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

Ctenophores, or comb jellies, are one of the earliest branching basal metazoan groups, whose phylogenetic position continues to be controversial. They have eight rows of iridescent structures, called comb plates, which are huge multiciliated paddle-like structures used for locomotion and uniquely found in this group of animals [1]. Despite a number of morphological and physiological studies over the past 50 years, the molecular nature of comb plates remains completely unknown. Here, we identified a protein CTENO64 that is specifically localized in the comb plates. This protein is only found in ctenophores and not in other animals or eukaryotic species that possess multiciliary cells or tissues. It is localized to regions, called compartmenting lamella (CL), which are uniquely seen in ctenophore multicilia, connecting adjacent cilia in the comb plates. Knockdown of the CTENO64 gene did not affect the formation of comb plates but caused the loss or misformation of CLs and the disruption of ciliary orientation, resulting in aberrant and non-planar waveforms in the mid-distal region of the comb plates. We propose that CLs have been convergently acquired in ctenophores to overcome the hydrodynamic constraints of possessing extremely long multicilia. Our findings provide the initial step in unveiling the molecular structure and evolutionary significance of ciliary comb plates and shed light not only on the hidden biology of ctenophores but also on the unique evolutionary pathway of these animals. VIDEO ABSTRACT.