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Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan.

ABSTRACT: Pseudomonas aeruginosa is an opportunistic pathogen often associated with chronic lung infections in individuals with the genetic disease cystic fibrosis (CF). Previous work from our laboratory revealed that five genes predicted to be important for catabolism of N-acetylglucosamine (GlcNAc) are induced during in vitro growth in CF lung secretions (sputum). Here, we demonstrate that these genes comprise an operon (referred to as the nag operon) and that NagE, a putative component of the GlcNAc phosphotransferase system, is required for growth on and uptake of GlcNAc. Using primer extension analysis, the promoter of the nag operon was mapped and shown to be inducible by GlcNAc and regulated by the transcriptional regulator NagR. Transcriptome analysis revealed that in addition to induction of the nag operon, several P. aeruginosa genes encoding factors critical for extracellular antimicrobial production are also induced by GlcNAc. Finally, we show that the GlcNAc-containing polymer peptidoglycan induces production of the antimicrobial pyocyanin. Based on this data, we propose a model in which P. aeruginosa senses surrounding bacteria by monitoring exogenous peptidoglycan and responds to this cue through enhanced production of an antimicrobial.

SUBMITTER: Korgaonkar AK

PROVIDER: S-EPMC3028681 | biostudies-literature | 2011 Feb

REPOSITORIES: biostudies-literature

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Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan.

Korgaonkar Aishwarya K AK Whiteley Marvin M

Journal of bacteriology 20101217 4

Pseudomonas aeruginosa is an opportunistic pathogen often associated with chronic lung infections in individuals with the genetic disease cystic fibrosis (CF). Previous work from our laboratory revealed that five genes predicted to be important for catabolism of N-acetylglucosamine (GlcNAc) are induced during in vitro growth in CF lung secretions (sputum). Here, we demonstrate that these genes comprise an operon (referred to as the nag operon) and that NagE, a putative component of the GlcNAc ph ...[more]

PMID: 21169497

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Project description:UnlabelledCystic fibrosis (CF) is a heritable disease characterized by chronic, polymicrobial lung infections. While Staphylococcus aureus is the dominant lung pathogen in young CF patients, Pseudomonas aeruginosa becomes predominant by adulthood. P. aeruginosa produces a variety of antimicrobials that likely contribute to this shift in microbial populations. In particular, secretion of 2-alkyl-4(1H)-quinolones (AQs) contributes to lysis of S. aureus in coculture, providing an iron source to P. aeruginosa both in vitro and in vivo. We previously showed that production of one such AQ, the Pseudomonas quinolone signal (PQS), is enhanced by iron depletion and that this induction is dependent upon the iron-responsive PrrF small RNAs (sRNAs). Here, we demonstrate that antimicrobial activity against S. aureus during coculture is also enhanced by iron depletion, and we provide evidence that multiple AQs contribute to this activity. Strikingly, a P. aeruginosa ΔprrF mutant, which produces very little PQS in monoculture, was capable of mediating iron-regulated growth suppression of S. aureus. We show that the presence of S. aureus suppresses the ΔprrF1,2 mutant's defect in iron-regulated PQS production, indicating that a PrrF-independent iron regulatory pathway mediates AQ production in coculture. We further demonstrate that iron-regulated antimicrobial production is conserved in multiple P. aeruginosa strains, including clinical isolates from CF patients. These results demonstrate that iron plays a central role in modulating interactions of P. aeruginosa with S. aureus. Moreover, our studies suggest that established iron regulatory pathways of these pathogens are significantly altered during polymicrobial infections.ImportanceChronic polymicrobial infections involving Pseudomonas aeruginosa and Staphylococcus aureus are a significant cause of morbidity and mortality, as the interplay between these two organisms exacerbates infection. This is in part due to enhanced production of antimicrobial metabolites by P. aeruginosa when these two species are cocultured. Using both established and newly developed coculture techniques, this report demonstrates that iron depletion increases P. aeruginosa's ability to suppress growth of S. aureus. These findings present a novel role for iron in modulating microbial interaction and provide the basis for understanding how essential nutrients drive polymicrobial infections.

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Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan.

Publications

Pseudomonas aeruginosa enhances production of an antimicrobial in response to N-acetylglucosamine and peptidoglycan.

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