The Rise and Fall of TRP-N, an Ancient Family of Mechanogated Ion Channels, in Metazoa.

Mechanoreception, the sensing of mechanical forces, is an ancient means of orientation and communication and tightly linked to the evolution of motile animals. In flies, the transient-receptor-potential N protein (TRP-N) was found to be a cilia-associated mechanoreceptor. TRP-N belongs to a large and diverse family of ion channels. Its unusually long N-terminal repeat of 28 ankyrin domains presumably acts as the gating spring by which mechanical energy induces channel gating. We analyzed the evolutionary origins and possible diversification of TRP-N. Using a custom-made set of highly discriminative sequence profiles we scanned a representative set of metazoan genomes and subsequently corrected several gene models. We find that, contrary to other ion channel families, TRP-N is remarkably conserved in its domain arrangements and copy number (1) in all Bilateria except for amniotes, even in the wake of several whole-genome duplications. TRP-N is absent in Porifera but present in Ctenophora and Placozoa. Exceptional multiplications of TRP-N occurred in Cnidaria, independently along the Hydra and the Nematostella lineage. Molecular signals of subfunctionalization can be attributed to different mechanisms of activation of the gating spring. In Hydra this is further supported by in situ hybridization and immune staining, suggesting that at least three paralogs adapted to nematocyte discharge, which is key for predation and defense. We propose that these new candidate proteins help explain the sensory complexity of Cnidaria which has been previously observed but so far has lacked a molecular underpinning. Also, the ancient appearance of TRP-N supports a common origin of important components of the nervous systems in Ctenophores, Cnidaria, and Bilateria.

Hydrozoan nematocytes send and receive synaptic signals induced by mechano-chemical stimuli.

Nematocytes, the stinging cells of Hydrozoa, can be considered as prototypic mechanosensory hair cells bearing a concentric hair bundle, the cnidocil apparatus. These cells produce typical mechanoreceptor potentials in response to deflection of their cnidocil. Here we show that mechanosensory signals are relayed to neighbouring nematocytes via chemical neurotransmission and that nematocytes receive synaptic input from surrounding nematocytes, hair cells and probably from epithelial cells. Intracellular voltage recordings from stenotele nematocytes of capitate hydroid polyps showed two distinct types of responses when other nematocytes within the same tentacle were mechanically stimulated: (i) graded depolarizations of variable duration ('L-potentials'), and (ii) uniform impulse-like, often repetitive depolarizations ('T-potentials') that occurred in correlation with contractions of epitheliomuscular cells. Voltage clamp experiments showed that despite the stereotyped time course of T-potentials, their generation did not involve electrically excitable conductances. Instead, time course, post-stimulus delay, susceptibility to blockers of neurotransmission and gap junctions, and induction by electrical stimulation of other nematocytes indicate that L- and T-potentials are postsynaptic, most likely glutamatergic potentials. Both result from different presynaptic pathways: L-potentials are induced monosynaptically by presynaptic receptor potentials, T-potentials are most likely triggered by presynaptic action potentials propagating through the ectodermal epithelium via gap junctions. Moreover, contact-chemosensory (phospholipid) stimulation of the presynaptic nematocyte is a positive modulator of the nematocyte's afferent synaptic efficacy and of cnidocyst discharge, both triggered by mechanoreceptor potentials. The results reveal that hydrozoan nematocytes act as bimodal sensory cells, signalling coincident chemical and mechanical stimuli indicative of prey, and receive signals from other nematocytes and sensory cells.