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Surfactant protein A (SP-A) is an important lung innate immune protein that kills microbial pathogens by opsonization and membrane permeabilization. We investigated the basis of SP-A-mediated pulmonary clearance of  Pseudomonas aeruginosa  using genetically-engineered SP-A mice and a library of signature-tagged  P. aeruginosa  mutants. A mutant with an insertion into  flgE,  the gene that encodes flagellar hook protein, was preferentially cleared by the SP-A +/+  mice, but survived in the SP-A −/−  mice. Opsonization by SP-A did not play a role in  flgE  clearance. However, exposure to SP-A directly permeabilized and killed the  flgE  mutant, but not the wild-type parental strain.  P. aeruginosa  strains with mutation in other flagellar genes, as well as mucoid, nonmotile isolates from cystic fibrosis patients, were also permeabilized by SP-A. Provision of the wild-type  fliC  gene restored the resistance to SP-A-mediated membrane permeabilization in the  fliC -deficient bacteria. In addition, non-mucoid, motile revertants of CF isolates reacquired resistance to SP-A-mediated membrane permeability. Resistance to SP-A was dependent on the presence of an intact flagellar structure, and independent of flagellar-dependent motility. We provide evidence that flagellar-deficient mutants harbor inadequate amounts of LPS required to resist membrane permeabilization by SP-A and cellular lysis by detergent targeting bacterial outer membranes. Thus, the flagellum of  P. aeruginosa  plays an indirect but important role resisting SP-A-mediated clearance and membrane permeabilization.

The Flagellum of Pseudomonas aeruginosa Is Required for Resistance to Clearance by Surfactant Protein A