Description of ovary organization and oogenesis in a phreodrilid clitellate

Abstract

Phreodrilidae is a small family uniting about 50 species of minute freshwater clitellate annelids inhabiting mainly the Southern hemisphere. Other than the male and spermathecal genitalia, their internal organization is poorly known. Here, we present results of our study of the ovaries and oogenesis in Insulodrilus bifidus, a phreodrilid from Western Australia using light and electron microscopy. The ovaries are paired and located in segment XII. They are inconspicuous and composed of several (10–12) spherical germ‐line cysts loosely interconnected by flattened somatic cells. The cysts usually comprise 32 germ cells and each cell is connected via a cytoplasmic bridge (ring canal) to the central cytoplasmic mass (the cytophore). In ovaries, germ cells in a given cyst develop in full synchrony. However, there is no synchrony among cysts, so there is a developmental gradient of cysts (from oogonial to early meiotic) along the longitudinal ovary axis. Within the cysts that are located in the distal end of the ovary the synchrony is finally lost and interconnected cells diversify into two morphologically distinct categories: an oocyte and 31 nurse cells. Such cysts detach from the ovaries and further development occurs within the body cavity. The oocyte gathers nutrients, mainly in form of yolk spheres, whereas nurse cells grow slightly and do not gather yolk. Organelles such as ribosomes, mitochondria and endoplasmic reticulum pass freely through the ring canals and are present within the cytophore, which suggests cytoplasmic transfer towards the oocyte. The formation of female germ‐line cysts equipped with cytophore and cells differentiated into oocyte and nurse cells matches the general pattern of oogenesis found in clitellates. In details, the ovary organization and oogenesis found in I. bifidus resembles the situation described in some representatives of Naidinae and Enchytraeidae.

Microorganization of ovaries and oogenesis of Haplotaxis sp. (Clitellata: Haplotaxidae)

“…is similar to the other oligochaetous clitellates studied to date. Ovaries in non‐leech like clitellate annelids are usually inconspicuous structures, where one end (proximal) is connected to the dissepiment, whereas the rest of the gonad is freely suspended in the segmental cavity (Stephenson, 1930; Świątek et al, 2018, 2020; Urbisz et al, 2017; Urbisz et al, 2018). In detail, the gross morphology of ovaries in oligochaetous clitellates may be different and show variety; however, with a few exceptions (Gates, 1974, 1976), these characters do not attract the researchers' attention.…”

“…In the three types—“Enchytraeus,” “Phreodrilus,” and “Stylaria,” representing the Enchytraeidae, Phreodrilidae, and Naidinae naidids, respectively—several small and almost spherical cysts composed of a low number of germ cells and a small spherical cytophore are formed. The majority of oogenesis takes place either inside the ovaries or exclusively outside—within the cysts floating in the body cavity (Gorgoń et al, 2017; Świątek et al, 2018, 2020; Urbisz et al, 2017). A different strategy is observed in “Tubifex” (described in numerous microdriles such as tubificines, limnodriloidines, propappids, and lumbriculids as well as in representatives of leech‐like branchiobdellids) and in the “Dendrobaena” types (found in lumbricid earthworms), in which the cysts are huge, multicellular and numerus nurse cells and several oocytes differentiate during oogenesis.…”

“…Recent histological and ultrastructural analyses revealed that the spatial organization (architecture) of germ‐line cysts, and as a consequence the organization and morphology of ovaries in Clitellata, may substantially differ between taxa, whereas, of particular interest, it seems to be conserved at the family/subfamily level (Świątek & Urbisz, 2019). Briefly, in non‐leech Clitellata (the organization of ovaries in Hirudinida is different and will not be discussed here, for details see (Świątek & Urbisz, 2019)), four different strategies in ovary organization have been recognized so far: Ovaries are composed of several small and almost spherical cysts; each cyst contains a small number of germ cells (30 or fewer) and the a small spherical cytophore; the majority of oogenesis may take place inside the ovaries and then only late vitellogenic oocytes detach to the coelom (in enchytraeids and phreodrilids), or oocyte growth occurs exclusively outside the ovaries within the cysts freely floating in the body cavity (in naidinae naidids; Gorgoń et al, 2017; Świątek et al, 2018; Świątek, Pinder, & Gajda, 2020; Urbisz et al, 2017). Ovaries are composed of huge multicellular (even more than 2000 cells) and polarized cysts (with developmental gradient of germ cells, distributed along the long axis of the ovary) equipped with the voluminous and branched cytophore; previtellogenic/early vitellogenic oocytes detach from the ovary and finalize yolk uptake in the body cavity; such a mode has been found in numerous microdriles such as tubificines, limnodriloidines, propappids, and lumbriculids (Urbisz et al, 2015; Urbisz et al, 2018; Urbisz & Świątek, 2013).…”

“…See text for more details. Tree topology after Erséus et al (2020) oocytes detach to the coelom (in enchytraeids and phreodrilids), or oocyte growth occurs exclusively outside the ovaries within the cysts freely floating in the body cavity (in naidinae naidids; Gorgo n et al, Świątek et al, 2018;Świątek, Pinder, & Gajda, 2020;Urbisz et al, 2017).…”

Acrylamide Exposure Destroys the Distribution and Functions of Organelles in Mouse Oocytes

“…Treatment of mouse oocytes with hydrogen peroxide induced mitochondrial dysfunction in vitro , which affects the development of mouse embryos ( Usama et al, 2020 ). If the function of ribosomes is damaged during ovary organization and oogenesis in phreodrilid clitellate, it can bring about oocyte dysfunction or abnormal fertilization ( Witek et al, 2020 ). The expression of endoplasmic reticulum stress-related proteins in mouse oocytes increased in obese mice, which led to the decrease in mouse oocyte quality and embryo development ( Rao et al, 2020 ).…”