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The mechanism of outer membrane penetration by the eubacterial flagellum and implications for spirochete evolution

¹ Department of Biology, University of Utah, Salt Lake City, Utah 84112, USA; ² Core Research for Evolutional Science and Technology (CREST), "Soft Nano-machine Project," Kagamiyama Higashi-Hiroshima 739-0046, Japan; ³ Department of Microbiology, University of Washington Seattle, Washington 98195, USA

The rod component of the bacterial flagellum polymerizes from the inner membrane across the periplasmic space and stops at a length of 25 nm at the outer membrane. Bushing structures, the P- and L-rings, polymerize around the distal rod and form a pore in the outer membrane. The flagellar hook structure is then added to the distal rod growing outside the cell. Hook polymerization stops after the rod–hook structure reaches 80 nm in length. This study describes mutants in the distal rod protein FlgG that fail to terminate rod growth. The mutant FlgG subunits continue to polymerize close to the length of the normal rod–hook structure of 80 nm. These filamentous rod structures have multiple P-rings and fail to form the L-ring pore at the outer membrane. The flagella grow within the periplasm similar to spirochete flagella. This provides a simple method to evolve intracellular flagella as in spirochetes. The mechanism that couples rod growth termination to the ring assembly and outer membrane penetration exemplifies the importance of stopping points in the construction of a complex macromolecular machine that facilitate efficient coupling to the next step in the assembly pathway.

[Keywords: Flagellar assembly; spirochete evolution; membrane penetration]

Received May 15, 2007; revised version accepted July 23, 2007.

E-MAIL fabienne{at}biology.utah.edu; FAX (801) 581-4668.

Article published online ahead of print. Article and publication date are online at http://www.genesdev.org/cgi/doi/10.1101/gad.1571607

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