Ciliate cortical organization and dynamics for cell motility: Comparing ciliates and vertebrates

Abstract

HYDRODYNAMIC flow supports a myriad of biological processes during organismal development, homeostasis, and motility. Most living organisms are equipped with multi-ciliary arrays (MCAs) to promote fluid flow. Despite being evolutionarily distant from multicellular organisms, ciliates possess a remarkably conserved ciliary and cortical architecture and therefore serve as ideal model systems for understanding the universal principles of MCAs. Adopting a ciliate and Tetrahymena thermophila-centric perspective, we highlight cytoskeletal elements that organize and stabilize MCAs. We further discuss the dynamic nature of MCAs in modulating hydrodynamic flow during environmental change.

Basal body organization and cell geometry during the cell cycle in Tetrahymena thermophila

“…, 2014 ; Junker et al. , 2019 ; Soh and Pearson, 2022 ). Moreover, these BBs organize the Tetrahymena cell cortical geometry by serving as a foundation upon which the cell cortex and the cortical cytoskeleton are organized ( Nanney, 1971a ; Frankel, 2008 ).…”

“…Motile cilia are microtubule-based organelles that undulate to produce fluid flow. In the case of multiciliated cells, tens to hundreds of motile cilia are organized into arrays that beat in a coordinated manner ( Soh and Pearson, 2022 ). This supports fluid movement along epithelia and cell mobility.…”

“…The organization of motile ciliary arrays is established by basal bodies (BBs) that support cilia formation and positioning at the cell cortex. Unique patterns of BB and cilia organization exist in multiciliated cells from different tissues and organisms ( Allen, 1967 ; Spassky and Meunier, 2017 ; Soh and Pearson, 2022 ). Moreover, the establishment of these patterns is unique such that some patterns are maintained epigenetically within an existing pattern while others are built de novo ( Sonneborn, 1964 ; Beisson and Sonneborn, 1965 ; Mitchell et al.…”

Intracellular connections between basal bodies promote the coordinated behavior of motile cilia

“…, 1984 ). Proper BB orientation in biflagellates and in multiciliary arrays is fundamental for polarized ciliary beating to drive fluid flow and cell motility ( Soh and Pearson, 2021 ). It is plausible that disoriented BBs lead to ciliary beating defects, which consequently cause the loss of cilia coordination ( Quaranta et al.…”

Intracellular connections between basal bodies promote the coordinated behavior of motile cilia

“…Notably, the loss of connections between the two BBs in vfl3 mutants is also associated with BB disorientation, whereby BBs no longer dock at the cell cortex in a polarized manner (Hoops et al, 1984). Proper BB orientation in bi-flagellates and in multi-ciliary arrays are fundamental for polarized ciliary beating to drive fluid flow and cell motility (Soh and Pearson, 2021). It is plausible that disoriented BBs lead to ciliary beating defects, which consequently cause the loss of cilia coordination (Gilpin et al, 2017b; Quaranta et al, 2015; Wan and Goldstein, 2016).…”