Syst Parasitol (2010) 77:163–174 DOI 10.1007/s11230-010-9267-6
Ultrastructure of the ovary of Amphilina japonica Goto & Ishii, 1936 (Cestoda) and its implications for phylogenetic studies Larisa G. Poddubnaya • Willi E. R. Xylander
Received: 20 April 2010 / Accepted: 23 June 2010 Ó Springer Science+Business Media B.V. 2010
Abstract The ultrastructure of the ovary of the amphilinidean cestode Amphilina japonica Goto & Ishii, 1936 from the body-cavity of the American sturgeon Acipenser transmontanus Richardson is described using transmission electron microscopy. The characters of the ovary of Amphilina japonica are different from those of all other cestodes. The most important difference is in the nature of the relationship between the germ and accessory cells within the ovary. In A. japonica the oocytes and accessory cells form numerous different intercellular contacts (desmosome-like junctions and zonulae adherentes). Gap junctions are present between the narrow cytoplasmic processes of the accessory cells. Numerous micropinocytotic vesicles and vacuoles from the accessory cells discharge their content into spaces between the oocytes and the accessory cells. The accessory cells are closely associated with the oocytes during the early and middle stages of oogenesis. As the volume of oocytes increases, the accessory cells gradually lose their association with the oocyte surfaces. Peripherally located individual
L. G. Poddubnaya (&) Institute of Biology of Inland Waters, Russian Academy of Sciences, Borok, Yaroslavl Province, Russia 152742 e-mail:
[email protected] W. E. R. Xylander Senckenberg Museum fu¨r Naturkunde Go¨rlitz, Postfach 300 154, 02806 Go¨rlitz, Germany
accessory cells of A. japonica give rise to a cellular epithelial layer of irregular shape and thickness which breaks down via numerous invaginations of the basal membrane and underlying basal matrix. The different arrangements of the interconnection of cell components in the Amphilinidea compared with the Gyrocotylidea and Eucestoda (the absence of specialised cell contacts and the syncytial nature of the accessory ‘interstitial’ cells) are evidence suggesting the presence of unrelated groups within the Cestoda. The nature of the association of the accessory and germ cells in ovary of A. japonica more closely resembles the ovary of non-platyhelminth invertebrates rather than that of other neodermatans.
Introduction The Amphilinidea Poche, 1922 represents a group of flatworms which occur as adult parasites in teleosts, chondrosteans and chelonians. Most authors support a view that amphilinideans belong to the Cestoda (Ehlers, 1985; Brooks et al., 1985; Brooks, 1989; Rohde; 1990; Rohde et al., 1995; Xylander, 2001; Lockyer et al., 2003), although there is an alternative opinion that they represent a separate class, the Amphilinida, within the parasitic flatworms (Bychowsky, 1957; Dubinina, 1982; Galkin, 1999). Janicki (1928, 1930) speculated that their original definitive hosts (he considered them to have been Cretaceous sauropods) may have been lost from their life cycle,
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possibly due to their extinction, and that the amphilinideans survived by maturing in the last intermediate host as coelomic parasites (see Xylander, 2001, for aspects of the evolution of early cestodes). In a recent molecular study on the phylogeny of basal cestodes, Olson et al. (2008, p. 899) claimed that ‘‘the Gyrocotylidea and Amphilinidea are each monophyletic and form either a single lineage that is the sister group of the Eucestoda (28S results) or two separate lineages (18S results) in which the Amphilinidea is sister group to the Eucestoda’’. As reported by Olson & Caira (1999), amphilinidean rRNA sequences are highly divergent from those of eucestodes. The structure of the female gonad is quite heterogeneous within the Platyhelminthes (Beklemishev, 1952; Gremigni & Falleni, 1998), and the ovary has undergone significant evolutionary modifications (Gremigni, 1997; Gremigni & Falleni, 1998). A number of both free-living and parasitic platyhelminths have been investigated by means of electron microscopy with regard to their ovaries (Gremigni & Falleni, 1998; Poddubnaya et al., 2005). Ultrastructural investigations of the ovary of species of Amphilina Wagener, 1858 are of interest in relation to the discovery of new characters that might prove useful in clarifying the uncertain phylogenetic relationships of the Amphilinidea with other parasitic flatworms, especially with the Gyrocotylidea and Eucestoda. The ovary of species of Amphilina has not been examined ultrastructurally to date, although there are light-microscopical observations on the morphology of the oogenotop of A. japonica Goto & Ishii, 1936 (=A. bipunctata Riser, 1948) by Dubinina (1982) and Coil (1987). The present work has three main objectives: (1) to improve our understanding of the cellular organisation of the ovary of Amphilina japonica; (2) to describe heterologous junctions between the oocytes and accessory cells during the course of oogenesis; and (3) to elucidate any ovarian characters of Amphilina which might constitute autapomorphies for phylogenetic analyses.
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of the American sturgeon Acipenser transmontanus Richardson caught in the Columbia River close to Asteria, Oregon, USA. Pieces (approx. 3 mm3) of live mature worms containing the ovary were fixed in 3% glutaraldehyde in 0.1M Na-cacodylate buffer with 0.7M sucrose for 45 days at ?4°C, rinsed three times for 15 min periods in the same buffer and postfixed in 1% OsO4, dehydrated through an ethanol series and embedded in Araldite. Ultrathin sections (60–80 nm in thickness) were stained with uranyl acetate and lead citrate, and examined using a JEOL 1011 transmission electron microscope operating at 80 kV.
Results The ovary of Amphilina japonica is multilobate, consisting of up to 10 lobes (irregular digitiform processes) originating from the central ovarian core (Fig. 1). In each ovarian lobe there are two different cell types, germ cells at different stages of differentiation and accessory cells (Fig. 2). Individual, peripherally located accessory cells give rise to a cellular ovarian epithelial layer of irregular shape and thickness (Figs. 2C, 3A), which is attached to a thin basal matrix surrounding the ovary (Figs. 2A, 3A). The epithelial layer is broken down by numerous invaginations of the underlying basal matrix (Fig. 3A). Apically, the surface of the accessory cells is enlarged by many long, branched processes extending between the oocytes (Figs. 2A, 3A). Isolated accessory cells can also be observed between the oocytes (Fig. 2D).
Materials and methods Specimens of Amphilina japonica were obtained from the body cavity of naturally infected specimens
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Fig. 1 Diagrammatic representation of the shape of the ovary of Amphilina japonica. Abbreviations: cc, central core of the ovary; ol, ovarian lobe
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Fig. 2 Accessory cells within the ovary of Amphilina japonica: A. Outer portion of the ovarian lobe showing germ cells surrounded by processes of the accessory cells; B. Two oocytes between the processes of the accessory cells; C. Peripheral accessory cell located on a thin basal matrix; note numerous vesicles in the cytoplasm and membranous concentrations in the intercellular space; D. Accessory cell within the ovarian lumen. Abbreviations: ac, accessory cell; ap, accessory cell processes; bm, basal matrix; mc, membranous concentrations; n, nucleus; nc, nucleolus; oc, oocyte; v, vesicles. Scale-bars: A,D, 10 lm; B,C, 5 lm
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Syst Parasitol (2010) 77:163–174 b Fig. 3 Ultrastructure of the accessory cells of Amphilina
japonica: A. Outer portion of the ovary enveloped by a thin basal matrix; note deep invagination of the basal matrix into a groove formed by the basal membrane of the accessory cell, cytoplasm of the accessory cell containing vesicles and a fusion of the vesicles leading to vacuoles; B. Multiple layers of accessory cell cytoplasm; note the gap junction between neighbouring cytoplasmic extensions; C. Formation of the dense bodies within the cytoplasm of the accessory cell; D. Zonulae adherentes between the oocyte and the process of the accessory cell; note a confluence of vesicles within the intercellular space. Abbreviations: ap, accessory cell processes; bg, basal groove; bm, basal matrix; cv, vesicle confluence; db, dense bodies; gc, Golgi complex; ger, granular endoplasmic reticulum; gj, gap junction; m, mitochondrion, mc, membranous concentrations; mcl, multiple cytoplasmic layers; n, nucleus; oc, oocyte; pe, pseudopodium-like extension of the oocyte; v, vesicles; za, zonula adherentes. Scale-bars: A,C, 1 lm; B,D, 0.5 lm
Ultrastructural characters of the accessory cells The accessory cells vary in volume and dimensions. The nucleus of every cell is large and irregularly shaped (Fig. 2C,D) and contains an homogenous matrix, small clumps of chromatin material and a variable number (1–3) of nucleoli. A layer of electron-dense perinuclear cytoplasm contains large numbers of free ribosomes (Fig. 2). Numerous cytoplasmic processes extend from each accessory cell (Fig. 2D). These cells exhibit different types of inclusions (Figs. 2C, 3). Firstly, a huge number of translucent vesicles, the fusion of which eventually leads to an accumulation of membrane-bound spherical or irregularly-shaped vacuoles that contain a fine filamentous material or membranous residues (Figs. 2C, 3A,C,D). The limited membrane of the vesicles is often found in close contact with the cell plasma membrane and their content may be discharged into the intercellular space (Figs. 2C, 3A,D); the ovarian space between the cells is filled with vesicle material (Figs. 2C, 3D, 4A, 6). Secondly, dense bodies of various shape and size represent another type of inclusion (Fig. 3C,D). The cell cytoplasm also contains mitochondria, granular endoplasmic reticulum and Golgi complexes which are involved in the formation of the aforementioned inclusions (Fig. 3A,D). Some parts of the cytoplasm of the accessory cells are divided into narrow cytoplasmic extensions which are arranged in parallel and separated by narrow intercellular spaces (Figs. 3B, 4C,E), forming a
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multilayered tunica around the oocytes (Fig. 6B). Adjacent extensions of two neighbouring accessory cells are connected by long gap junctions of about 70–100 nm in size; these are characterised by narrow, junctional intercellular spaces and the absence of adjacent dense material within the cytoplasm of these cells (Figs. 3B, 4C). Interactions between growing oocytes and accessory cells The processes of the accessory cells are localised at some distance from the growing oocytes (Figs. 2A,B, 4A,B, 6B). These oocytes form pseudopodium-like protrusions of different shapes and thickness in the direction of the accessory cell processes (Figs. 3D, 4A,B, 6B). The accessory cell cytoplasm possesses small elevations adjacent to the oocytes (Figs. 4B, 6B). Contact sites form in areas where the oolemma and the accessory cell membrane are adjacent (Figs. 3D, 4, 6B). There are numerous heterologous junctions between every oocyte and accessory cell cytoplasm; the contact sites are variable in length and occur in two forms that can be identified as desmosome-like junctions (Fig. 4E,F) and zonulae adherentes (Figs. 3D, 4B,D,G), both of which are characterised by the presence of electron-dense material on the subsurface areas of both connected cells. The desmosome-like junctions have more dense material beneath the junction and contain a greater amount of dense material in the junctional space (Fig. 4E,F). The intercellular space at both contact sites measures from 20 nm (for desmosome-like junctions) to 50 nm (for zonulae adherentes); here vacuoles are frequently observed in the accessory cell cytoplasm (Fig. 4D,F). Relationship of the maturing oocytes with accessory cells Maturing oocytes can be observed close to the central core in every ovarian lobe, and also within the lumen of the central core. With increasing oocyte volume, accessory cells and oocytes detach from the special junctions, and the accessory cells gradually retract their processes from the oocytes and lose their intimate association with the oocyte surface (Fig. 5A–C). Once the accessory cells have withdrawn, the oocyte membrane does not exhibit
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b Fig. 4 Relationship between the growing oocytes and the
between cells of different types), separating the developing oocytes and the accessory cells, in the form of desmosome-like junctions and zonulae adherentes. The accessory cells of this species, which completely encircle the oocytes during early oogenesis with their multiple narrow projections, interdigitate with oocyte pseudopodium -like extensions and result in the formation of contact sites with every oocyte. As the oocyte volume increases, the accessory cells gradually lose their association with its surface. This is different to the situation in eucestodes (Davies & Roberts, 1983; Korneva & Davydov, 2001; Poddubnaya et al., 2005, 2007) and the gyrocotylidean Gyrocotyle urna (Grube & Wagener, 1852) (Poddubnaya et al., 2010), where the so-called ‘interstitial cells’ of the ovary (or of isolated ovarian follicles in the case of G. urna) never form such junctions with the oocytes.
accessory cells of Amphilina japonica: A. Growing oocyte surrounded by processes of the accessory cells; note the oocyte with pseudopodium-like extensions and contact sites with ‘oocyte-accessory cells’ and that the intercellular space is becoming filled with membranous concentrations; B. The process of an accessory cell forming zonula adherentes with an oocyte; note the intercellular membranous concentrations; C. Accessory cell-accessory cell gap junction; D. Two zonulae adherentes between an oocyte and an accessory cell process; note pinocytic vesicles in close association with each junction; E,F. Desmosome-like junctions with a lot of dense material under the junction and a narrow junctional space; G. Zonula adherentes; note less cytoplasmic material under the junction and a wider junctional space. Abbreviations: ap, accessory cell processes; cs, contact site; dm, dense material; gj, gap junction; js, junctional space; oc, oocyte; pe, pseudopodium-like extension; v, vesicles; za, zonula adherentes. Scale-bars: A, 5 lm; B, 1 lm; C,D,F, 0.5 lm; E,G, 0.2 lm
pseudopodia-like extensions, and the intercellular space contains no trace of vacuolar material (Fig. 5B). In these regions of the ovary, the cell bodies of the accessory cells are tightly packed at the periphery (Fig. 5A,C). No gap was observed between adjacent accessory cells (Fig. 5C). The accessory cells undergo a number of characteristic ultrastructural changes, including a decrease in the secretion of the vesicles (Fig. 5A,C).
(2)
In A. japonica both peripherally and centrally located accessory cells produce narrow processes which extend around the oocytes; between adjacent processes of accessory cells gap junctions can be seen. In eucestodes and Gyrocotyle, the accessory cells or ‘interstitial cells’ have a syncytial structure with several nuclei and cytoplasm surrounding the germ cells (Korneva & Davydov, 2001; Poddubnaya et al., 2005, 2007, 2010).
(3)
The accessory cells of A. japonica are characterised by their great number of micropinocytotic vesicles and vacuoles, the contents of which fill the intercellular space between the oocytes and the accessory cells via exocytosis. Morphological structures, such as micropinocytic vesicles, can be indicative of a functional relationship between accessory cells and oocytes, providing each oocyte with a microenvironment within the ovarian lumen (Wourms, 1987; Pipe, 1987). Whereas, in other cestode groups, the syncytial cytoplasm of the accessory cells (‘interstitial cytoplasm’) lacks typical pinocytotic vesicles and small, narrow areas of intercellular space are commonly devoid of such discharged content (Poddubnaya et al., 2005, 2007, 2010).
Discussion The arrangements and relationship of different cell components within ovary of the Cestoda The present study is the first to describe the ultrastructural features of the ovary of a member of the Amphilinidea and shows that the ovarian structure of Amphilina japonica is different from those of both the Gyrocotylidea and Eucestoda (cf. Davies & Roberts, 1983; Korneva & Davydov, 2001; Poddubnaya et al., 2005, 2007, 2010) with regard to: (1) interaction between the oocytes and the accessory cells; (2) interaction between the accessory cells; (3) its ability to discharge material via the accessory cells into the intercellular spaces between the oocytes and the accessory cells; and (4) the structure of the ovarian epithelial sheath. (1)
The most important trait of the ovarian structure of A. japonica is the presence of numerous heterologous junctions (i.e. junctions formed
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Fig. 5 Relationship of accessory cells and maturing oocytes of Amphilina japonica: A. Outer portion of the ovarian central core showing a tight packing of accessory cells along the periphery of the ovary; note the absence of long, branched processes of the accessory cells and numerous inclusions within cell cytoplasm; B. Maturing oocytes with fewer contact sites with the accessory cells; C. Peripheral accessory cell showing the absence of gap junctions with a neighbouring accessory cell; note that there are no membranous concentrations within the intercellular space. Abbreviations: ac, accessory cell; ap, accessory cell processes; bm, basal matrix; is, intercellular space; mo, maturing oocytes. Scale-bars: A, 5 lm; B, 10 lm; C, 2 lm
(4)
The ovary in all groups of the Cestoda is enveloped by a basal matrix; directly beneath this, the plasma membrane of the interstitial syncytial cytoplasm is situated in both the Eucestoda and the Gyrocotylidea (see Poddubnaya et al., 2005, 2007, 2010). Nevertheless, individual, peripherally located accessory cells of A. japonica give rise to a cellular epithelial layer of the ovary, which is broken down by numerous invaginations of the basal membrane and underlying basal matrix. This layer is characterised by its irregular shape and thickness along its length, and by possessing the same set of organelles and inclusions as the accessory cell cytoplasm.
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With the aim of elucidating the nature of ovarian characteristics of specimens of Amphilina in relation to those of other Platyhelminthes, the following comparative analysis was undertaken. Characteristics of the ovarian cell types of free-living neoophoran platyhelminths The germaria of neoophoran free-living platyhelminths are enveloped by an extracellular lamina and/or epithelial sheath (Ehlers, 1985; Gremigni, 1988, 1997; Gremigni & Falleni, 1998) and contain oocytes and accessory cells. The accessory cells are limited spatially to the periphery, where they form an enveloping sheath, as in some Proseriata and some
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Rhabdocoela, or are located at both the periphery of the gonad as well as between the oocytes, extending their cytoplasmic projections into the spaces between the oocytes (see Soppott-Ehlers, 1986; Falleni & Gremigni, 1992; Lucchesi et al., 1995; Falleni et al., 1998). In temnocephalids, thin overlapping cytoplasmic projections of the accessory cells surround the oogonia and early oocytes in the germinative area, but are absent between growing and mature oocytes in the growth area (Falleni et al., 1998), as they are between growing and mature oocytes in the Rhabdocoela (see Falleni & Lucchesi, 1992; Falleni et al., 2002). Neither intercellular bridges nor specialised junctional complexes have been observed between the oocytes and accessory cells or between the different adjacent accessory cells in the Rhabdocoela (see Lucchesi et al., 1995) or Proseriata (see SoppotEhlers, 1986; Falleni & Gremigni, 1992; Falleni et al., 1998). The accessory cells of free-living neoophoran platyhelminths appear to be rich in cell organelles and inclusions and are considered to take part in the production of the basal matrix (Falleni et al., 1998), whereas, in other groups, the accessory cells have only a central body, with a nucleus and a peripheral cytoplasm which is almost devoid of organelles and apparently inactive (Gremigni & Falleni, 1998). Characteristics of the relationship between the accessory cells and oocytes of the Digenea and Monogenea In the case of the Digenea, no data are available in terms of the detailed relationship between the germ and accessory cells (the so-called ‘supporting cells’ or ‘nurse cells’) in the ovary. Most authors have indicated that primary oocytes are embedded in ‘supporting tissue’ at the periphery of the ovary and that maturing oocytes appear from the network of the ‘supporting tissue’ (Gresson, 1964; Koulish, 1965; Erasmus, 1973; Grant et al., 1977; Cifrian et al., 1993). For some digeneans, the presence of the several cells of ‘supporting tissue’ has been reported (Orido, 1987; Podvyaznaya, 2003). Bjo¨rkman & Thorsell (1964) stated that the internal wall of the ovary of Fasciola hepatica L. is lined by a cellular layer of irregularly shaped ‘nurse cells’. Information on the ovarian accessory cells of the Monogenea and their relationship with oocytes in the
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ovary is not available, studies being limited to observations of oocyte development (Halton et al., 1976; Justine & Mattei, 1986). The role of the ovarian accessory cells in oogenesis Accessory cells occur almost universally in invertebrate gonads, where they have a nutritive function, since they are intimately associated with oocytes, possess numerous proteosynthetic organelles and undergo extensive endocytotic activity. They have often been suspected as playing some role in oocyte nutrition (Eckelbarger et al., 1984; Wourms, 1987; Eckelbarger, 1994). It is assumed that the accessory cells of the female gonads of the Cestoda (i.e. an interstitial system in the form of a syncytium with several nuclei) are involved in the transport of materials and supply of nutrients for intercellular exchange (Conn, 1993; S´widerski & Xylander, 2000). Accessory cells of Amphilina japonica provide each oocyte, at early stages of oogenesis, with a compartmentalised microenvironment within the ovarian lumen and undergo extensive endocytotic activity along their surface. They also form desmosome-like junctions and zonulae adherentes in the area of the attachment between pseudopodium-like extensions of the plasma membrane of both the oocyte and the accessory cell themsleves. Using histochemistry, Coil (1987) showed that the accessory cells in the ovary of A. japonica are PAS positive. So-called heterologous gap junctions have also been found in the ovaries of other taxa, e.g. in polychaetes (Eckelbarger, 2005), molluscs (Bottke, 1974; Eckelbarger & Davis, 1996); echinoderms (Beijnink et al., 1984), insects (Bilinski et al. 1985) and mammals (Anderson & Albertini, 1976). Evidence exists which suggests that heterologous gap junctions are involved in the transport of nutrient molecules between different cells of both the invertebrate and the vertebrate ovary (Anderson & Albertini, 1976; Gilula et al., 1978; Bilinski et al. 1985; Pipe, 1987). The presence of high micropinocytotic activity during oogenesis in the accessory cell cytoplasm with the release of material into the intercellular space, as in A. japonica, has been previously documented for
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an echinoderm, Asteria rubens L. (see Beijnink et al., 1984). Phylogenetic remarks The cestode branch of the phylogenetic tree of the Platyhelminthes, comprising the Amphilinidea, Gyrocotylidea and Eucestoda, is traditionally considered to be monophyletic (e.g. Ehlers, 1985; Lockyer et al., 2003). The present work establishes the existence of differences in the nature of the interconnection between the germ and accessory cells in the ovary of the Amphilinidea with that of the Gyrocotylidea and Eucestoda (Fig. 6). The different arrangements of the interconnection of the cell components in the Amphilinidea (desmosome-like junctions and zonulae adherents between the germ and accessory cells and gap junctions between the accessory cells) as opposed to those of the Gyrocotylidea and Eucestoda (the absence of specialised cell contacts and the syncytial nature of the accessory ‘interstitial’ cells) may be used as an argument to suggest the presence of unrelated groups within the Cestoda. The specialised cell junctions and the high micropinocytotic activity of the accessory cells within the ovary of Amphilina japonica resemble similar findings reported for the ovary of nonplatyhelminth invertebrates rather than those reported for other neodermatans. This can be interpreted as agreeing with the statement of Littlewood (2008, p. 334) that ‘‘flatworms (and especially parasitic flatworms) are best viewed as an ancient, but relatively derived and specialized group of lophotrochozoans, with their lack of many key characters indicating losses rather than indicating ‘primitive’ bilaterian features’’. Finally, we conclude that the nature of the relationship between the accessory and germ cells within the female gonads of parasitic platyhelminths will prove to be an important feature for the study of the evolutionary morphology of this organ. However, our knowledge of the ovarian structure of platyhelminths is still limited to a very small number of studied species from other parasitic groups, such as the Aspidogastrea, Digenea and Monogenea, preventing conclusions regarding the possible relationships between the Amphilinidea and other parasitic platyhelminth groups using ovarian ultrastructural markers.
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Fig. 6 Diagrammatic representation of the relationhip of the ‘oocyte-accessory’ cells of the Eucestoda (A) and Amphilinidea (B). Abbreviations: ap, accessory cell processes; cs, contact site between the oocyte and the accessory cell processes; gj, gap junction between two accessory cell processes; mc, membranous concentrations; oc, oocyte; sc, syncytial cytoplasm Acknowledgements The authors extend their appreciation to Dr John S. Laurie (Oregon, USA), who collected and kindly handed the material over to one of us (WERX). The valuable, constructive comments of anonymous referees are gratefully acknowledged. The present study was supported by the Russian Foundation for Fundamental Research Project No. 09-0400342a to LGP and by a grant from the German Science Council (Deutsche Forschungsgemeinschaft) to WERX (XY 12/5-1). The authors would also like to thank the staff of the Centre of Electron Microscopy, Institute of Biology of Inland Waters, Borok, Russia for the technical assistance.
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