Phagocytosis of sperm by follicle cells of the carnivorous sponge Asbestopluma occidentalis (Porifera, Demospongiae)

Phagocytosis of sperm by follicle cells of the carnivorous sponge Asbestopluma occidentalis (Porifera, Demospongiae)
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  Tissue and Cell 42 (2010) 198–201 Contents lists available at ScienceDirect TissueandCell  journal homepage: Short communication Phagocytosis of sperm by follicle cells of the carnivorous sponge  Asbestoplumaoccidentalis  (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 2010Received in revised form 11 March 2010Accepted 13 March 2010 Available online 20 April 2010 Keywords: SpermatogenesisGametogenesisReproductionSertoli-like cells a b s t r a c t During spermatogenesis of the carnivorous sponge  Asbestopluma occidentalis , follicle cells that lined thespermatocysts phagocytosed unreleased mature sperm. Such follicle cells are part of the complex enve-lopethatlimitsspermatocystsof   A.occidentalis ,whichisalsocomprisedofacollagenlayer,athicklayerof intertwined cells, and spicules. Follicle cells showed vesicles containing single phagocytosed spermato-zoawithintheircytoplasm.Additionally,lipidsandotherinclusionswereobservedwithinthecytoplasmof follicle cells. It is likely that follicle cells recapture nutrients by phagocytosing spermatozoa and usethem to form lipids and other inclusions. Such sperm phagocytosis is usually performed in higher inver-tebrates and vertebrates by Sertoli cells that are located in the testis wall. While Sertoli cells develop awiderangeoffunctionssuchascreatingablood-testisbarrier,providingcrucialfactorstoensurecorrectprogressionofspermatogenesis,andphagocytosisofaberrant,degenerating,andunreleasedspermcells,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 spermatozoaby follicle cells of the testis has been documented in many inver-tebrates (Buckland-Nicks and Chia, 1986; Guraya, 1995; Jørgensenand Lützen, 1997; Reunov et al., 2004) and vertebrates (Griswold, 1995, 1998; Nakanishi and Shiratsuchi, 2004). In most of theseanimals, such follicle cells have been identified as Sertoli cells(Hinsch, 1980; Buckland-Nicks and Chia, 1986; Jørgensen andLützen, 1997), although in marine invertebrates they have notalways been called Sertoli cells, but “accessory cells”, “auxiliarycells”,“nutritivephagocytes”or“wallcells”.Inordertosimplifyter-minology, many authors propose to use the term Sertoli cells (e.g.,Hinsch, 1980; Buckland-Nicks and Chia, 1986; Erkan and Sousa,2002)torefertothosecellsofinvertebratesthatdisplayafunctionanalogous to that of Sertoli cells of mammals (Hess and Franc¸a,2005). Sertoli cells are usually located in the walls of the testesand 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 germcells into spermatozoa (Guraya, 1995; Griswold, 1995, 1998; HessandFranc¸a,2005).Inaddition,Sertolicellsestablishtheupperlimitofspermproductionintestis;hence,theyphagocytosebothdegen- ∗ Presentaddress:DepartmentofOrganismicandEvolutionaryBiology,Museumof Comparative Zoology, Harvard University, Cambridge, MA, 02138, USA. E-mail addresses:, eratingspermatogeniccellsandalsoregularspermcells(Griswold,1995; Jørgensen and Lützen, 1997; Hess and Franc¸a, 2005).Untilveryrecently,spongeshavebeenconsideredtolackfolliclecells developing functions similar to those of Sertoli cells (Guraya,1995).Nevertheless,Riesgoetal.(2008)haverecentlydocumented the occurrence of somatic cells phagocytosing sperm cells withinthe 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 sper-matic cyst to phagocytose sperm precursors. Nevertheless, folliclecells that either regulate cell numbers in spermatic cysts or recap-ture nutrients by phagocytosis may not be exclusive of those threesponge species.In the present study, several mature spermatozoa were foundin vesicles within follicle cells of the spermatic cysts of   Asbesto- pluma occidentalis  (LAMBE 1893), presumably indicating variousevents of phagocytosis.  A. occidentalis  is a carnivorous spongethat belongs to the family Cladorhizidae (Poecilosclerida: Demo-spongiae). Cladorhizids usually lack, or have a reduced aquiferoussystem typically found in sponges (Vacelet and Boury-Esnault,1995;Vaceletetal.,1995;KüblerandBarthel,1999).Theaquiferoussystem plays an essential role in the reproduction of Porifera (seeSimpson,1984f orareview),andthereforethereproductionofcar-nivorous sponges is rather atypical in many features including themorphology of spermatic cysts and the process of the fertilization(seeRiesgoetal.,2007f ormoredetails).HereIshowthatalthough carnivorous sponges possess an unusual reproductive mode,basic processes that occur during the reproduction, such as the 0040-8166/$ – see front matter © 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tice.2010.03.001   A. Riesgo / Tissue and Cell 42 (2010) 198–201 199 Fig.1.  Phagocytosisofspermbyfolliclecellsofthespermaticcystsof   Asbestoplumaoccidentalis .(AandB)Thestructureoftheenvelopeofspermaticcysts:Thefirstlayerafterthespermatozoa(sp)isformedbyflatfolliclecells(fc),thenalayerofcollagen(c),andfinallyanenvelopingstructurecomprisedofseveralintertwinedcells(ec).Notetheflatappearance 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).Notethesimilarappearanceofthenucleiofthespermatozoalocatedinthelumenofthecyst(sp)andthosecontainedwithinthefolliclecells(whitearrowheads).(E)Highermagnification of (A). Triangular follicle cell (fc) containing two spermatozoa within its cytoplasm (arrowheads). (F) Follicle cell (fc) showing the nucleus (n), numerous lipiddroplets (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 folliclecell (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 thoseappearing in the rest of animal groups. 2. Materials and methods Approximately 45 specimens of   A. occidentalis  were collectedby the remote-operated vehicle ROPOS from fjord walls at 120mdepth in Barkley Sound (48 ◦ 53  54  N,125 ◦ 03  9  W) in July 2003,and by dredge at 100m depth near Tahsis Inlet, Vancouver Island,in August 2004. For transmission electron microscopy (TEM), fivespecimens were fixed and prepared as described by Leys andDegnan(2002),withtheonlychangebeingthatallspecimenswerefractured in liquid nitrogen before embedding in epoxy for TEM.Specimens were viewed in a Phillips (FEI Company, Hillsboro, OR,USA) transmission electron microscope at 75kV. Further detailsabout sample collection and processing can be found in Riesgo etal. (2007). 3. Results In  A.occidentalis ,spermatogeniccellsarecontainedinspermaticcysts(alsocalledspermatocysts)widespreadovertheentirespongetissue.Asinglelayerofflatfolliclecellslimitsearlyspermaticcysts(the ultrastructure of the follicle envelope and the sperm mor-phology can be found in Riesgo et al. (2007)). As development of spermatogenic cells progresses, the follicle of spermatocystsbecomes more complex. Spermatocysts containing mature sper-matozoa show a first single layer of flat follicle cells, then a thinlayer of collagen (not shown), and finally a complex envelope con-sistingofseveralintertwinedcells(Fig.1A–CandE–F).Folliclecells are usually flat (Fig. 1C, D and F), although in some instances they appearastriangularasaresultoftheextensionofapseudopodiumtothelumenofthecyst(Fig.1E).Folliclecellsshowanovalnucleus of approximately 3–5  m in longest diameter with partially con-densed 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 var-ious spermatozoa within their cytoplasm (Figs. 1A–E), presumably resulting from multiple phagocytotic events. Within the folliclecells, 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 andthe flagellum could be observed clearly (Fig. 1C and D). Abnormal features in the spermatozoa were not found to suggest they wereaberrantordegeneratingspermatozoa(Fig.1CandD),andtheyare presumably randomly phagocytosed. 4. Discussion Phagocytosis of sperm by follicle cells is an important processin animal reproduction because it ensures an optimal sperm pro-duction and provides reserves after the high energy-consumingprocess of spermatogenesis (Griswold, 1995; Hess and Franc¸a,2005;Guraya,1995).SpermphagocytosisisusuallycarriedoutbyaspecialfolliclecellcalledSertolicell(orSertoli-likecellinsomeani-mals).SertoliorSertoli-likecellshavenotonlybeenfoundinrecentanimals(Guraya,1995)butalsoinbasalinvertebrates(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 etal., 2008), which belongs to the same order as  A. occidentalis  (Poe-cilosclerida). The finding is also noteworthy because sperm cellswere 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 sufferstarvation because the transformation of almost all their feedingchambersintospermatocysts(Tanaka-Ichiaraetal.,1990;Tsurumiand Reiswig, 1997). Therefore, it seems plausible that sponges usethe recaptured nutrients from phagocytosed sperm to ensure theaccomplishmentofspermatogenesis(Riesgoetal.,2008).Although reproduction does not affect the feeding frequency of carnivo-rous sponges since they do not rely on choanocyte chambers fornourishing, phagocytosis of spermatozoa may still be oriented tonutrientrecapture.Nutrientsmightbenecessaryforthesurvivalof follicle cells, which otherwise cannot be reached by the nutrient-transporting cells (i.e., archaeocytes) because of the thick cellularenvelope that surrounds them. Interestingly, follicle cells in  A.occidentalis  show lipid granules and other inclusions within theircytoplasm (Fig. 1F). Since such inclusions are not present in folli- cle cells at the beginning of spermatogenesis (Riesgo et al., 2007),they most likely derive from phagocytosed material as occurs insperm-phagocyting cells of other sponges (Riesgo et al., 2008).Sperm phagocytosis in  A. occidentalis  may also be directed toachieve an appropriate cell number in spermatic cysts as occursin many other animals (Buckland-Nicks and Chia, 1986; Jørgensenand Lützen, 1997; Hess and Franc¸a, 2005).With this new discovery, sperm phagocytosis has been provedto be widely distributed within the Class Demospongiae. To assesswhether the phenomenon is inherent to the phylum or wasacquired only by demosponges, studies on this aspect must beundertaken both in Calcarea and Hexactinellida.  Acknowledgments I am indebted to Dr. Sally P. Leys (SPL) who kindly provided theanimal samples and TEM services, and made helpful comments toimprove the manuscript. This work was funded by a NSERC Dis-covery Grant to SPL and a fellowship of the Spanish Ministry of ScienceandEducation(BES-2003-1789)attheUniversityofAlberta(Department of Biological Sciences). References Buckland-Nicks, J., Chia, F.S., 1986. Fine structure of Sertoli cells in three marinesnailswithadiscussiononthefunctionalmorphologyofSertolicellsingeneral.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.InteractionsbetweenGermcellsandSertolicellsinthetestis.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. 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