Functional significance of the outer dense fibers of mammalian sperm examined by computer simulations with the geometric clutch model.

The flagella of mammalian sperm possess certain structural characteristics that distinguish them from simple flagella. Most notable of these features are the sheath (surrounding the axoneme), the outer dense fibers of ODFs (that are attached to the outer doublets), and the connecting piece (which anchors the ODFs at the base of the flagellum). In this study, the significance of these specialized axonemal elements is explored. Their impact on microtubule sliding and force production within the axoneme is specifically analyzed. A working hypothesis is developed based on the premise that forces produced by interdoublet sliding are transferred to the ODFs. In this way, the torque required to bend the flagellum is developed between the ODFs, which are anchored in the connecting piece. This working hypothesis was incorporated into the pre-existing "geometric clutch" model that earlier simulated only cilia and simple flagella. The characteristic length and stiffness of bovine sperm flagella were specified as modelling parameters. Additionally, the inter-ODF spacing of bull sperm was incorporated to calculate doublet sliding and bending torque. The resultant computer-simulated pattern of flagellar beating possesses many of the attributes of the beat of a live bull sperm flagellum. Notably, this life-like simulation can be produced using parameters for the central axonemal "motor" that are comparable to those effective in modelling a simple flagellum. In the proposed scheme, the accessory structures of the mammalian sperm axoneme provide increased stiffness while at the same time providing a means to proportionately raise the bending torque to overcome that additional flexural rigidity. This capacity is due to the inter-ODF distances being larger than the corresponding interdoublet spacings. If force is transmitted to the flagellar base by way of the ODFs, then the larger effective diameter generates both a greater bending torque and increased interdoublet sliding. This has the interesting effect of consolidating the energy from more dynein cross-bridges into the production of a single bend. Consequently. greater bending torque development is permitted than would be possible in a simple flagellum. In This way, the same 9 + 2 organization of a simple flagellum can power a much larger (and stiffer) version than would otherwise be possible.