The phenomenon of ciliary coordination has garnered increasing attention in recent decades and multiple theories have been proposed to explain its occurrence in different biological systems. While hydrodynamic interactions are thought to dictate the large-scale coordinated activity of epithelial cilia for fluid transport, it is rather basal coupling that accounts for synchronous swimming gaits in model microeukaryotes such as Chlamydomonas. Unicellular ciliates present a fascinating yet understudied context in which coordination is found to persist in ciliary arrays positioned across millimetre scales on the same cell. Here, we focus on the ciliate Stentor coeruleus , chosen for its large size, complex ciliary organization, and capacity for cellular regeneration. These large protists exhibit ciliary differentiation between cortical rows of short body cilia used for swimming, and an anterior ring of longer, fused cilia called the membranellar band (MB). The oral cilia in the MB beat metachronously to produce strong feeding currents. Remarkably, upon injury, the MB can be shed and regenerated de novo. Here, we follow and track this developmental sequence in its entirety to elucidate the emergence of coordinated ciliary beating: from band formation, elongation, curling and final migration towards the cell anterior. We reveal a complex interplay between hydrodynamics and ciliary restructuring in Stentor , and highlight for the first time the importance of a ring-like topology for achieving long-range metachronism in ciliated structures. This article is part of the Theo Murphy meeting issue ‘Unity and diversity of cilia in locomotion and transport’.
20The phenomenon of ciliary coordination has garnered increasing attention in recent decades, with multiple 21 theories accounting for its emergence in different contexts. The heterotrich ciliate Stentor coeruleus is a 22unicellular organism which boasts a number of features which present unrivalled opportunities for 23 biophysical studies of cilia coordination. With their cerulean colour and distinctive morphology, these large 24protists possess a characteristic differentiation between cortical rows of short body cilia used for swimming, 25and an anterior ring structure of fused oral cilia forming a membranellar band. The oral cilia beat 26 metachronously to produce strong feeding currents. In addition to this complex body plan, Stentor have 27 remarkable regenerative capabilities. Minute fragments of single cells can over the period of hours or days, 28 regenerate independently into new, proportional individuals. Certain environmental perturbations elicit a 29 unique programmed response known as oral regeneration wherein only the membranellar band is shed and 30 a new, ciliated oral primordium formed on the side of the body. Here, we target oral regeneration induced by 31sucrose-shock to reveal the complex interplay between ciliary restructuring and hydrodynamics in Stentor, 32which accompanies the complete developmental sequence from band formation, elongation, curling, and 33 migration toward the cell anterior. 34 35
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