Cilium evolution: identification of a novel protein, nematocilin, in the mechanosensory cilium of Hydra nematocytes.

ABSTRACT

The cnidocil at the apical end of Hydra nematocytes is a mechanosensory cilium, which acts as a "trigger" for discharge of the nematocyst capsule. The cnidocil protrudes from the center of the cnidocil apparatus and is composed of singlet and doublet microtubules surrounding an electron-dense central filament. In this paper, we identify a novel protein, nematocilin, which is localized in the central filament. Immunofluorescence staining and immunogold electron microscopy show that nematocilin forms filaments in the central core of the cnidocil. Nematocilin represents a new member of the intermediate filament superfamily. Two paralogous sequences of nematocilin are present in the Hydra genome and appear to be the result of recent gene duplication. Comparison of the exon-intron structure suggests that the nematocilin genes evolved from the nuclear lamin gene by conserving exons encoding the coiled-coil domains and replacing the C-terminal lamin domains. Molecular phylogenetic analyses also support the hypothesis of a common ancestor between lamin and nematocilin. Comparison of cnidocil structures in different cnidarians indicates that a central filament is present in the cnidocils of several hydrozoan and a cubozoan species but is absent in the cnidocils of anthozoans. A nematocilin homolog is absent in the recently completed genome of the anthozoan Nematostella. Thus, the evolution of a novel ciliary structure, which provides mechanical rigidity to the sensory cilium during the process of mechanoreception, is associated with the evolution of a novel protein.