Pseudomonas aeruginosa enhances production of a non-alginate exopolysaccharide during long-term colonization of the cystic fibrosis lung

The gram-negative opportunistic pathogen Pseudomonas aeruginosa is the primary cause of chronic respiratory infections in individuals with the heritable disease cystic fibrosis (CF). These infections can last for decades, during which time P. aeruginosa has been proposed to acquire beneficial traits...

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Bibliographic Details
Published in:PloS one 2013-12, Vol.8 (12), p.e82621-e82621
Main Authors: Huse, Holly K, Kwon, Taejoon, Zlosnik, James E A, Speert, David P, Marcotte, Edward M, Whiteley, Marvin
Format: Article
Language:English
Subjects:
Adaptation
Alginic acid
Analysis
Antibiotics
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Biofilms
Biological evolution
Colonization
Cystic fibrosis
Cystic Fibrosis - microbiology
E coli
Escherichia coli
Evolution
Evolution & development
Evolutionary genetics
Fitness
Gene expression
Gene Expression Regulation, Bacterial
Genes
Genetic aspects
Genetic screening
Genomes
Genomics
Health aspects
Humans
Infection
Infections
Lungs
Molecular biology
Operons
Opportunist infection
Pathogens
Pediatrics
Polysaccharides, Bacterial - biosynthesis
Post-transcription
Production increases
Pseudomonas aeruginosa
Pseudomonas aeruginosa - genetics
Pseudomonas aeruginosa - metabolism
Pseudomonas Infections - microbiology
Reproductive fitness
RNA Processing, Post-Transcriptional
Signal transduction
Synthetic biology
Transcription (Genetics)
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Summary:The gram-negative opportunistic pathogen Pseudomonas aeruginosa is the primary cause of chronic respiratory infections in individuals with the heritable disease cystic fibrosis (CF). These infections can last for decades, during which time P. aeruginosa has been proposed to acquire beneficial traits via adaptive evolution. Because CF lacks an animal model that can acquire chronic P. aeruginosa infections, identifying genes important for long-term in vivo fitness remains difficult. However, since clonal, chronological samples can be obtained from chronically infected individuals, traits undergoing adaptive evolution can be identified. Recently we identified 24 P. aeruginosa gene expression traits undergoing parallel evolution in vivo in multiple individuals, suggesting they are beneficial to the bacterium. The goal of this study was to determine if these genes impact P. aeruginosa phenotypes important for survival in the CF lung. By using a gain-of-function genetic screen, we found that 4 genes and 2 operons undergoing parallel evolution in vivo promote P. aeruginosa biofilm formation. These genes/operons promote biofilm formation by increasing levels of the non-alginate exopolysaccharide Psl. One of these genes, phaF, enhances Psl production via a post-transcriptional mechanism, while the other 5 genes/operons do not act on either psl transcription or translation. Together, these data demonstrate that P. aeruginosa has evolved at least two pathways to over-produce a non-alginate exopolysaccharide during long-term colonization of the CF lung. More broadly, this approach allowed us to attribute a biological significance to genes with unknown function, demonstrating the power of using evolution as a guide for targeted genetic studies.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0082621