A dynamic basal complex modulates mammalian sperm movement

Sushil Khanal,Barbara Saltzman,Emily L Fishman,Tzviya Zeev-Ben-Mordehai,Hermes Bloomfield-Gadêlha,Abigail Royfman,Miguel Ricardo Leung,Tomer Avidor-Reiss

doi:10.1038/s41467-021-24011-0

Abstract

Reproductive success depends on efficient sperm movement driven by axonemal dynein-mediated microtubule sliding. Models predict sliding at the base of the tail – the centriole – but such sliding has never been observed. Centrioles are ancient organelles with a conserved architecture; their rigidity is thought to restrict microtubule sliding. Here, we show that, in mammalian sperm, the atypical distal centriole (DC) and its surrounding atypical pericentriolar matrix form a dynamic basal complex (DBC) that facilitates a cascade of internal sliding deformations, coupling tail beating with asymmetric head kinking. During asymmetric tail beating, the DC’s right side and its surroundings slide ~300 nm rostrally relative to the left side. The deformation throughout the DBC is transmitted to the head-tail junction; thus, the head tilts to the left, generating a kinking motion. These findings suggest that the DBC evolved as a dynamic linker coupling sperm head and tail into a single self-coordinated system.

Highlights

Reproductive success depends on efficient sperm movement driven by axonemal dyneinmediated microtubule sliding
We show that the microtubulebinding proteins FAM161A and WDR90 colocalize with the luminal and rod protein CETN1, labeling both at the distal centriole (DC) and proximal centriole (PC) in human, rabbit, and bovine sperm (Fig. 1b, c)
Like the other inner scaffold proteins, they appear mostly as two distinct rods in the DC (Fig. 1d–f, Supplementary Fig. 1a–d) and are enriched in the DC compared to the PC in all three species (Fig. 1g)

Summary

Introduction

Reproductive success depends on efficient sperm movement driven by axonemal dyneinmediated microtubule sliding. We show that, in mammalian sperm, the atypical distal centriole (DC) and its surrounding atypical pericentriolar matrix form a dynamic basal complex (DBC) that facilitates a cascade of internal sliding deformations, coupling tail beating with asymmetric head kinking. The capitulum connects to the nuclear basal plate, forming the implantation fossa at the head-tail junction (Fig. 1a) How this basal multi-component assembly supports sperm movement is unclear, but it is usually modeled as a rigid structure that anchors the tail firmly, like a clamp, to the head, with little compliance allowed by the SCs10,27 The DC movement is coordinated with the movement of the PC, SCs, and sperm head These findings suggest the sperm neck structures, the DC, PC, and SCs, form a dynamic basal complex (DBC) that transmits the tail’s microtubule sliding to the head

Methods

Results

Conclusion