TY - JOUR
T1 - A dynamic basal complex modulates mammalian sperm movement
AU - Khanal, Sushil
AU - Leung, Miguel Ricardo
AU - Royfman, Abigail
AU - Fishman, Emily L
AU - Saltzman, Barbara
AU - Bloomfield-Gadêlha, Hermes
AU - Zeev-Ben-Mordehai, Tzviya
AU - Avidor-Reiss, Tomer
PY - 2021/6/21
Y1 - 2021/6/21
N2 - Reproductive success depends on efficient sperm movement driven by dynein-mediated microtubule sliding in the axoneme. Models predict sliding at the base of the tail – the centriole – but such sliding has never been observed. Centrioles are evolutionarily-ancient organelles with a conserved architecture, and their rigidity is thought to restrict microtubule sliding 1. 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. This deformation is transmitted through the DBC to the head-tail junction; as a result, the head tilts to the left, generating a kinking motion. These findings suggest that the DBC evolved to act as a mechanotransducer, coupling sperm head and tail into a single self-coordinated system. The DBC may act as a morphological computer, regulating tail beating from external feedback imparted to the head during sperm navigation. We anticipate our findings will enable studies of coordinated motion in sperm and cilia in many contexts.
AB - Reproductive success depends on efficient sperm movement driven by dynein-mediated microtubule sliding in the axoneme. Models predict sliding at the base of the tail – the centriole – but such sliding has never been observed. Centrioles are evolutionarily-ancient organelles with a conserved architecture, and their rigidity is thought to restrict microtubule sliding 1. 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. This deformation is transmitted through the DBC to the head-tail junction; as a result, the head tilts to the left, generating a kinking motion. These findings suggest that the DBC evolved to act as a mechanotransducer, coupling sperm head and tail into a single self-coordinated system. The DBC may act as a morphological computer, regulating tail beating from external feedback imparted to the head during sperm navigation. We anticipate our findings will enable studies of coordinated motion in sperm and cilia in many contexts.
KW - Reproductive Success
KW - Microtubule Sliding
KW - Axoneme
KW - Internal Sliding Deformations
KW - Tail Beating
KW - Mechanotransducer
KW - Coordinated Motion
U2 - 10.21203/rs.3.rs-136145/v1
DO - 10.21203/rs.3.rs-136145/v1
M3 - Article (Academic Journal)
SN - 2041-1723
JO - Nature Communications
JF - Nature Communications
ER -