A spider web strategy of type IV pili-mediated migration to build a fibre-like Psl polysaccharide matrix in Pseudomonas aeruginosa biofilms

• Published in: Environmental microbiology 2013-08, Vol.15 (8), p.2238-2253
• Main Authors: Wang, Shiwei, Parsek, Matthew R., Wozniak, Daniel J., Ma, Luyan Z.
• Format: Article
• Language: English
• Subjects: Alginates - metabolism; Animals; Araneae; Bacteria; Bacteriology; Biofilms - growth & development; Environmental Microbiology; Fimbriae, Bacterial - genetics; Fimbriae, Bacterial - metabolism; Flagella - genetics; Flagella - metabolism; Glucuronic Acid - metabolism; Hexuronic Acids - metabolism; Microbiology; Migration; Motility; Polysaccharides, Bacterial - genetics; Polysaccharides, Bacterial - metabolism; Pseudomonas aeruginosa; Pseudomonas aeruginosa - genetics; Pseudomonas aeruginosa - metabolism; Pseudomonas aeruginosa - physiology; Sequence Deletion
• ISSN: 1462-2912; 1462-2920
• DOI: 10.1111/1462-2920.12095

Summary Bacterial motilities participate in biofilm development. However, it is unknown how/if bacterial motility affects formation of the biofilm matrix. Psl polysaccharide is a key biofilm matrix component of Pseudomonas aeruginosa. Here we report that type IV pili (T4P)‐mediated bacterial migration leads to the formation of a fibre‐like Psl matrix. Deletion of T4P in wild type and flagella‐deficient strains results in loss of the Psl‐fibres and reduction of biofilm biomass in flow cell biofilms as well as pellicles at air‐liquid interface. Bacteria lacking T4P‐driven twitching motility including those that still express surface T4P are unable to form the Psl‐fibres. Formation of a Psl‐fibre matrix is critical for efficient biofilm formation, yet does not require flagella and polysaccharide Pel or alginate. The Psl‐fibres are likely formed by Psl released from bacteria during T4P‐mediated migration, a strategy similar to spider web formation. Starvation can couple Psl release and T4P‐driven twitching motility. Furthermore, a radial‐pattern Psl‐fibre matrix is present in the middle of biofilms, a nutrient‐deprived region. These imply a plausible model for how bacteria respond to nutrient‐limited local environment to build a polysaccharide‐fibre matrix by T4P‐dependent bacterial migration strategy. This strategy may have general significance for bacterial survival in natural and clinical settings.