Spermatogenesis in a Free-Living Marine Nematode Neochromadora poecilosoma (Chromadorida,Chromadoridae) Studied Using TEM

Spermatogenesis and the structure of mature spermatozoa were studied using TEM in a free-living marine chromadorid nematode Neochromadora poecilosoma from the Sea of Japan. In spermatocytes, fibrous bodies (FB) develop; in spermatids, the synthetic apparatus lies in the residual body, while the nucleus, mitochondria, and FB are located in the main cell body (MCB). The nucleus consists of a diffuse chromatin of fibrous structure, which is not enclosed in a nuclear envelope. In the spermatid stage, the development of FB is completed, and immature spermatozoa from the proximal region of the testis do not show any structural differences from the MCB of spermatids. The mature spermatozoa are polarized cells. They attach to the uterus wall by a pseudopod filled with filaments of the cytoskeleton; in the MCB of spermatozoon, there is a nucleus surrounded by mitochondria and osmiophilic bodies. The spermatozoa of N. poecilosoma show typical ultrastructure features of sperm cells found in most studied nematodes (amoeboid nature and the absence of axoneme, acrosome, and nuclear envelope). However, no aberrant organelles characteristic of nematode spermatozoa were found throughout sperm development in N. poecilosoma and other chromadorids.     

Electron microscopic study of spermiogenesis in the free-living marine nematode <Emphasis Type="Italic">Leptosomatides marinae</Emphasis> Platonova 1976 (Enoplida: Leptosomatidae)

The ultrastructure of spermatocytes, spermatids and spermatozoa of the free-living marine nematode Leptosomatides marinae was studied by transmission electron microscopy. In early spermatids, the number of mitochondria, cisterns of the rough endoplasmic reticulum (RER) and dictyosomes increased; the number of membranous organelles (MOs) was insignificant. Later, dictyosomes and MOs filled the cytoplasm. The cytoplasm became distinctly segregated in late spermatids and the MOs concentrated around the nucleus; the mitochondria and organelles of synthesis settled on the cell periphery. Later, a densely packed conglomerate was formed from the central nucleus and a mass of MOs surrounded by an extensive zone of the cytoplasm containing mitochondria and organelles of synthesis. Early spermatozoa had an elongated nucleus surrounded by a layer of cytoplasm containing mitochondria, polarized MOs and bundles of filamentous material, which can be interpreted as fibrous bodies (FBs). The formed spermatozoa had elongated nuclei surrounded by a transparent halo; the cell periphery was a dense matrix, in which MOs and sparse mitochondria were submerged; no FBs were revealed in that phase. In general, the spermatozoa of L. marinae have the main attributes common to the Enoplida spermatozoa, availability of nuclear environment and development of the specific organelles, MOs and FBs, which are not united in complexes.     

Ultrastructure of sperm development in the free-living marine nematode Metachromadora itoi (Chromadoria, Desmodorida)

The spermatogenesis of the free‐living marine nematode Metachromadora itoi was studied with electron microscopy. Spermatocytes and early spermatids have no cytoplasmic components specific for nematodes, i.e. membranous organelles (MO) and fibrous bodies (FB). The late spermatids are subdivided into the residual body and the main cell body with a centrally located nucleus devoid of a nuclear envelope. A pair of 9 × 2 centrioles is associated with the nuclei of spermatids and spermatozoa. The nucleus of the mature spermatid is surrounded by a thick mass of radially arranged FB delimited externally by a discontinuous layer of mitochondria, which underlie a thin ectoplasm. Sperm development is accompanied by transfer of FB matter through the mitochondrion layer into the ectoplasm. The immature spermatozoa from the testis have the centrally located nucleus surrounded by a transparent halo with remnants of FB. The halo is delimited by a sphere of mitochondria that underlie the thick fibrous ectoplasm, a derivative of the FB. In the mature spermatozoa the ectoplasm is transformed into the prominent unpolarized pseudopod. The central nucleus is surrounded by a transparent halo and a sphere of mitochondria, which underlie the pseudopod. MO were not found throughout spermatogenesis. In general, spermatogenesis in M. itoi differs from that observed in many nematodes but resembles in some details the sperm development in some chromadorid and tylenchomorph nematodes. The phylogenetic importance of this sperm development is discussed.     

Ultrastructural spermatid and sperm morphology in Poecilocerus pictus (Fab.) with a reference to spermeiophagic cells in the testis and sperm duct

Electron microscopical studies were carried out on spermatid and sperm structure in P. pictus. The spermatid nuclear envelope possesses pores and is surrounded by microtubules which disappear on metamorphosis to sperm though centriolar adjunct, and its corresponding centriole comprising the basal body for flagellum. remains persistent in both. The mitochondria are arranged as two fused bodies with prominent cristae flanking the central axoneme and also contain curved end feet. In axoneme the microtubular complex is comprised of 9 + 9 (doublet) + 2 tubules + nine coarse fibres and also reveals nine radial links with electron-dense link heads. In P. pictus an alteration in temperature range, ambient for its rearing and generation of fertile spermatozoa, induces the production of sterile sperms which are characterized by multiple axonemes and mitochondrial bodies engirdled by a common plasma membrane. Presence of phagocytic cells is also an essential feature of its testis and vas deferens. These spermeiophagic cells engulf the neighbouring spermatozoa as evidenced by the fragments of axoneme, nuclei, and acrosomes in their cytoplasm.     

Fine structure of the germinating cells during the spermiogenesis of Arion rufus (Mollusca,Pulmonate Gastropoda)

Changes in spermatozoan ultrastructure have been studied during spermiogenesis of the slug Arion rufus (Gastropoda, Pulmonata, Stylommatophora). The ovotestis was investigated during the male stage, definite by the presence of spermatozoa. Some peculiar characteristics are shown by early spermatids: Around the nucleus, the nuclear envelope presents two thick layers located on opposite sides, the apical and basal plates, that will determine the antero-posterior axis of the spermatid. The chromatin, first dispersed throughout the nucleoplasm gives later on thick filaments which become attached over the inner surface of these plates. The chromatin filaments are then arranged parallel to the antero-posterior axis as the nucleus elongates. The position of the plates determines the antero-posterior axis of the spermatid. In the mature spermatozoa, the chromatin is more condensed and the nucleus presents an helical organization. The acrosome and flagellum are respectively attached externally to the center of the apical and basal plates. The acrosome consists of a membrane-bound vesicle and forms a column of homogeneous material. In the middle piece, the mitochondria have been transformed into a mitochondrial derivate by the way of a complicated metamorphosis. The axoneme is surrounded by three mitochondrial helices but only one of them contains glycogene granules. © 1996 Wiley-Liss, Inc.     

Ultrastructure of the spermatozoon of the American Alligator,Alligator mississippiensis (Reptilia: Alligatoridae)

This study details the ultrastructure of the spermatozoa of the American Alligator, Alligator mississippiensis. American Alligator spermatozoa are filiform and slightly curved. The acrosome is tapered at its anterior end and surrounded by the acrosome vesicle and an underlying subacrosomal cone, which rests just cephalic to the nuclear rostrum. One endonuclear canal extends from the subacrosomal cone through the rostral nucleus and deep into the nuclear body. The neck region separates the nucleus and midpiece and houses the proximal centriole and pericentriolar material. The distal centriole extends through the midpiece and has 9 × 3 sets of peripheral microtubules with a central doublet pair within the axoneme that is surrounded by a dense sheath. The midpiece is composed of seven to nine rings of mitochondria, which have combinations of concentrically and septate cristae. The principal piece has a dense fibrous sheath that surrounds an axoneme with a 9 + 2 microtubule arrangement. The sheath becomes significantly reduced in size caudally within the principal piece and is completely missing from the endpiece. Dense peripheral fibers, especially those associated with microtubule doublets 3 and 8, penetrate into the anterior portion of the principal piece axoneme. The data reported here hypothesize that sperm morphology is highly conserved in Crocodylia; however, specific morphological differences can exist between species. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.     

Ultrastructural analysis of spermiogenesis in Iguana iguana (Reptilia: Sauria: Iguanidae)

Spermiogenesis in the lizard, Iguana iguana, was studied by transmission and scanning electron microscopy. During this process, structures such as the acrosomal complex in the spermatid head and the axonemal complex in the mid and principal pieces of the flagellum are formed. The nuclear content is initially compacted into thick, longitudinal chromatin filaments. Nuclear shape is determined by further compaction and by the manchette, a layer of microtubules surrounding the head. The acrosomal complex originates from Golgi vesicles and the interaction between the proacrosomal vesicle and the nucleus. The midpiece consists of a pair of centrioles, surrounded by a fibrous sheath and rings of simple and modified mitochondria. The centrioles sustain the axoneme that appears at the end of the midpiece. The axoneme extends throughout the principal piece of the flagellum with the 9 + 2 pattern, still surrounded by the fibrous sheath. In the endpiece, the axoneme continues, surrounded only by the plasma membrane. In the lumen of seminiferous tubules, immature spermatozoa retain abundant residual cytoplasm.     

Spermiogenesis in the Marine Shrimp, Sicyonia ingentis

Spermiogenesis in the marine prawn Sicyonia ingentis was examined using transmission electron microscopy. The acrosomal vesicle, derived from the fusion of pro-acrosomal vesicles blebbed from the nuclear envelope, contains the membrane pouches, anterior granule and a spike. The anterior granule is formed from the coalescence of granular aggregates within the proacrosomal vesicles. Primordia underlying the apical acrosomal vesicle membrane polymerize to form a spike approximately 6 μm long. The convoluted pouch membranes arise from the posterior acrosomal vesicle membrane. Lateral and apical portions of the acrosomal vesicle are surrounded by a pentalaminar membrane comprised of the spermatid plasma membrane and the acrosomal vesicle membrane. Subacrosomal structures include the dense saucer plate, granular core and crystalline lattice. These components condense just posterior to the acrosomal vesicle and are separated from the chromatin by a nuclear plate.
The spermatid nucleus becomes surrounded by rough endoplasmic reticulum (RER) and membranous lamellar bodies. RER gives rise to smooth endoplasmic reticulum. These membrane systems degenerate, forming a band of reticular elements around the lateral and posterior portions of the nucleus. The nucleus undergoes condensation followed by decondensation with concomitant breakdown of the nuclear envelope. The resultant chromatin is fibrillar in appearance.     

Fine structure of spermiogenesis with special reference to the spermatid morulae of the freshwater mussel Prisodon alatus (Bivalvia,Unionoidea)

Within the testicular cysts of the mussel Prisodon alatus are numerous somatic host cells described as Sertoli cells (SC), each containing a variable number of young spermatid morulae. Among them, several free spermatid morulae, spermatids, and spermatozoa were observed. Each free spermatid morula is surrounded by an external membrane. The early spermatids enclosed within the morulae have dense and homogeneous chromatin, and the cytoplasm occupies little space around the nucleus. Later, during spermiogenesis, the SC show lysis and disrupt to liberate the spermatid morulae. The membrane of the free morula is then disrupted, releasing the young spermatids. The SC disappear just after the appearance in the testis of a large number of free young spermatids. The nucleus of each free spermatid becomes gradually smaller and denser by the appearance of a granular pattern of condensed chromatin. During the maturation phase of the spermatids, the cytoplasm becomes more voluminous, and mitochondria and centrioles are more evident. Then, flagellogenesis occurs, and the nucleus gradually condenses into thicker strands. In the mature sperm, the apical zone has a disc-shaped acrosomal vesicle and the midpiece contains five mitochondria and two centrioles located at the same level. The flagellum has the common 9+2 microtubular pattern. The results are discussed with particular reference to Sertoli cells and clusters of spermatid morulae with those of species of closely related taxa in the bivalves. J. Morphol. 238:63–70, 1998. © 1998 Wiley-Liss, Inc.     

Ultrastructure of the nuclear apparatus of the lower ciliateRemanella granulosa Kahl (Karyorelictida)

Summary The nuclear apparatus ofRemanella granulosa has been investigated using conventional TEM methods and Bernhard's technique of preferential RNP staining. This species has two (rarely three) macronuclei and a single micronucleus (rarely two micronuclei). The nuclei always form a single group.The macronuclei contain a fibro-granular matrix resistant to EDTA destaining, and several nucleoli and chromatin bodies. The chromatin bodies are readily bleached with EDTA and are often clustered, or even fused, forming chromocenters. The nuclei are of the compact concentric type. Some macronuclei contain nuclear bodies, as finely fibrous spheres or bundles of coarse fibers, or both. Neither type of nuclear body is destained with EDTA. The spheres are frequently associated with nucleoli. There is no evidence of any transition between the two types of nuclear bodies. The macronuclear envelope contains numerous pore complexes and is strengthened with an electron dense layer. The micronucleus is filled with spongy condensed chromatin and surrounded by an envelope with occasional pores. This nucleus lacks nucleoli and nuclear bodies.     

Spermatozoa and spermatogenesis in the northern quahaug <Emphasis Type="Italic">Mercenaria mercenaria</Emphasis> (Mollusca,Bivalvia)

We studied the ultrastructure of spermatogenesis and spermatozoa in the northern quahaug, the clam Mercenaria mercenaria. Spermatogenetic cells gradually elongate. Mitochondria gradually fuse and increase in size and electron density. During spermatid differentiation, proacrosomal vesicles migrate towards the presumptive anterior pole of the nucleus and eventually form the acrosome. The spermatozoon of M. mercenaria is of a primitive type. It is composed of head, mid-piece, and tail. The acrosome shows a subacrosomal space with a short conical contour. The slightly curved nucleus of the spermatozoon contains fine-grained dense chromatin. The middle piece consists of a centriolar complex which is surrounded by four mitochondria. The flagellum has a standard “9 + 2” microtubular structure. The ultrastructure of spermatozoa and spermatogenesis of M. mercenaria shares a number of features with other species of the family Veneridae. M. mercenaria may be a suitable model species for further investigations into the mechanisms of spermatogenesis in the Bivalvia.     

Fine structural observations on nuclear maturation during spermiogenesis in Hydra littoralis

Cytodifferentiation during spermiogenesis in Hydra littoralis was studied at the fine structural level. Concentration of nuclear material as well as specific orientation of granular and filamentous nuclear elements are apparent in two regions of the early spermatid: where the nuclear envelope is in contact with mitochondrial membranes at one pole of the cell and at an opposite region where the nucleus is closely apposed to the plasma membrane. Ultimately the mass of condensed nuclear material becomes concentrated at the mitochondrial pole of the cell. Additional electron-dense material is extruded from the nucleus into a large vacuole which is in continuity with the nuclear membrane as well as associated with Golgi lamellae and vesicles. Eventually all residual cytoplasm is sloughed, leaving the nucleus, mitochondria, and flagellum. These observations are suggestive of nucleocytoplasmic interactions during development, especially influences of mitochondria and plasma membranes on chromatin condensation.     

The structure and development of the spermatozoon of Heterakis gallinamm (Nematoda)

The structure and development of the spermatozoon of the nematode Heterakis gallinamm has been described. The spermatozoon is amoeboid. The centrioles have the unusual structure of nine single fibres. The nucleus has no limiting membrane and is surrounded by mitochondria and organelles, here called alpha bodies. These alpha bodies appear to arise from Golgi complexes in association with granular endoplasmic reticulum in the spermatocytes and have a fibrillar component which is released into the peripheral cytoplasm of the spermatid when the spermatozoon is formed. There is no refringent cone as in other ascaroid spermatozoa.     

Ultrastructural study of spermatogenesis in<Emphasis Type="Italic"> Phoronopsis harmeri</Emphasis> (Lophophorata,Phoronida)

The process of sperm development in Phoronopsis harmeri was studied by electron microscopy. Developing spermatogenical cells are aggregated around the capillaries of the haemal plexus. The spermatogonia, which are situated around the capillary walls of the caeca, are remarkable for the presence of germ-line vesicles and contain their centrioles near the cell membrane. The spermatocytes and spermatids are flagellated cells arranged in clusters. During spermiogenesis the basal body/flagellum complex migrates to the apical pole of the spermatid. The acrosome-like structure arises from material produced by the Golgi complex. It lacks a surrounding membrane and has a fibrillar content. The nucleus elongates and the condensation of chromatin is caused by an activation of 'initiation centres'. The late spermatid and the spermatozoon appear as two-armed 'V'-shaped cells in which one arm contains the nucleus and posteriorly located mitochondria, and the other one is the axoneme. Spermatogenesis of P. harmeri is an interesting example of gamete differentiation where advanced sperm structure is combined with a plesiomorphic pattern of sperm development characterized as 'flagellate spermatogenesis'. Communicated by H.-D. Franke     

Ultrastructure of Gonionchus australis (Xyalidae,Nematoda)

Observations are reported on the ultrastructure of the buccal cavity, body cuticle, spermatids, spermatozoa, male genitalia, and caudal glands of Gonionchus australis. The buccal cuticle is a continuation of the pharyngeal cuticle. Anteriorly it is secreted by arcade tissue and overlaps the mouth rim; laterally it forms longitudinal tooth ridges. The non-annulated cephalic cuticle differs sharply from the remainder of the body wall cuticle. The cortical and basal zones become much thinner, while a largely structureless, lucent median zone expands to fill the bulk of the lips and lip flaps. Spermatids possess fibrous bodies, multimembrane organelles, mitochondria, and compact chromatin. The spermatozoa of G. australis resemble those of most other nematodes by the absence of the nuclear envelope and presence of fibrous bodies, mitochondria, and compact chromafin. The ejaculatory duct possesses microvilli. Two ejaculatory glands lie beside the duct. Two neurons are located within each spicule and each part of the paired gubernaculum. Caudal gland nuclei are large, with dispersed chromatin. The ducts of all three caudal glands are filled with secretory vesicles.     

Meiosis,spindle pole body cycle,and taxonomy of the heterobasidiomycetePachnocybe ferruginea

Meiosis and the meiotic spindle pole body cycle were studied electron microscopically in basidia of the heterobasidiomycetePachnocybe ferruginea. Spindle pole body splitting in prometaphase I and II, and intermeiotic and postmeiotic duplication were investigated in particular detail. During prophase, the spindle pole body consists of two three-layered discs connected by a middle piece. At late prophase I and again in prometaphase II, the discs contact the nuclear envelope. Then, the nuclear membrane at the contact area is separated from the non-contacted part of the nuclear envelope and finally disappears. Each disc nests into the nuclear opening of the otherwise intact nuclear envelope. The disc remains in the gap and generates a half spindle. At late metaphase I, a co-disc develops eccentrically within the parent disc. The co-disc detaches from the parent disc during interphase I and becomes one of the metaphase II spindle pole bodies. Co-discs are absent during the second division. A cap of endoplasmic reticulum encloses each disc during prophase I through anaphase I. In the second meiotic division, the caps covering the spindle pole bodies of one nucleus of the pair, are developed from the neighbouring nucleus. Spindle pole bodies ofP. ferruginea are similar to those of the rusts, and especially to those ofEocronartium muscicola andHelicobasidium mompa. Part 73 of the series Studies inHeterobasidiomycetes.     

Nuclear and cytoplasmic differentiation in developing sperm of the crayfish,Cambaroides japonicus

Summary In the present electron microscopic study of spermatogenesis in the crayfish, Cambaroides japonicus, it was possible to clarify several aspects of the unusual differentiation which leads to the production of an aflagellate sperm. The centriole is followed from the metaphase of the second spermatocyte division to the time at which, in the nearly mature sperm, it appears to disintegrate. It has no connection with the acrosome but in the late spermatid and maturing sperm it is found randomly oriented among the convoluted membranes of the filamentous endoplasmic reticulum.There appears to be a close association of mitochondria with the developing acrosomal vesicle. Typical mitochondria, however, are not present after the late spermatid stage of development. It is suggested that the complex lamellar bodies associated with the nuclear envelope in the late stages of spermatogenesis may be related to mitochondria for these lamellar bodies resemble the complex mitochondria found in the adjacent nutritive cells.The development of the acrosome has been traced from an aggregate of dense granules which first appear in the interzonal spindle region and are later segregated at one side of the cell after the second spermatocyte division. As differentiation proceeds, tubular elements appear and disappear within the acrosome, while somewhat later, fibrous elements appear in the matrix. In the mature acrosome, the fibrous elements remain only adjacent to the granular periphery of the acrosome and the core again becomes homogeneous.No typical Golgi complex is found in these cells at any time during their differentiation.In the maturing sperm the development of the arms of the nucleus was studied. Preceding the differentiation of the arms a coarse fibrous material develops in the periphery of the nucleus. It is shown that the fibrillar material in the matrix of the arms is in continuity with the fibrillar material in the matrix of the nucleus proper.Supported in part by Grant No. B 2314 of the National Institute of Neurological Diseases and Blindness, U.S. Public Health Service.Predoctoral Research Fellow of the National Institute of Neurological Diseases and Blindness, U.S. Public Health Service.     

The Spermatozoon of Siboglinum (Pogonophora)

The spermatozoon and some spermatid stages of Siboglinum (Pogonophora) have been examined by light and electron microscopy. In the spermatozoon a helical acrosome, a helical nucleus and a “body” with axonema follow each other in normal sequence. Head and tail are joined by a very short neck region containing two modified centrioles. The posterior portion of the nucleus is surrounded by a mitochondrial sheath consisting of three tightly wound mitochondrial helices. In the main portion of the tail the 9+2 unit is sorrounded by a granular sheath of dense material. In the neck region a centriole adjunct develops into a dense substance containing about nine rods. At an early stage, when the centriolar apparatus and flagellum become associated with the nucleus, three large mitochondria with fairly regular cristae are seen at the base of the nucleus. A well developed Golgi apparatus is present in early stages. Rows of microtubules are observed encircling the spermatid nucleus. Compared with the primitive type of spermatozoon the pogonophore sperm shows elongated and specialized nucleus, acrosome and mitochondria. It is concluded that the ancestral form must have had a fairly primitive spermatozoon and that evolution has proceeded towards a modified sperm with complicated spiral structure in connection with the evolution of a modified biology of fertilization, viz. specialized spermatophores. It is not known how the spermatophore discharges the spermatozoa nor how the spermatozoa find their way to the eggs. Two kinds of sperms are produced in the gonads of Siboglinum. The atypical sperm is smaller than the typical one.     

Ultrastructure of sperm development in the plant-parasitic nematode Xiphinema theresiae

Spermatogenesis and sperm ultrastructure were studied by transmission electron microscopy (TEM) and scanning electron microscopy (SEM) in the longidorid Xiphinema theresiae. All germ cell stages, except spermatogonia, are present in the testes of young adult males. The nonflagellated, slightly elongated sperm displays little intraspecific variation and, although never polarized into a head and tail region, has a remarkably precise form, with a high degree of internal organization. Incipient fingerlike pseudopodia appear in the young spermatid and increase to such an extent that the adult sperm has a conspicuous “woolly” appearance. Microfilament bundles encircle the perinuclear mitochondria in the spermatid, and seem to be closely associated with the evaginated plasma membrane, especially in the spermatozoon. A large nucleus with nuclear envelope is prominent in the spermatocyte, but the envelope is absent in the young spermatid. Mitochondria are present in all germ cell stages and undergo certain morphological changes (e.g., in size and number, presence or absence of cristae), as well as changes in intracellular movements during spermatogenesis. Membranous organelles are prominent in the spermatocyte, but disappear in the older spermatid. Annulate lamellae and a residual body (i.e., cytophore) are conspicuous in the spermatocyte and spermatid, respectively; the spermatozoon clearly lacks a refringent body (i.e., acrosome).     

Studies on the polymorphic spermatozoa of a marine snail. 2. Genesis of the eupyrene sperm

Spermiogenesis of the eupyrene sperm in the snail, Fusitriton oregonensis, was studied with light and electron microscopes. Endoplasmic reticulum, which encircles the nucleus in each spermatid, appears to connect with the Golgi body and to interconnect between adjacent spermatids via cytoplasmic bridges. It is suggested that as the Golgi body migrates around the nucleus the endoplasmic reticulum may circulate with it. The alignment of the proacrosome with the nucleus is effected by a 180° rotation of the Golgi body, after which it separates and migrates posteriorly with the residual cytoplasm. Each sperm possesses a well-developed intracellular digestive system as indicated by multivesicular bodies, residual bodies, and myeloid figures. Autophagy begins in the residual cytoplasm before it is released from the middle piece. Microtubules are found outside the nucleus and mitochondria during the final stages of spermiogenesis, when elongation is almost complete. These microtubules appear to be involved in the final shaping and twisting process, in which torsion is locked in the nucleus and the mitochondria spiral around the axoneme. The annulus attaches the distal centriole to the plasma membrane in the early spermatid and as flagellar production begins they move towards the implantation fossa at the base of the nucleus. There are two centrioles in the early spermatid, the distal centriole and procentriole. The small procentriole fuses with the distal centriole in the intranuclear canal to form the centriolar cap of the basal body. This cap is pushed through the end of the nuclear tube and is separated from the subacrosomal space by only the nuclear membranes.