The mechanism of outer membrane penetration by the eubacterial flagellum and implications for spirochete evolution.
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 approximately 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.
Chevance
Fabienne F V
FF
Department of Biology, University of Utah, Salt Lake City, UT 84112, USA.
Takahashi
Noriko
N
Karlinsey
Joyce E
JE
Gnerer
Joshua
J
Hirano
Takanori
T
Samudrala
Ram
R
Aizawa
Shin-Ichi
S
Hughes
Kelly T
KT
D000595:Amino Acid Sequence; D001425:Bacterial Outer Membrane Proteins / Q000235:genetics / Q000378:metabolism; D001426:Bacterial Proteins / Q000737:chemistry / Q000378:metabolism / Q000502:physiology; D005075:Biological Evolution; D002462:Cell Membrane / Q000378:metabolism*; D005407:Flagella / Q000737:chemistry / Q000378:metabolism*; D008954:Models, Biological; D008958:Models, Molecular; D008969:Molecular Sequence Data; D019897:Periplasm / Q000378:metabolism; D017386:Sequence Homology, Amino Acid; D013144:Spirochaetales / Q000502:physiology*
D001425:Bacterial Outer Membrane Proteins; D001426:Bacterial Proteins; C097681:FlgE protein, Bacteria; C099486:FliK protein, Bacteria; C117211:flgFG protein, bacteria; C071266:FlgM protein, Bacteria