CTENO64 is Required for Coordinated Paddling of Ciliary Comb Plate in Ctenophores

Abstract

Motile cilia are oscillating nanomachinery that are essential for cell locomotion and the generation of extracellular fluid flow. They typically comprise an axoneme with a 9+2 microtubule structure with dynein arms on each microtubule doublet that generate force by sliding between adjacent microtubules. These structures are efficient for motility and have therefore been conserved in cellular-level aquatic microflow throughout eukaryotic evolution. Diversity in the ciliary structures is seen in the basic microtubule arrangements but also in the bundling of multiple cilia, such as compound cilia. Studies on the structural diversity of cilia shed light on the mechanisms underlying ciliary formation and the biological adaptation to different aquatic environments. Ctenophores (comb jellies) have eight rows of iridescent comb plates that facilitate locomotion. A comb plate consists of tens of thousands of cilia to form a “puddle-like” ciliary plate with lengths of up to 1 mm. It exhibits structural color by light diffraction and is reported to have properties similar to photonic crystals. Here we identified a protein specific to the construction of comb plates (CTENO64). This protein is specifically present in ctenophore species and is localized on the compartmenting lamella (CL), which is the structure connecting adjacent cilia on the comb plates. Knockdown of the CTENO64 gene caused loss or misformation of CLs, resulting in aberrant waveforms in the comb plates. Our findings provide the initial characterization of a protein involved in the bundling of cilia into giant compound ciliary comb plates.

Keywords: comb jelly, ctenophore, compound cilia, plankton locomotion, dynein, axoneme