Structural basis for curvature generation and functional specialization in spirochete flagella
Spirochetes are a distinctive phylum of spiral-shaped bacteria, defined by their curved periplasmic flagella, which drive motility by deforming the cell body and enabling efficient corkscrew-like propulsion through viscous environments. Despite their clinical importance, the molecular mechanisms underlying flagellar assembly, curvature and thus motility, remain poorly understood. Here we used cryo-electron microscopy combined with visual proteomic analysis to determine near-atomic resolution structures of two distinct flagellar filaments natively isolated from T. denticola, a major oral pathogen. Our structures reveal that filament curvature is generated by the asymmetric decoration of a conserved FlaB core by multiple sheath proteins, including FlaA1/2/3 and two previously uncharacterized proteins, termed FlaL1 and FlaL2. We show that the sheath imposes differential axial compaction on the FlaB core: FlaA1 expands the lattice at the outer curvature, FlaA2/3 compress the lattice at the inner curvature, and FlaL proteins stabilize these asymmetric interactions. Incorporation of distinct FlaB homologs contributes to assembled filament identity, with FlaB3 forming thin filaments and FlaB1/2 interacting with the sheath to form thick filaments. Comparative analysis reveals that FlaL proteins are conserved amongst some Treponema species and several other spirochetes, indicating that asymmetric assembly represents a modular solution to the mechanical demands of periplasmic flagella. These findings provide a structural framework for understanding functional specialization in bacterial filaments.