Transient disruptions of axonemal structure and microtubule sliding during bend propagation by Ciona sperm flagella

Demembranated sperm flagella of Ciona were reactivated at increased salt concentrations (0.45 to 0.5 M K acetate). In addition to a decrease in amplitude of propagated bends, some flagella switch between "stable" and "transient" bending cycles. In the transient bending cycles, there is increased intermicrotubule sliding, in the direction that forms a new principal bend at the base of the flagellum, during the first half of a bending cycle. The magnitude of this increased sliding may be as much as 1 radian, or 0.06 micron between adjacent doublet microtubules. Most transient bending patterns also show a characteristic disruption of axonemal structure, involving separation between strands of microtubule doublets over a distance of up to 5 microns, occurring within a principal bend, typically about 16 microns from the base of the flagellum. The disruptions usually disappear after the principal bend propagates beyond the region of the disruption. Formation of these disruptions requires additional sliding, in the direction that would form a principal bend at the base of the flagellum, of up to about 0.3 micron. Formation of these disruptions may be explained by weakening of structural interactions by increased salt concentration and transverse forces, proportional to curvature and transmitted force, that will tend to separate doublets in a bend. These observations indicate that an actively beating flagellum possesses active sliding capability that is activated but not expressed during normal bend initiation and propagation. The initiation and propagation of flagellar bends may not be explicable solely in terms of local activation and inactivation of dynein-driven sliding.