Sensory cells and the organization of the peripheral nervous system of the siboglinid Oligobrachia haakonmosbiensis Smirnov, 2000

BMC Zool. 2022 Mar 29;7(1):16. doi: 10.1186/s40850-022-00114-z.

Abstract

Background: The nervous system of siboglinids has been studied mainly in Osedax and some Vestimentifera, while data in Frenulata - one of the four pogonophoran main branches - is still fragmentary. In most of the studies, the focus is almost always on the central nervous system, while the peripheral nervous system has traditionally received little attention. In contrast to other annelids, the structure and diversity of sensory structures in siboglinids are still quite undescribed. Meanwhile, the peripheral nervous system, as well as sensory elements, are extremely evolutionarily labile, and information about their organization is of high importance to understand lifestyles and behavior as well as main trends that lead siboglinids to their peculiar organization.

Results: The structure of the peripheric nervous system, sensory elements, and neuromuscular relationships of Oligobrachia haakonmosbiensis were studied using both scanning electron and confocal laser microscopy. A significant number of monociliary sensory cells, as well as sensory complexes located diffusely in the epithelium of the whole body were revealed. The latter include the cephalic tentacles, sensory cells accumulations along the dorsal furrow and ciliary band, areas of the openings of the tubiparous glands, and papillae. The oval ciliary spot located on the cephalic lobe at the base of the tentacles can also be regarded as a sensory organ. Most of the detected sensory cells show immunoreactivity to substance P and/or acetylated α-tubulin. FMRFamide- and serotonin-like immunoreactivity are manifested by neurons that mainly innervate tentacles, muscles, body wall epithelium, skin glands, tubiparous glands, and papillae. In the larva of O. haakonmosbiensis, monociliary sensory elements were revealed in the region of the apical organ, along the body, and on the pygidium.

Conclusions: The diversity of sensory structures in O. haakonmosbiensis comprises epidermal solitary sensory cells, sensory spots around tubiparous glands openings, and putative sensory organs such as cephalic tentacles, an oval ciliary spot on the cephalic lobe, the dorsal furrow, and papillae. Sensory structures associated with papillae and tubiparous glands play presumable mechanosensory functions and are associated with regulation of tube building as well as anchorage of the worm inside the tube. Sensory structures of the dorsal furrow are presumably engaged in the regulation of reproductive behavior. An overall low level of morphological differentiation of O. haakonmosbiensis peripheral nervous system is not typical even for annelids with the intraepithelial nervous system. This can be considered as a plesiomorphic feature of its peripheral plexus's organization, or as evidence for the neotenic origin of Siboglinidae.

Keywords: CLSM; Immunohistochemistry; Morphology; Peripheral nervous system; Pogonophora; Receptors; SEM; Siboglinidae.