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Phagocytosis of sperm by follicle cells of the carnivorous sponge Asbestopluma occidentalis (Porifera, Demospongiae)
Tissue and Cell 42 (2010) 198–201
Contents lists available at ScienceDirect
Tissue and Cell journal homepage: www.elsevier.com/locate/tice
Short communication
Phagocytosis of sperm by follicle cells of the carnivorous sponge Asbestopluma occidentalis (Porifera, Demospongiae) Ana Riesgo ∗ Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9
a r t i c l e
i n f o
Article history: Received 25 January 2010 Received in revised form 11 March 2010 Accepted 13 March 2010 Available online 20 April 2010 Keywords: Spermatogenesis Gametogenesis Reproduction Sertoli-like cells
a b s t r a c t During spermatogenesis of the carnivorous sponge Asbestopluma occidentalis, follicle cells that lined the spermatocysts phagocytosed unreleased mature sperm. Such follicle cells are part of the complex envelope that limits spermatocysts of A. occidentalis, which is also comprised of a collagen layer, a thick layer of intertwined cells, and spicules. Follicle cells showed vesicles containing single phagocytosed spermatozoa within their cytoplasm. Additionally, lipids and other inclusions were observed within the cytoplasm of follicle cells. It is likely that follicle cells recapture nutrients by phagocytosing spermatozoa and use them to form lipids and other inclusions. Such sperm phagocytosis is usually performed in higher invertebrates and vertebrates by Sertoli cells that are located in the testis wall. While Sertoli cells develop a wide range of functions such as creating a blood-testis barrier, providing crucial factors to ensure correct progression of spermatogenesis, and phagocytosis of aberrant, degenerating, and unreleased sperm cells, sponge follicle cells may only display phagocytotic activity on spermatogenic cells. © 2010 Elsevier Ltd. All rights reserved.
1. Introduction Phagocytosis of spermatogenic cells and mature spermatozoa by follicle cells of the testis has been documented in many invertebrates (Buckland-Nicks and Chia, 1986; Guraya, 1995; Jørgensen and Lützen, 1997; Reunov et al., 2004) and vertebrates (Griswold, 1995, 1998; Nakanishi and Shiratsuchi, 2004). In most of these animals, such follicle cells have been identified as Sertoli cells (Hinsch, 1980; Buckland-Nicks and Chia, 1986; Jørgensen and Lützen, 1997), although in marine invertebrates they have not always been called Sertoli cells, but “accessory cells”, “auxiliary cells”, “nutritive phagocytes” or “wall cells”. In order to simplify terminology, many authors propose to use the term Sertoli cells (e.g., Hinsch, 1980; Buckland-Nicks and Chia, 1986; Erkan and Sousa, 2002) to refer to those cells of invertebrates that display a function analogous to that of Sertoli cells of mammals (Hess and Franc¸a, 2005). Sertoli cells are usually located in the walls of the testes and seminiferous tubules (Hess and Franc¸a, 2005) and provide crucial factors (e.g., regulatory proteins: peptide growth factors, hormones, etc.) that facilitate the successful progression of germ cells into spermatozoa (Guraya, 1995; Griswold, 1995, 1998; Hess and Franc¸a, 2005). In addition, Sertoli cells establish the upper limit of sperm production in testis; hence, they phagocytose both degen-
∗ Present address: Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA, 02138, USA. E-mail addresses: [email protected], [email protected]. 0040-8166/$ – see front matter © 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tice.2010.03.001
erating spermatogenic cells and also regular sperm cells (Griswold, 1995; Jørgensen and Lützen, 1997; Hess and Franc¸a, 2005). Until very recently, sponges have been considered to lack follicle cells developing functions similar to those of Sertoli cells (Guraya, 1995). Nevertheless, Riesgo et al. (2008) have recently documented the occurrence of somatic cells phagocytosing sperm cells within the spermatic cysts of oviparous demosponges: Chondrilla nucula, Raspaciona aculeata, and Petrosia ficiformis. At least in R. aculeata, such cells were thought to be follicle cells that penetrate the spermatic cyst to phagocytose sperm precursors. Nevertheless, follicle cells that either regulate cell numbers in spermatic cysts or recapture nutrients by phagocytosis may not be exclusive of those three sponge species. In the present study, several mature spermatozoa were found in vesicles within follicle cells of the spermatic cysts of Asbestopluma occidentalis (LAMBE 1893), presumably indicating various events of phagocytosis. A. occidentalis is a carnivorous sponge that belongs to the family Cladorhizidae (Poecilosclerida: Demospongiae). Cladorhizids usually lack, or have a reduced aquiferous system typically found in sponges (Vacelet and Boury-Esnault, 1995; Vacelet et al., 1995; Kübler and Barthel, 1999). The aquiferous system plays an essential role in the reproduction of Porifera (see Simpson, 1984 for a review), and therefore the reproduction of carnivorous sponges is rather atypical in many features including the morphology of spermatic cysts and the process of the fertilization (see Riesgo et al., 2007 for more details). Here I show that although carnivorous sponges possess an unusual reproductive mode, basic processes that occur during the reproduction, such as the
A. Riesgo / Tissue and Cell 42 (2010) 198–201
199
Fig. 1. Phagocytosis of sperm by follicle cells of the spermatic cysts of Asbestopluma occidentalis. (A and B) The structure of the envelope of spermatic cysts: The first layer after the spermatozoa (sp) is formed by flat follicle cells (fc), then a layer of collagen (c), and finally an enveloping structure comprised of several intertwined cells (ec). Note the flat appearance of the follicle cells (fc) and the various spermatozoa contained in vesicles within the cytoplasm of the follicle cells (arrowheads). (C and D) Mature spermatozoa (white arrowheads) contained in vesicles of the follicle cells (fc). The structure of the flagellum of the spermatozoa can be observed within the vesicles (black arrowheads). Note the similar appearance of the nuclei of the spermatozoa located in the lumen of the cyst (sp) and those contained within the follicle cells (white arrowheads). (E) Higher magnification of (A). Triangular follicle cell (fc) containing two spermatozoa within its cytoplasm (arrowheads). (F) Follicle cell (fc) showing the nucleus (n), numerous lipid droplets (li) and inclusions of unknown nature (i). In both (E) and (F), note the spermatozoa located in the lumen of the cyst (sp), the layer of collagen (c) below the follicle cell (fc) layer, and the complex structure of the envelope (ec) comprised of intertwined cells.
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A. Riesgo / Tissue and Cell 42 (2010) 198–201
phagocytosis of sperm by follicle cells, are analogous to those appearing in the rest of animal groups. 2. Materials and methods Approximately 45 specimens of A. occidentalis were collected by the remote-operated vehicle ROPOS from fjord walls at 120 m depth in Barkley Sound (48◦ 53 54 N,125◦ 03 9 W) in July 2003, and by dredge at 100 m depth near Tahsis Inlet, Vancouver Island, in August 2004. For transmission electron microscopy (TEM), five specimens were fixed and prepared as described by Leys and Degnan (2002), with the only change being that all specimens were fractured in liquid nitrogen before embedding in epoxy for TEM. Specimens were viewed in a Phillips (FEI Company, Hillsboro, OR, USA) transmission electron microscope at 75 kV. Further details about sample collection and processing can be found in Riesgo et al. (2007). 3. Results In A. occidentalis, spermatogenic cells are contained in spermatic cysts (also called spermatocysts) widespread over the entire sponge tissue. A single layer of flat follicle cells limits early spermatic cysts (the ultrastructure of the follicle envelope and the sperm morphology can be found in Riesgo et al. (2007)). As development of spermatogenic cells progresses, the follicle of spermatocysts becomes more complex. Spermatocysts containing mature spermatozoa show a first single layer of flat follicle cells, then a thin layer of collagen (not shown), and finally a complex envelope consisting of several intertwined cells (Fig. 1A–C and E–F). Follicle cells are usually flat (Fig. 1C, D and F), although in some instances they appear as triangular as a result of the extension of a pseudopodium to the lumen of the cyst (Fig. 1E). Follicle cells show an oval nucleus of approximately 3–5 m in longest diameter with partially condensed chromatin (Fig. 1F). They contain lipid granules and other electron-dense inclusions with unknown nature (Fig. 1F). Most follicle cells of the mature cysts contain either one or various spermatozoa within their cytoplasm (Figs. 1A–E), presumably resulting from multiple phagocytotic events. Within the follicle cells, spermatozoa are located in slender electron-clear vesicles of 0.5–0.8 m of diameter (Fig. 1C and D). Most phagocytic vesicles contained spermatozoa still partially intact so that the body and the flagellum could be observed clearly (Fig. 1C and D). Abnormal features in the spermatozoa were not found to suggest they were aberrant or degenerating spermatozoa (Fig. 1C and D), and they are presumably randomly phagocytosed. 4. Discussion Phagocytosis of sperm by follicle cells is an important process in animal reproduction because it ensures an optimal sperm production and provides reserves after the high energy-consuming process of spermatogenesis (Griswold, 1995; Hess and Franc¸a, 2005; Guraya, 1995). Sperm phagocytosis is usually carried out by a special follicle cell called Sertoli cell (or Sertoli-like cell in some animals). Sertoli or Sertoli-like cells have not only been found in recent animals (Guraya, 1995) but also in basal invertebrates (Kutznetsov et al., 2001; Riesgo et al., 2008). The finding of sperm phagocytosis in the carnivorous poriferan A. occidentalis is remarkable because follicle cells are in charge of the process. Although such is the condition in the rest of animals, it has only been described in other sponge, R. aculeata (Riesgo et al., 2008), which belongs to the same order as A. occidentalis (Poecilosclerida). The finding is also noteworthy because sperm cells were phagocytosed prior to sperm release, again like in R. aculeata
(Riesgo et al., 2008), while in the rest of sponges sperm cells were engulfed after spawning (Riesgo et al., 2008). Reproduction is known to be a costly process in terms of energy in animals (e.g., Van Voorhies, 1992; Olsson et al., 1997). It is even more dramatic in poriferans, since many also suffer starvation because the transformation of almost all their feeding chambers into spermatocysts (Tanaka-Ichiara et al., 1990; Tsurumi and Reiswig, 1997). Therefore, it seems plausible that sponges use the recaptured nutrients from phagocytosed sperm to ensure the accomplishment of spermatogenesis (Riesgo et al., 2008). Although reproduction does not affect the feeding frequency of carnivorous sponges since they do not rely on choanocyte chambers for nourishing, phagocytosis of spermatozoa may still be oriented to nutrient recapture. Nutrients might be necessary for the survival of follicle cells, which otherwise cannot be reached by the nutrienttransporting cells (i.e., archaeocytes) because of the thick cellular envelope that surrounds them. Interestingly, follicle cells in A. occidentalis show lipid granules and other inclusions within their cytoplasm (Fig. 1F). Since such inclusions are not present in follicle cells at the beginning of spermatogenesis (Riesgo et al., 2007), they most likely derive from phagocytosed material as occurs in sperm-phagocyting cells of other sponges (Riesgo et al., 2008). Sperm phagocytosis in A. occidentalis may also be directed to achieve an appropriate cell number in spermatic cysts as occurs in many other animals (Buckland-Nicks and Chia, 1986; Jørgensen and Lützen, 1997; Hess and Franc¸a, 2005). With this new discovery, sperm phagocytosis has been proved to be widely distributed within the Class Demospongiae. To assess whether the phenomenon is inherent to the phylum or was acquired only by demosponges, studies on this aspect must be undertaken both in Calcarea and Hexactinellida. Acknowledgments I am indebted to Dr. Sally P. Leys (SPL) who kindly provided the animal samples and TEM services, and made helpful comments to improve the manuscript. This work was funded by a NSERC Discovery Grant to SPL and a fellowship of the Spanish Ministry of Science and Education (BES-2003-1789) at the University of Alberta (Department of Biological Sciences). References Buckland-Nicks, J., Chia, F.S., 1986. Fine structure of Sertoli cells in three marine snails with a discussion on the functional morphology of Sertoli cells in general. Cell Tissue Res. 245, 305–313. Erkan, M., Sousa, M., 2002. Fine structural study of the spermatogenic cycle in Pitar rudis and Chamelea gallina (Mollusca, Bivalvia, Veneridae). Tissue Cell 34, 262–272. Griswold, M.D., 1995. Interactions between Germ cells and Sertoli cells in the testis. Biol. Reprod. 52, 211–216. Griswold, M.D., 1998. The central role of Sertoli cells in spermatogenesis. Cell Dev. Biol. 9, 411–416. Guraya, S.S., 1995. The comparative cell biology of accessory somatic (or Sertoli) cells in the animal testis. Int. Rev. Cytol. 160, 163–220. Hess, R.A., Franc¸a, L.R., 2005. Structure of the Sertoli cell. In: Skinner, M.K., Griswold, M.D. (Eds.), Sertoli Cell Biology. Elsevier Academic Press, San Diego, pp. 19–40. Hinsch, G.W., 1980. Spermiogenesis in a hermit-crab, Coenobita clypeatus. II. Sertoli cells. Tissue Cell 12, 255–262. Jørgensen, C., Lützen, J., 1997. Ultrastructure of the non-germinal cells in the testes of ascidians (Urochordata) and their role in the phagocytosis of sperm. Zoomorphology 117, 103–113. Kübler, B., Barthel, D., 1999. A carnivorous sponge. Chondrocladia gigantea (Porifera: Demospongiae: Cladorhizidae), the giant deep-sea clubsponge from the Norwegian trench. Mem. Queens. Mus. 44, 289–298. Kutznetsov, S., Lyanguzowa, M., Bosch, T.C.G., 2001. Role of epithelial cells and programmed cell death in Hydra spermatogenesis. Zoology 104, 25–31. Leys, S.P., Degnan, B.M., 2002. Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invertebr. Biol. 121, 171–189. Nakanishi, Y., Shiratsuchi, A., 2004. Phagocytic removal of apoptotic spermatogenic cells by Sertoli cells: mechanisms and consequences. Biol. Pharm. Bull. 27, 13–16.
A. Riesgo / Tissue and Cell 42 (2010) 198–201 Olsson, M., Madeson, T., Shine, R., 1997. Is sperm really cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. Lond. B 264, 455–459. Reunov, A.A., Yurchenko, O.V., Kalachev, A.V., Au, D.W.T., 2004. An ultrastructural study of phagocytosis and shrinkage in nutritive phagocytes of the sea urchin Anthocidaris crassispina. Cell Tissue Res. 318, 419–428. Riesgo, A., Maldonado, M., Durfort, M., 2008. Occurrence of somatic cells within the spermatic cysts of demosponges: a discussion of their role. Tissue Cell 40, 387–396. Riesgo, A., Taylor, C., Leys, S.P., 2007. Reproduction in a carnivorous sponge: the significance of the absence of an aquiferous system to the sponge body plan. Evol. Dev. 9, 618–631. Simpson, T.L., 1984. Gamete, embryo, larval development. In: The Cell Biology of Sponges. Springer Verlag, Berlin, pp. 341–413.
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Tanaka-Ichiara, K., Watanabe, Y., Rützler, K., 1990. Gametogenic cycle of Halichondria okadai. In: New Perspective in Sponge Biology. Smithsonian Institution Press, Washington, pp. 170–174. Tsurumi, M., Reiswig, H.M., 1997. Sexual versus asexual reproduction in an oviparous rope-form sponge. Aplysina cauliformis (Porifera: Verongida). Invertebr. Reprod. Dev. 32, 1–9. Vacelet, J., Boury-Esnault, N., 1995. Carnivorous sponges. Nature 373, 333–335. Vacelet, J., Boury-Esnault, N., Fiala-Médioni, A., Fisher, C.R., 1995. A methanotrophic carnivorous sponge. Nature 377, 296. Van Voorhies, W.A., 1992. Production of sperm reduces nematode life-span. Nature 360, 456–459.
Contents lists available at ScienceDirect
Tissue and Cell journal homepage: www.elsevier.com/locate/tice
Short communication
Phagocytosis of sperm by follicle cells of the carnivorous sponge Asbestopluma occidentalis (Porifera, Demospongiae) Ana Riesgo ∗ Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9
a r t i c l e
i n f o
Article history: Received 25 January 2010 Received in revised form 11 March 2010 Accepted 13 March 2010 Available online 20 April 2010 Keywords: Spermatogenesis Gametogenesis Reproduction Sertoli-like cells
a b s t r a c t During spermatogenesis of the carnivorous sponge Asbestopluma occidentalis, follicle cells that lined the spermatocysts phagocytosed unreleased mature sperm. Such follicle cells are part of the complex envelope that limits spermatocysts of A. occidentalis, which is also comprised of a collagen layer, a thick layer of intertwined cells, and spicules. Follicle cells showed vesicles containing single phagocytosed spermatozoa within their cytoplasm. Additionally, lipids and other inclusions were observed within the cytoplasm of follicle cells. It is likely that follicle cells recapture nutrients by phagocytosing spermatozoa and use them to form lipids and other inclusions. Such sperm phagocytosis is usually performed in higher invertebrates and vertebrates by Sertoli cells that are located in the testis wall. While Sertoli cells develop a wide range of functions such as creating a blood-testis barrier, providing crucial factors to ensure correct progression of spermatogenesis, and phagocytosis of aberrant, degenerating, and unreleased sperm cells, sponge follicle cells may only display phagocytotic activity on spermatogenic cells. © 2010 Elsevier Ltd. All rights reserved.
1. Introduction Phagocytosis of spermatogenic cells and mature spermatozoa by follicle cells of the testis has been documented in many invertebrates (Buckland-Nicks and Chia, 1986; Guraya, 1995; Jørgensen and Lützen, 1997; Reunov et al., 2004) and vertebrates (Griswold, 1995, 1998; Nakanishi and Shiratsuchi, 2004). In most of these animals, such follicle cells have been identified as Sertoli cells (Hinsch, 1980; Buckland-Nicks and Chia, 1986; Jørgensen and Lützen, 1997), although in marine invertebrates they have not always been called Sertoli cells, but “accessory cells”, “auxiliary cells”, “nutritive phagocytes” or “wall cells”. In order to simplify terminology, many authors propose to use the term Sertoli cells (e.g., Hinsch, 1980; Buckland-Nicks and Chia, 1986; Erkan and Sousa, 2002) to refer to those cells of invertebrates that display a function analogous to that of Sertoli cells of mammals (Hess and Franc¸a, 2005). Sertoli cells are usually located in the walls of the testes and seminiferous tubules (Hess and Franc¸a, 2005) and provide crucial factors (e.g., regulatory proteins: peptide growth factors, hormones, etc.) that facilitate the successful progression of germ cells into spermatozoa (Guraya, 1995; Griswold, 1995, 1998; Hess and Franc¸a, 2005). In addition, Sertoli cells establish the upper limit of sperm production in testis; hence, they phagocytose both degen-
∗ Present address: Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, Cambridge, MA, 02138, USA. E-mail addresses: [email protected], [email protected]. 0040-8166/$ – see front matter © 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tice.2010.03.001
erating spermatogenic cells and also regular sperm cells (Griswold, 1995; Jørgensen and Lützen, 1997; Hess and Franc¸a, 2005). Until very recently, sponges have been considered to lack follicle cells developing functions similar to those of Sertoli cells (Guraya, 1995). Nevertheless, Riesgo et al. (2008) have recently documented the occurrence of somatic cells phagocytosing sperm cells within the spermatic cysts of oviparous demosponges: Chondrilla nucula, Raspaciona aculeata, and Petrosia ficiformis. At least in R. aculeata, such cells were thought to be follicle cells that penetrate the spermatic cyst to phagocytose sperm precursors. Nevertheless, follicle cells that either regulate cell numbers in spermatic cysts or recapture nutrients by phagocytosis may not be exclusive of those three sponge species. In the present study, several mature spermatozoa were found in vesicles within follicle cells of the spermatic cysts of Asbestopluma occidentalis (LAMBE 1893), presumably indicating various events of phagocytosis. A. occidentalis is a carnivorous sponge that belongs to the family Cladorhizidae (Poecilosclerida: Demospongiae). Cladorhizids usually lack, or have a reduced aquiferous system typically found in sponges (Vacelet and Boury-Esnault, 1995; Vacelet et al., 1995; Kübler and Barthel, 1999). The aquiferous system plays an essential role in the reproduction of Porifera (see Simpson, 1984 for a review), and therefore the reproduction of carnivorous sponges is rather atypical in many features including the morphology of spermatic cysts and the process of the fertilization (see Riesgo et al., 2007 for more details). Here I show that although carnivorous sponges possess an unusual reproductive mode, basic processes that occur during the reproduction, such as the
A. Riesgo / Tissue and Cell 42 (2010) 198–201
199
Fig. 1. Phagocytosis of sperm by follicle cells of the spermatic cysts of Asbestopluma occidentalis. (A and B) The structure of the envelope of spermatic cysts: The first layer after the spermatozoa (sp) is formed by flat follicle cells (fc), then a layer of collagen (c), and finally an enveloping structure comprised of several intertwined cells (ec). Note the flat appearance of the follicle cells (fc) and the various spermatozoa contained in vesicles within the cytoplasm of the follicle cells (arrowheads). (C and D) Mature spermatozoa (white arrowheads) contained in vesicles of the follicle cells (fc). The structure of the flagellum of the spermatozoa can be observed within the vesicles (black arrowheads). Note the similar appearance of the nuclei of the spermatozoa located in the lumen of the cyst (sp) and those contained within the follicle cells (white arrowheads). (E) Higher magnification of (A). Triangular follicle cell (fc) containing two spermatozoa within its cytoplasm (arrowheads). (F) Follicle cell (fc) showing the nucleus (n), numerous lipid droplets (li) and inclusions of unknown nature (i). In both (E) and (F), note the spermatozoa located in the lumen of the cyst (sp), the layer of collagen (c) below the follicle cell (fc) layer, and the complex structure of the envelope (ec) comprised of intertwined cells.
200
A. Riesgo / Tissue and Cell 42 (2010) 198–201
phagocytosis of sperm by follicle cells, are analogous to those appearing in the rest of animal groups. 2. Materials and methods Approximately 45 specimens of A. occidentalis were collected by the remote-operated vehicle ROPOS from fjord walls at 120 m depth in Barkley Sound (48◦ 53 54 N,125◦ 03 9 W) in July 2003, and by dredge at 100 m depth near Tahsis Inlet, Vancouver Island, in August 2004. For transmission electron microscopy (TEM), five specimens were fixed and prepared as described by Leys and Degnan (2002), with the only change being that all specimens were fractured in liquid nitrogen before embedding in epoxy for TEM. Specimens were viewed in a Phillips (FEI Company, Hillsboro, OR, USA) transmission electron microscope at 75 kV. Further details about sample collection and processing can be found in Riesgo et al. (2007). 3. Results In A. occidentalis, spermatogenic cells are contained in spermatic cysts (also called spermatocysts) widespread over the entire sponge tissue. A single layer of flat follicle cells limits early spermatic cysts (the ultrastructure of the follicle envelope and the sperm morphology can be found in Riesgo et al. (2007)). As development of spermatogenic cells progresses, the follicle of spermatocysts becomes more complex. Spermatocysts containing mature spermatozoa show a first single layer of flat follicle cells, then a thin layer of collagen (not shown), and finally a complex envelope consisting of several intertwined cells (Fig. 1A–C and E–F). Follicle cells are usually flat (Fig. 1C, D and F), although in some instances they appear as triangular as a result of the extension of a pseudopodium to the lumen of the cyst (Fig. 1E). Follicle cells show an oval nucleus of approximately 3–5 m in longest diameter with partially condensed chromatin (Fig. 1F). They contain lipid granules and other electron-dense inclusions with unknown nature (Fig. 1F). Most follicle cells of the mature cysts contain either one or various spermatozoa within their cytoplasm (Figs. 1A–E), presumably resulting from multiple phagocytotic events. Within the follicle cells, spermatozoa are located in slender electron-clear vesicles of 0.5–0.8 m of diameter (Fig. 1C and D). Most phagocytic vesicles contained spermatozoa still partially intact so that the body and the flagellum could be observed clearly (Fig. 1C and D). Abnormal features in the spermatozoa were not found to suggest they were aberrant or degenerating spermatozoa (Fig. 1C and D), and they are presumably randomly phagocytosed. 4. Discussion Phagocytosis of sperm by follicle cells is an important process in animal reproduction because it ensures an optimal sperm production and provides reserves after the high energy-consuming process of spermatogenesis (Griswold, 1995; Hess and Franc¸a, 2005; Guraya, 1995). Sperm phagocytosis is usually carried out by a special follicle cell called Sertoli cell (or Sertoli-like cell in some animals). Sertoli or Sertoli-like cells have not only been found in recent animals (Guraya, 1995) but also in basal invertebrates (Kutznetsov et al., 2001; Riesgo et al., 2008). The finding of sperm phagocytosis in the carnivorous poriferan A. occidentalis is remarkable because follicle cells are in charge of the process. Although such is the condition in the rest of animals, it has only been described in other sponge, R. aculeata (Riesgo et al., 2008), which belongs to the same order as A. occidentalis (Poecilosclerida). The finding is also noteworthy because sperm cells were phagocytosed prior to sperm release, again like in R. aculeata
(Riesgo et al., 2008), while in the rest of sponges sperm cells were engulfed after spawning (Riesgo et al., 2008). Reproduction is known to be a costly process in terms of energy in animals (e.g., Van Voorhies, 1992; Olsson et al., 1997). It is even more dramatic in poriferans, since many also suffer starvation because the transformation of almost all their feeding chambers into spermatocysts (Tanaka-Ichiara et al., 1990; Tsurumi and Reiswig, 1997). Therefore, it seems plausible that sponges use the recaptured nutrients from phagocytosed sperm to ensure the accomplishment of spermatogenesis (Riesgo et al., 2008). Although reproduction does not affect the feeding frequency of carnivorous sponges since they do not rely on choanocyte chambers for nourishing, phagocytosis of spermatozoa may still be oriented to nutrient recapture. Nutrients might be necessary for the survival of follicle cells, which otherwise cannot be reached by the nutrienttransporting cells (i.e., archaeocytes) because of the thick cellular envelope that surrounds them. Interestingly, follicle cells in A. occidentalis show lipid granules and other inclusions within their cytoplasm (Fig. 1F). Since such inclusions are not present in follicle cells at the beginning of spermatogenesis (Riesgo et al., 2007), they most likely derive from phagocytosed material as occurs in sperm-phagocyting cells of other sponges (Riesgo et al., 2008). Sperm phagocytosis in A. occidentalis may also be directed to achieve an appropriate cell number in spermatic cysts as occurs in many other animals (Buckland-Nicks and Chia, 1986; Jørgensen and Lützen, 1997; Hess and Franc¸a, 2005). With this new discovery, sperm phagocytosis has been proved to be widely distributed within the Class Demospongiae. To assess whether the phenomenon is inherent to the phylum or was acquired only by demosponges, studies on this aspect must be undertaken both in Calcarea and Hexactinellida. Acknowledgments I am indebted to Dr. Sally P. Leys (SPL) who kindly provided the animal samples and TEM services, and made helpful comments to improve the manuscript. This work was funded by a NSERC Discovery Grant to SPL and a fellowship of the Spanish Ministry of Science and Education (BES-2003-1789) at the University of Alberta (Department of Biological Sciences). References Buckland-Nicks, J., Chia, F.S., 1986. Fine structure of Sertoli cells in three marine snails with a discussion on the functional morphology of Sertoli cells in general. Cell Tissue Res. 245, 305–313. Erkan, M., Sousa, M., 2002. Fine structural study of the spermatogenic cycle in Pitar rudis and Chamelea gallina (Mollusca, Bivalvia, Veneridae). Tissue Cell 34, 262–272. Griswold, M.D., 1995. Interactions between Germ cells and Sertoli cells in the testis. Biol. Reprod. 52, 211–216. Griswold, M.D., 1998. The central role of Sertoli cells in spermatogenesis. Cell Dev. Biol. 9, 411–416. Guraya, S.S., 1995. The comparative cell biology of accessory somatic (or Sertoli) cells in the animal testis. Int. Rev. Cytol. 160, 163–220. Hess, R.A., Franc¸a, L.R., 2005. Structure of the Sertoli cell. In: Skinner, M.K., Griswold, M.D. (Eds.), Sertoli Cell Biology. Elsevier Academic Press, San Diego, pp. 19–40. Hinsch, G.W., 1980. Spermiogenesis in a hermit-crab, Coenobita clypeatus. II. Sertoli cells. Tissue Cell 12, 255–262. Jørgensen, C., Lützen, J., 1997. Ultrastructure of the non-germinal cells in the testes of ascidians (Urochordata) and their role in the phagocytosis of sperm. Zoomorphology 117, 103–113. Kübler, B., Barthel, D., 1999. A carnivorous sponge. Chondrocladia gigantea (Porifera: Demospongiae: Cladorhizidae), the giant deep-sea clubsponge from the Norwegian trench. Mem. Queens. Mus. 44, 289–298. Kutznetsov, S., Lyanguzowa, M., Bosch, T.C.G., 2001. Role of epithelial cells and programmed cell death in Hydra spermatogenesis. Zoology 104, 25–31. Leys, S.P., Degnan, B.M., 2002. Embryogenesis and metamorphosis in a haplosclerid demosponge: gastrulation and transdifferentiation of larval ciliated cells to choanocytes. Invertebr. Biol. 121, 171–189. Nakanishi, Y., Shiratsuchi, A., 2004. Phagocytic removal of apoptotic spermatogenic cells by Sertoli cells: mechanisms and consequences. Biol. Pharm. Bull. 27, 13–16.
A. Riesgo / Tissue and Cell 42 (2010) 198–201 Olsson, M., Madeson, T., Shine, R., 1997. Is sperm really cheap? Costs of reproduction in male adders, Vipera berus. Proc. R. Soc. Lond. B 264, 455–459. Reunov, A.A., Yurchenko, O.V., Kalachev, A.V., Au, D.W.T., 2004. An ultrastructural study of phagocytosis and shrinkage in nutritive phagocytes of the sea urchin Anthocidaris crassispina. Cell Tissue Res. 318, 419–428. Riesgo, A., Maldonado, M., Durfort, M., 2008. Occurrence of somatic cells within the spermatic cysts of demosponges: a discussion of their role. Tissue Cell 40, 387–396. Riesgo, A., Taylor, C., Leys, S.P., 2007. Reproduction in a carnivorous sponge: the significance of the absence of an aquiferous system to the sponge body plan. Evol. Dev. 9, 618–631. Simpson, T.L., 1984. Gamete, embryo, larval development. In: The Cell Biology of Sponges. Springer Verlag, Berlin, pp. 341–413.
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