The multi‐scale architecture of mammalian sperm flagella and implications for ciliary motility. (10th March 2021)

• Record Type: Journal Article
• Authors: Leung, Miguel Ricardo; Roelofs, Marc C; Ravi, Ravi Teja; Maitan, Paula; Henning, Heiko; Zhang, Min; Bromfield, Elizabeth G; Howes, Stuart C; Gadella, Bart M; Bloomfield‐Gadêlha, Hermes; Zeev‐Ben‐Mordehai, Tzviya
• Is Part Of: EMBO journal. Volume 40:Number 7(2021)
• Page Start: n/a
• Page End: n/a
• Publication Date: 2021-03-10
• Subjects: centrioles -- cryo‐electron tomography -- cryo‐FIB milling -- motile cilia -- sperm; Molecular biology -- Periodicals; 572.805
• DOI: 10.15252/embj.2020107410
• Languages: English
• ISSNs: 0261-4189

Abstract

Abstract: Motile cilia are molecular machines used by a myriad of eukaryotic cells to swim through fluid environments. However, available molecular structures represent only a handful of cell types, limiting our understanding of how cilia are modified to support motility in diverse media. Here, we use cryo‐focused ion beam milling‐enabled cryo‐electron tomography to image sperm flagella from three mammalian species. We resolve in‐cell structures of centrioles, axonemal doublets, central pair apparatus, and endpiece singlets, revealing novel protofilament‐bridging microtubule inner proteins throughout the flagellum. We present native structures of the flagellar base, which is crucial for shaping the flagellar beat. We show that outer dense fibers are directly coupled to microtubule doublets in the principal piece but not in the midpiece. Thus, mammalian sperm flagella are ornamented across scales, from protofilament‐bracing structures reinforcing microtubules at the nano‐scale to accessory structures that impose micron‐scale asymmetries on the entire assembly. Our structures provide vital foundations for linking molecular structure to ciliary motility and evolution. SYNOPSIS: Diverse organisms and cell types rely on evolutionarily ancient and structurally conserved motile cilia to swim through a broad range of fluid environments. Here, in situ cryo‐electron tomography uncovers structural specialisations of sperm flagella in several mammalian species. Mammalian sperm flagella are reinforced by micron‐scale accessory structures and nano‐scale microtubule inner proteins. The connecting piece at the base of the flagellum forms an intricate, asymmetric chamber around the sperm centrioles. The atypical distal centriole is composed of doublet microtubules splayed out around two singlet microtubules. Outer dense fibers are directly coupled to axonemal doublet microtubules in the principal piece, but not in the midpiece. Abstract : In situ cryo‐electron tomography uncovers structural specialisations of sperm flagella in several mammalian species.