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Biol. Bull. 209: 31-48. (August 2005)
© 2005 Marine Biological Laboratory

Nutritive Phagocyte Incubation Chambers Provide a Structural and Nutritive Microenvironment for Germ Cells of Strongylocentrotus droebachiensis, the Green Sea Urchin

Charles W. Walker1,*, Laura M. Harrington1, Michael P. Lesser1 and Wayne R. Fagerberg2

1 Department of Zoology, Marine Biomedical Research Group and Center for Marine Biology, University of New Hampshire, Durham, New Hampshire 03824
2 Department of Plant Biology, University of New Hampshire, Durham, New Hampshire 03824

* To whom correspondence should be addressed. E-mail: cwwalker{at}christa.unh.edu

Here we characterize the germinal epithelia of both sexes of Strongylocentrotus droebachiensis, the green sea urchin, throughout its annual gametogenic cycle, using light and electron microscopy and cytochemistry. In both sexes, germinal epithelia include two interacting cellular populations: nutritive phagocytes (NPs) and germ cells. After spring spawning, NPs accumulate nutrients; amitotic oogonia and often mitotic spermatogonia occur in clusters beneath NPs; and subsequent gametogenic stages are residual or absent. During the summer, NP nutrients are mobilized for use in vitellogenesis by residual primary oocytes or to support limited spermatogenesis. In addition, some residual primary oocytes may degenerate and be phagocytized by NPs. Significant nutrient mobilization from NPs and substantial gonial cell mitoses (indicative of new gametogenesis) occur in the fall. In both sexes, all of these changes are facilitated by NPs that form basal incubation chambers near the gonadal wall and within which germ cells are surrounded by nutrients released from the NPs. In females, germ cells at several stages of gametogenesis may be housed in separate chambers in the same NP. Primary oocytes also carry out jelly coat formation, meiosis, and cortical granule translocation within NP incubation chambers. In males, many NPs cooperate to provide large continuous chambers that contain spermatogenic cells at diverse stages. In both sexes these chambers persist throughout the year and isolate gametogenesis from the gonadal lumen. NPs become slender and shorten as their nutrients are depleted. Ova or spermatozoa are stored in the gonadal lumen. Post-spawning, NPs phagocytize differentiated germ cells while simultaneously enclosing intact gonial and residual gametogenic cells in basal chambers near the gonadal wall. In light of our observations, we suggest investigating proteins that may be important in the structural, phagocytic, and nutritive functions of NPs and for which corresponding genes have already been identified in the genome of S. purpuratus, the closely related purple sea urchin.

Abbreviations: AO, amitotic oogonium • AS, amitotic spermatogonia • BPB, mercuric bromophenol blue • C, coelom • CG, cortical granules • DPO, degenerating primary oocyte • FGPO, fully grown primary oocyte • GHS, genital hemal sinus • GI, gonad index • LSS, later spermatogenic stages • MS, mitotic spermatogonia • MYP, major yolk protein • NP, nutritive phagocyte • NPIC, nutritive phagocyte incubation chamber • NS, new spermatozoa • NVPO, new vitellogenic primary oocyte • O, ovum • OL, ovarian lumen • PAS, periodic acid Schiff • RIC, residual NP incubation chamber • RVPO, residual vitellogenic primary oocyte • RSC, residual spermatogenic cells • TL, testicular lumen




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J.-F. Hamel, P. Becker, I. Eeckhaut, and A. Mercier
Exogonadal Oogenesis in a Temperate Holothurian
Biol. Bull., October 1, 2007; 213(2): 101 - 109.
[Abstract] [Full Text] [PDF]




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