A Survival Strategy for Pseudomonas aeruginosa That Uses Exopolysaccharides To Sequester and Store Iron To Stimulate Psl-Dependent Biofilm Formation

• Published in: Applied and environmental microbiology 2016-11, Vol.82 (21), p.6403-6413
• Main Authors: Yu, Shan, Wei, Qing, Zhao, Tianhu, Guo, Yuan, Ma, Luyan Z
• Format: Article
• Language: English
• Subjects: Bacterial Proteins - metabolism; Biofilms; Biofilms - drug effects; Biofilms - growth & development; Biosynthesis; Cystic Fibrosis - microbiology; Cystic Fibrosis - therapy; Environmental Microbiology; Gene Expression Regulation, Bacterial; Glycolipids - biosynthesis; Glycolipids - metabolism; Gram-negative bacteria; Humans; Iron; Iron - metabolism; Iron - pharmacology; Iron Chelating Agents - therapeutic use; Matrix; Mutation; Polysaccharides, Bacterial - metabolism; Pseudomonas aeruginosa; Pseudomonas aeruginosa - drug effects; Pseudomonas aeruginosa - physiology; Spotlight; Survival analysis
• ISSN: 0099-2240; 1098-5336
• DOI: 10.1128/AEM.01307-16

Exopolysaccharide Psl is a critical biofilm matrix component in Pseudomonas aeruginosa, which forms a fiber-like matrix to enmesh bacterial communities. Iron is important for P. aeruginosa biofilm development, yet it is not clearly understood how iron contributes to biofilm development. Here, we showed that iron promoted biofilm formation via elevating Psl production in P. aeruginosa The high level of iron stimulated the synthesis of Psl by reducing rhamnolipid biosynthesis and inhibiting the expression of AmrZ, a repressor of psl genes. Iron-stimulated Psl biosynthesis and biofilm formation held true in mucoid P. aeruginosa strains. Subsequent experiments indicated that iron bound with Psl in vitro and in biofilms, which suggested that Psl fibers functioned as an iron storage channel in P. aeruginosa biofilms. Moreover, among three matrix exopolysaccharides of P. aeruginosa, Psl is the only exopolysaccharide that can bind with both ferrous and ferric ion, yet with higher affinity for ferrous iron. Our data suggest a survival strategy of P. aeruginosa that uses exopolysaccharide to sequester and store iron to stimulate Psl-dependent biofilm formation. Pseudomonas aeruginosa is an environmental microorganism which is also an opportunistic pathogen that can cause severe infections in immunocompromised individuals. It is the predominant airway pathogen causing morbidity and mortality in individuals affected by the genetic disease cystic fibrosis (CF). Increased airway iron and biofilm formation have been proposed to be the potential factors involved in the persistence of P. aeruginosa in CF patients. Here, we showed that a high level of iron enhanced the production of the key biofilm matrix exopolysaccharide Psl to stimulate Psl-dependent biofilm formation. Our results not only make the link between biofilm formation and iron concentration in CF, but also could guide the administration or use of iron chelators to interfere with biofilm formation in P. aeruginosa in CF patients. Furthermore, our data also imply a survival strategy of P. aeruginosa under high-iron environmental conditions.