Parapodial glandular organs in Owenia borealis (Annelida: Oweniidae) and their possible relationship with nephridia

Abstract

Oweniidae is a basal group of recent annelids and nowadays it attracts the attention of researchers of many biological fields. Surprisingly, details of their anatomy, like the adult excretory system, remain obscure. Researchers recently suggested that the paired organs of tubeworms in the family Oweniidae are related to nephridia. In the current study of Owenia borealis adults, we determined that these structures are parapodial glandular organs (PGOs) and are located in the first two segments of adults. The PGOs are complex subepidermal multicellular glands that contain secretory cells, that is, goblet cells, which are differentiated by the type of the producing tube matter. The goblet cells are surrounded by muscles that are used to extrude material stored in the PGO's lumen into the external environment. The anterior pair of PGOs have very well‐developed rough endoplasmatic reticulum in the proximal cells, spacious Golgi complexes, numerous nail‐shaped microvilli, and apocrine secretory processes in the goblet cells of the distal parts. The posterior pair of PGOs only consists of cells, which probably produce proteinaceous fibrils. We discuss the homology of goblet cells with specific nail‐shaped microvilli that produce β‐chitin within annelids. We also discuss the possibility that PGOs and nephridia have a common origin. This study provides new information on the ultrastructure of cells that secrete the organic material used to form the tubes inhabited by tube‐dwelling annelids.

Molecular evidence for a single origin of ultrafiltration-based excretory organs

“…30 In contrast to the previous reports 30,31 that suggested loss of larval protonephridia during metamorphosis, we found that those ciliated larval organs contribute to the adult metanephridia as a pair of ciliated dorsal ducts (Figure S3A), while structures interpreted previously as metanephridial rudiments 32 are non-ciliated (Figure S3A) and probably represent prospective tube-secreting glands. 33,34 Eya, six1/2, sall, and hb were all expressed in the protonephridia of both early and advanced larvae (Figure 3B), while pou3 expression was detected in the nephridial duct only at the late larval stage (Figure 3B). Out of the four paralogs of lhx1/5 present in the transcriptome of O. fusiformis, one was detected in the developing nephridia (Figure 3B), while neither of the two osr paralogs was expressed in the nephridial tissues (Figure S2C).…”

On the Systematics and Biodiversity of the Palaeoannelida

“…The monophyly of Oweniidae is supported by embryos which do not go through the typical spiralian development, by having a unique mitraria larvae, a pair of protonephridia resembling those of deuterostomes, lacking the typical external cuticle of most annelids, possessing a monociliated epidermis and a nerve cord that is intraepidermal in some species [17,57,65,[142][143][144][145][146][147][148]. Although robust and unambiguous characters, some of the aforementioned attributes are not easily observed.…”

“…Helm et al [2,183] compared the development of oweniid neuroarchitecture with that of other annelids based on histology, SEM and immunohistochemistry and found that development and metamorphosis of the mitraria larva is mostly similar to that of other annelids irrespective of the drastic changes in body shape during metamorphosis. The central nervous system in Oweniidae is medullary, with a ring-shaped and basiepidermal brain lacking higher brain centers, ganglia associated to ventral nerve cord or complex sensory organs (Figure 21A-C) [147,148,161]. In Owenia borealis Koh, Bhaud and Jirkov, 2003, the glandular structures located in the first two segments are parapodial organs (Figures 20B,C and 21D) which contain secretory cells producing the tube materials.…”

“…In Owenia borealis Koh, Bhaud and Jirkov, 2003, the glandular structures located in the first two segments are parapodial organs (Figures 20B,C and 21D) which contain secretory cells producing the tube materials. Their relationship with the nephridial sacs located in first chaetigers of the abdominal region remains obscure and warrants further investigation [148].…”

A single origin of animal excretory organs

“…S3), while structures interpreted previously as metanephridial rudiments(27) are non-ciliated (Fig. S3) and probably represent prospective tube-secreting glands(28). Eya, six1/2, sall and hb were all expressed in the protonephridia of both early and advanced larvae (Fig.…”