Two distinct compartments of a ctenophore comb plate provide structural and functional integrity for the motility of giant multicilia

Abstract

Comb plates are large ciliary structures uniquely seen in comb jellies (ctenophores).1,2,3 A comb plate is constructed from tens of thousands of cilia that are bundled together by structures called compartmenting lamellae (CLs).4,5,6 We previously reported the first component of the CL, CTENO64, and found that it was specifically found in ctenophores and was essential for the determination of ciliary orientation.3 However, CTENO64 is localized only in the proximal region of the CL; therefore, the molecular architecture of the CL over the entire length of a comb plate has not been elucidated. Here, we identified a second CL component, CTENO189. This ctenophore-specific protein was present in the distal region of comb plates, with a localization clearly segregated from CTENO64. Knockdown of the CTENO189 gene using morpholino antisense oligonucleotides resulted in complete loss of CLs in the distal region of comb plates but did not affect the formation of comb plates or the orientation of each cilium. However, the hexagonal distribution of cilia was disarranged, and the metachronal coordination of comb plates along a comb row was lost in the CTENO189 morphants. The morphant comb plate showed asymmetric ciliary-type movement in normal seawater, and in a high-viscosity solution, it could not maintain the normal waveforms but showed a symmetric flagellar-type movement. Our findings demonstrated two distinct compartments of a comb plate: the proximal CL as the building foundation that rigidly fixes the ciliary orientation, and the distal CL that reinforces the elastic connection among cilia to overcome the hydrodynamic drag of giant multiciliary plates.