modulating host nitrogen metabolism, thereby diverting nitrogen-containing compounds to invading P. aeruginosa cells.…”

Section: Discussionmentioning

confidence: 87%

Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants

et al. 2013

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Pseudomonas aeruginosa strain PA14 is a multi-host pathogen that infects plants, nematodes, insects, and vertebrates. Many PA14 factors are required for virulence in more than one of these hosts. Noting that plants have a fundamentally different cellular architecture from animals, we sought to identify PA14 factors that are specifically required for plant pathogenesis. We show that synthesis by PA14 of the disaccharide trehalose is required for pathogenesis in Arabidopsis, but not in nematodes, insects, or mice. In-frame deletion of two closely-linked predicted trehalose biosynthetic operons, treYZ and treS, decreased growth in Arabidopsis leaves about 50 fold. Exogenously co-inoculated trehalose, ammonium, or nitrate, but not glucose, sulfate, or phosphate suppressed the phenotype of the double ΔtreYZΔtreS mutant. Exogenous trehalose or ammonium nitrate does not suppress the growth defect of the double ΔtreYZΔtreS mutant by suppressing the plant defense response. Trehalose also does not function intracellularly in P. aeruginosa to ameliorate a variety of stresses, but most likely functions extracellularly, because wild-type PA14 rescued the in vivo growth defect of the ΔtreYZΔtreS in trans. Surprisingly, the growth defect of the double ΔtreYZΔtreS double mutant was suppressed by various Arabidopsis cell wall mutants that affect xyloglucan synthesis, including an xxt1xxt2 double mutant that completely lacks xyloglucan, even though xyloglucan mutants are not more susceptible to pathogens and respond like wild-type plants to immune elicitors. An explanation of our data is that trehalose functions to promote the acquisition of nitrogen-containing nutrients in a process that involves the xyloglucan component of the plant cell wall, thereby allowing P. aeruginosa to replicate in the intercellular spaces in a leaf. This work shows how P. aeruginosa, a multi-host opportunistic pathogen, has repurposed a highly conserved “house-keeping” anabolic pathway (trehalose biosynthesis) as a potent virulence factor that allows it to replicate in the intercellular environment of a leaf.

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Section: Discussionmentioning

confidence: 87%

Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants

et al. 2013

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“…We compiled lists from six transcriptomic (2,(83)(84)(85)(86)(87) and five proteomic (88-92) investigations of differential expression between biofilm and planktonic cells. This expands on previous analyses (93)(94)(95).…”

Section: Resultsmentioning

confidence: 99%

Contribution of Stress Responses to Antibiotic Tolerance in Pseudomonas aeruginosa Biofilms

Stewart

Franklin

Williamson

et al. 2015

Antimicrob Agents Chemother

122

118

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bEnhanced tolerance of biofilm-associated bacteria to antibiotic treatments is likely due to a combination of factors, including changes in cell physiology as bacteria adapt to biofilm growth and the inherent physiological heterogeneity of biofilm bacteria. In this study, a transcriptomics approach was used to identify genes differentially expressed during biofilm growth of Pseudomonas aeruginosa. These genes were tested for statistically significant overlap, with independently compiled gene lists corresponding to stress responses and other putative antibiotic-protective mechanisms. Among the gene groups tested were those associated with biofilm response to tobramycin or ciprofloxacin, drug efflux pumps, acyl homoserine lactone quorum sensing, osmotic shock, heat shock, hypoxia stress, and stationary-phase growth. Regulons associated with Anr-mediated hypoxia stress, RpoSregulated stationary-phase growth, and osmotic stress were significantly enriched in the set of genes induced in the biofilm. Mutant strains deficient in rpoS, relA and spoT, or anr were cultured in biofilms and challenged with ciprofloxacin and tobramycin. When challenged with ciprofloxacin, the mutant strain biofilms had 2.4-to 2.9-log reductions in viable cells compared to a 0.9-log reduction of the wild-type strain. Interestingly, none of the mutants exhibited a statistically significant alteration in tobramycin susceptibility compared to that with the wild-type biofilm. These results are consistent with a model in which multiple genes controlled by overlapping starvation or stress responses contribute to the protection of a P. aeruginosa biofilm from ciprofloxacin. A distinct and as yet undiscovered mechanism protects the biofilm bacteria from tobramycin.

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“…Several studies have attempted to define the interaction dynamics between the pathogen and the host by studying gene and protein expression of either one or the other7891011. These studies have identified P. aeruginosa genes and virulence factors involved in bacterial attachment during colonization, nutrient acquisition, biofilm formation, or resistance to the immune system to facilitate persistence.…”

mentioning

confidence: 99%

Dual-seq transcriptomics reveals the battle for iron during Pseudomonas aeruginosa acute murine pneumonia

Damron

Oglesby-Sherrouse

Wilks

et al. 2016

Sci Rep

134

144

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Determining bacterial gene expression during infection is fundamental to understand pathogenesis. In this study, we used dual RNA-seq to simultaneously measure P. aeruginosa and the murine host’s gene expression and response to respiratory infection. Bacterial genes encoding products involved in metabolism and virulence were differentially expressed during infection and the type III and VI secretion systems were highly expressed in vivo. Strikingly, heme acquisition, ferric-enterobactin transport, and pyoverdine biosynthesis genes were found to be significantly up-regulated during infection. In the mouse, we profiled the acute immune response to P. aeruginosa and identified the pro-inflammatory cytokines involved in acute response to the bacterium in the lung. Additionally, we also identified numerous host iron sequestration systems upregulated during infection. Overall, this work sheds light on how P. aeruginosa triggers a pro-inflammatory response and competes for iron with the host during infection, as iron is one of the central elements for which both pathogen and host fight during acute pneumonia.

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In-Vivo Expression Profiling of Pseudomonas aeruginosa Infections Reveals Niche-Specific and Strain-Independent Transcriptional Programs

Cited by 46 publications

References 47 publications

Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants

Trehalose Biosynthesis Promotes Pseudomonas aeruginosa Pathogenicity in Plants

Contribution of Stress Responses to Antibiotic Tolerance in Pseudomonas aeruginosa Biofilms

Dual-seq transcriptomics reveals the battle for iron during Pseudomonas aeruginosa acute murine pneumonia

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