Dataset Information

Involvement of flagella-driven motility and pili in Pseudomonas aeruginosa colonization at the air-liquid interface.

ABSTRACT: Many aerobic microorganisms can colonize at the air-liquid interface and form a multicellular structure, known as a pellicle. In this study, the involvement of motility and attachment traits in the Pseudomonas aeruginosa pellicle formation process was investigated. Flagella- and flagellar-motor-deficient mutants exhibited delayed pellicle formation and unusual pellicle morphology, indicating the large contribution of flagella-driven motility to structural development of the pellicle. A pili-deficient mutant showed normal pellicle formation properties, while the disruption of the pilus gene in the flagella-deficient mutant restored normal pellicle morphology. These results indicate that flagella and pili play key roles in P. aeruginosa pellicle development.

SUBMITTER: Yamamoto K

PROVIDER: S-EPMC4036044 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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Involvement of flagella-driven motility and pili in Pseudomonas aeruginosa colonization at the air-liquid interface.

Yamamoto Kyosuke K Arai Hiroyuki H Ishii Masaharu M Igarashi Yasuo Y

Microbes and environments 20120222 3

Many aerobic microorganisms can colonize at the air-liquid interface and form a multicellular structure, known as a pellicle. In this study, the involvement of motility and attachment traits in the Pseudomonas aeruginosa pellicle formation process was investigated. Flagella- and flagellar-motor-deficient mutants exhibited delayed pellicle formation and unusual pellicle morphology, indicating the large contribution of flagella-driven motility to structural development of the pellicle. A pili-defi ...[more]

PMID: 22353768

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Project description:In aquatic environments, Caulobacter spp. can be found at the boundary between liquid and air known as the neuston. I report an approach to study temporal features of Caulobacter crescentus colonization and pellicle biofilm development at the air-liquid interface and have defined the role of cell surface structures in this process. At this interface, C. crescentus initially forms a monolayer of cells bearing a surface adhesin known as the holdfast. When excised from the liquid surface, this monolayer strongly adheres to glass. The monolayer subsequently develops into a three-dimensional structure that is highly enriched in clusters of stalked cells known as rosettes. As this pellicle film matures, it becomes more cohesive and less adherent to a glass surface. A mutant strain lacking a flagellum does not efficiently reach the surface, and strains lacking type IV pili exhibit defects in organization of the three-dimensional pellicle. Strains unable to synthesize the holdfast fail to accumulate at the boundary between air and liquid and do not form a pellicle. Phase-contrast images support a model whereby the holdfast functions to trap C. crescentus cells at the air-liquid boundary. Unlike the holdfast, neither the flagellum nor type IV pili are required for C. crescentus to partition to the air-liquid interface. While it is well established that the holdfast enables adherence to solid surfaces, this study provides evidence that the holdfast has physicochemical properties that allow partitioning of nonmotile mother cells to the air-liquid interface and facilitate colonization of this microenvironment.IMPORTANCE In aquatic environments, the boundary at the air interface is often highly enriched with nutrients and oxygen. Colonization of this niche likely confers a significant fitness advantage in many cases. This study provides evidence that the cell surface adhesin known as a holdfast enables Caulobacter crescentus to partition to and colonize the air-liquid interface. Additional surface structures, including the flagellum and type IV pili, are important determinants of colonization and biofilm formation at this boundary. Considering that holdfast-like adhesins are broadly conserved in Caulobacter spp. and other members of the diverse class Alphaproteobacteria, these surface structures may function broadly to facilitate colonization of air-liquid boundaries in a range of ecological contexts, including freshwater, marine, and soil ecosystems.

Project description:Pseudomonas aeruginosa, an important opportunistic pathogen of man, exploits numerous factors for initial attachment to the host, an event required to establish bacterial infection. In this paper, we rigorously explore the role of two major bacterial adhesins, type IV pili (Tfp) and flagella, in bacterial adherence to distinct host receptors at the apical (AP) and basolateral (BL) surfaces of polarized lung epithelial cells and induction of subsequent host signaling and pathogenic events. Using an isogenic mutant of P. aeruginosa that lacks flagella or utilizing beads coated with purified Tfp, we establish that Tfp are necessary and sufficient for maximal binding to host N-glycans at the AP surface of polarized epithelium. In contrast, experiments utilizing a P. aeruginosa isogenic mutant that lacks Tfp or using beads coated with purified flagella demonstrate that flagella are necessary and sufficient for maximal binding to heparan sulfate (HS) chains of heparan sulfate proteoglycans (HSPGs) at the BL surface of polarized epithelium. Using two different cell-free systems, we demonstrate that Tfp-coated beads show highest binding affinity to complex N-glycan chains coated onto plastic plates and preferentially aggregate with beads coated with N-glycans, but not with single sugars or HS. In contrast, flagella-coated beads bind to or aggregate preferentially with HS or HSPGs, but demonstrate little binding to N-glycans. We further show that Tfp-mediated binding to host N-glycans results in activation of phosphatidylinositol 3-kinase (PI3K)/Akt pathway and bacterial entry at the AP surface. At the BL surface, flagella-mediated binding to HS activates the epidermal growth factor receptor (EGFR), adaptor protein Shc, and PI3K/Akt, and induces bacterial entry. Remarkably, flagella-coated beads alone can activate EGFR and Shc. Together, this work provides new insights into the intricate interactions between P. aeruginosa and lung epithelium that may be potentially useful in the development of novel treatments for P. aeruginosa infections.

Dataset Information

Involvement of flagella-driven motility and pili in Pseudomonas aeruginosa colonization at the air-liquid interface.

Publications

Involvement of flagella-driven motility and pili in Pseudomonas aeruginosa colonization at the air-liquid interface.

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