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121 Abstract The ciliates in this class are thought to represent the nature of the ancestral ciliate lineage. Their non-dividing macronuclei make them “karyo- logical relicts”. They are a strongly supported clade, characterized by postciliodesmata arising from the somatic kinetids, their non-dividing macronuclei, and by robust phylogenetic support based on small subunit rRNA gene sequences. The class is divided into three orders, based primarily on oral features. These ciliate are conspicuous inhabitants of benthic marine habitats. Their elongated worm-like bodies can be seen crawling between sand grains and detrital particles. Thus, they are quite contractile and fl exible, and also capable of regeneration. The extrusomes of this class are also unique with cnidocysts and orthonematocysts being found nowhere else in the phylum. Oral structures are quite variable, ranging from simple circumoral dikinetids to somewhat complex adoral ciliature. Stomatogenesis can be either parakinetal or buccokinetal, although much remains to be done on this aspect of their biology. Their non-dividing macronuclei, which arise at each cell division from division of a micronucleus, are often numerous and typically clustered around a micronucleus. Two unusual features of taxa in the group are the harvesting of epibiontic bacteria by Kentrophoros and the use of mineral crystals in the Müller’s vesicle to sense gravity by Loxodes . Keywords Postciliodesma, paradiploid, interstitial The ciliates assigned to this class are considered by some to represent the nature of the “dawn” or eociliates that first diverged from the alveolate lineage. They have been labeled “ karyological relicts ”, a term introduced by Grell (1962) and publicized by Raikov (1969, 1982, 1985), because they exhibit a simple form of nuclear dualism : the macronucleus is paradiploid but non-dividing. They have also been labeled “ cortical relicts ” because the cortex in some forms is thought to repre- sent the ancestral condition: Kentrophoros does not have differentiated oral ciliature, but it does have somatic dikinetids , which are presumed to be the ancestral condition for the phylum (Lynn & Small, 1981; Small, 1984). There are over 130 species of these primarily interstitial ciliates, commonly found in the sands and sediments of marine littoral environments (Foissner, 1998b). Intertidal sands are the habitat for “relict” forms of various groups of small invertebrates, leading one to believe that the psammophilic karyorelicteans are also of ancient vintage (Corliss, 1974b, 1975b; Raikov, 1969). Finlay and Fenchel (1986) have suggested, based on their research on Loxodes , which is the only freshwater representative of the class, that these ciliates might also be “biochemical relicts” because of the odd mitochondrial potential of nitrate respiration under low oxygen conditions, which are common in interstitial environments. The karyorelicteans are united by two major features: the presence of a non-dividing paradiploid macronucleus or macronuclei; and by postciliodesmata in which the microtubules are arranged as 2 + ribbon + 1 in a repeating fashion (see Somatic Structures ). The class is supported robustly by small subunit rRNA gene sequences (Hammerschmidt et al., 1996; Hirt et al., 1995). The actin of Loxodes is quite divergent from other ciliates (Kim, Yura, Go, Chapter 5 Subphylum 1. POSTCILIODESMATOPHORA: Class 1. KARYORELICTEA – The “Dawn” or Eociliates 122 5. Subphylum 1. POSTCILIODESMATOPHORA: Class 1. KARYORELICTEA – The “Dawn” & Harumoto, 2004). It is a matter of opinion whether this supports the ancestral nature of karyorelicteans or demonstrates again the unreliability of actin as a phylogenetic marker for ciliate evolution (see Philippe & Adoutte, 1998). They form a diverse assemblage when one considers their oral structures. Some genera are ventrostomous (e.g., Geleia , Loxodes ); some genera are pros- tomous (e.g., Trachelocerca , Trachelolophos ); and some genera have apparently no differentiated oral ciliature (e.g., Kentrophoros ). Bardele and Klindworth (1996) have observed that this parallels the evolution of oral structures in other groups. They argued that Kentrophoros may, in fact, have secondarily lost its oral apparatus when it acquired the obligatory symbiosis with thiotrophic or sul- fur bacteria , an interpretation consistent with the observations of Foissner (1995a). The distribution of these obligatorily psammobiotic species is global, though they are “endemic” with respect to their biotope. Means of dispersal remain unknown: Corliss and Hartwig (1977) supposed that continental drift may have been partially responsible. 5.1 Taxonomic Structure We recognize three orders in this class: Order Protostomatida ; Order Loxodida ; and Order Protoheterotrichida . Alternative classifications have been proposed: Foissner (1998b) has argued that the bristle kinety , which frames the glabrous stripe or non-ciliated somatic cortex of protostomatids is homologous to that of loxodids , and so he sup- ports uniting these in the Subclass Trachelocercia de Puytorac, Grain, and Mignot, 1987. We remain sceptical of this homology until ultrastructural investigation has demonstrated clear similarities in the kinetid structures or more extensive gene sequence data resolves the phylogeny of this class. The Order Protostomatida includes the prostomous Family Trachelocercidae and the “astomous” Family Kentrophoridae (Fig. 5.1). Oral struc- tures are simple and ingestion may be either at the anterior end or along the glabrous stripe (see Oral Structures ). The Order Loxodida includes the ventrostomous Families Loxodidae and Cryptopharyngidae . These ciliates typically swim on the right surface of their flattened bodies. The oral cavity has a simplified ciliature of dikinetids (Fig. 5.1). The Order Protoheterotrichida , which includes the ventrostomous Family Geleiidae , are holotrichously ciliated and contractile, resembling their namesakes the heterotrichs (see Chapter 6 ). Their non-dividing macronuclei relate them to the other karyorelicteans even though their oral struc- tures are more complex with simple adoral polyki- netids and unusual paroral polykinetids on the right side of the oral region (Fig. 5.1). A number of recent works have provided details of the morphology of these taxa: Trachelocercidae (Foissner, 1996c, 1997g; Foissner & Dragesco, 1996a, 1996b), Kentrophoridae (Foissner, 1995a, 1998b), Loxodidae (Foissner, 1995/1996, 1996b, 1998b), and Geleiidae (Dragesco, 1999), but refer to Chapter 17 for detailed descriptions. 5.2 Life History and Ecology These typically elongate and highly contractile ciliates are conspicuous consituents of interstitial habitats, especially sands and sediments of the marine littoral or brackish estuaries. Karyorelicteans have been recorded from interstitial habitats, often sandy ones in the marine sublittoral, in Africa (Dragesco, 1965), western and eastern Europe (Agamaliev, 1971; Azovsky & Mazei, 2003; Dragesco, 1963, 2002; Fernández-Leborans & Fernández-Fernández, 1999; Kovaleva & Golemansky, 1979; Mazei & Burkovsky, 2003), North America (Borror, 1963), and the Arabian Gulf (Al-Rasheid & Foissner, 1999). The only recorded exception is Loxodes , which is found in freshwater sediments (Finlay, 1982; Finlay & Berninger, 1984). Most species are classified as microaerophilic , restricted to sediments because these regions contain reduced oxygen concentrations, often becoming anoxic within a few centimeters of the sediment-water interface. However, Loxodes can move into the water column if the interstitial waters of the sediments become anoxic (Goulder, 1980). Finlay, Fenchel, and Gardener (1986) suggested that cyto- chrome oxidase is the oxygen receptor forLoxodes whose response to oxygen concentrations is modi- fied by light (Fenchel & Finlay, 1986b). Karyorelicteans are predaceous macrophages, using their filiform or vermiform bodies to crawl between the grains in the sediments in search of food. They have been recorded to ingest bacteria , Fig. 5.1. Representative genera of the Class KARYORELICTEA. The protostomatid Kentrophoros whose body in cross-section is ciliated on one surface (the right?) and harbors a “kitchen garden” of epibiotic bacteria on its glabrous zone (after Foissner, 1995a). The loxodid Loxodes whose ventral oral region has a paroral along its right border and an intrabuccal kinety extending posteriorly into the tube-like oral cavity. Note the bristle kinety along the ventral left surface of the cell (arrow) (after Bardele & Klindworth, 1996). The protostomatid Tracheloraphis showing its prostomial oral region and the glabrous zone bordered by the bristle kinety (After Foissner & Dragesco, 1996b). The protoheterotrichid Geleia, which is holotrichous and shows a complex oral region of dikinetid files and simple polykinetids. (after Dragesco, 1999.) 124 5. Subphylum 1. POSTCILIODESMATOPHORA: Class 1. KARYORELICTEA – The “Dawn” diatoms (e.g., Coscinodiscus , Phaeodactylum ), both autotrophic and heterotrophic flagellates (e.g., Euglena , dinoflagellates ), other ciliates (e.g., Euplotes , Strombidium , and smaller karyorelict- eans ), and even micrometazoans, such as rotifers and copepods (Foissner, 1998b). The many species sharing an interstitial habitat probably coexist in part by partitioning food resources: different-sized Loxodes species coexist in the same lake as the larger species consumes the larger food particles (Finlay & Berninger, 1984). Conjugation is rarely observed (see Sexuality and Life Cycle below). Since it does occur in some taxa, we presume it to be an ancestral feature of the group. Cysts are not known. Thus, explaining the presumed global distribution of some of these ciliates is problematic as it is with any group that does not form resistant phases in the life cycle. 5.3 Somatic Structures The karyorelictean cell body is typically long, some- times >5,000 µm, and frequently flattened to about 5–10 µm in thickness. In several genera, the cell surface on which the organism “crawls” is more densely ciliated (e.g., Loxodes , Kentrophoros ). The body is often pigmented, brown or yellowish, possibly due to pigmentocysts or extrusomes . The pigmento- cysts apparently have a defensive function, at least in Loxodes (Buonanno, Saltalamacchia, & Miyake, 2005). The cell surface may have a conspicuous glycocalyx , but is not underlain by a regular layer of cortical alveoli . When present, the alveoli are irregu- lar and small. Parasomal sacs have not been observed. The somatic dikinetids of these ciliates are com- posed of two kinetosomes joined by desmoses (Fig. 5.2), and oriented at 20–40° to the kinety axis. Both kinetosomes may be ciliated or only the anterior one. The postciliary microtubular ribbon of the posterior kinetosome is divergent, extending up to the cortex and posteriorly to overlap the ribbons of 10 or more anterior kinetids, and so forming the postciliodesma . The number of overlapping ribbons will vary depending upon the contractile state of the ciliate, as these microtubules are assumed to play the same role in cell elongation as those of Stentor (Huang & Mazia, 1975; Huang & Pitelka, 1973). It is not clear how the organization of the postciliary ribbons changes from their origin as a ribbon to the modified structure at the cell surface. There are two microtubules closest to the kinetosome followed by a ribbon of up to 20 microtubules perpendicular to the cell surface, and then a single microtubule. This 2 + ribbon + 1 pattern can be repeated for each over- lapping set (Fig. 5.2) (Klindworth & Bardele, 1996; Raikov, 1994b; Raikov & Kovaleva, 1995; Raikov, Gerassimova-Matvejeva, & de Puytorac, 1976). The postciliary microtubules are accompanied by dense material on either side near their base. The posterior kinetosome may also have a tangential transverse ribbon associated with triplets 3–5 (Fig. 5.2). The kinetodesmal fibril originates near triplets 5, 6, and 7 and is variable in form. It is striated and elongate in Remanella (Raikov, 1994b), striated and shovel- shaped in Loxodes (Bardele & Klindworth, 1996), and short and hooked with only a faint periodicity in Tracheloraphis (Raikov & Kovaleva, 1995) and Geleia (de Puytorac, Raikov, & Nouzarède, 1973a). The kinetodesmal fibril structure in the latter two genera is very reminiscent of Stentor ’s as described by Huang and Pitelka. In Loxodes, the shovel-shaped kinetodesmal fibril becomes branched, one branch of which extends to contact the postciliary ribbon of the next anterior kinetid. The anterior kinetosome has a tangential transverse ribbon associated with triplets 3–5. There may be ribbons of subkinetal microtubules that originate from the bases of the somatic kinetosomes and extend posteriorly beneath the kinety (Raikov & Kovaleva, 1995) or towards the left (Klindworth & Bardele, 1996). There are two kineties on the left side of Loxodes that have been interpreted to be one continuous kinety. Klindworth and Bardele (1996) have disproved this by showing that the kinetodesmal fibrils are oriented in the manner expected for two kineties: these kineties just hap- pen to abut near the anterior end and so appear to be continuous at the level of the light microscope. Until it is demonstrated otherwise by electron microscopy, we assume that the bristle kineties bordering the non-ciliated stripe in Kentrophoros are bipolar, contrary to the interpretations of Foissner (1995a, 1998b). Myonemes are arranged longitudinally and parallel to the somatic kineties in most karyorelicteans : to the right of the kinety in Tracheloraphis , to the left of the kinety in Remanella , and on both sides in Geleia . Since these ciliates are often not evenly ciliated around the body, contraction may cause Fig. 5.2. Ultrastructure of the cortex of the Class KARYORELICTEA. A Somatic dikinetids. (a) The protostomatid Tracheloraphis (after Raikov & Kovaleva, 1995). (b) The loxodid Loxodes. (after Klindworth & Bardele, 1996.) (c) The protoheterotrichid Geleia (after de Puytorac, Raikov, & Nouzarède, 1973a). B Somatic cortex of the protostome Tracheloraphis with postciliodesmata composed of overlapping ribbons in the 2 + ribbon + 1 arrangement. (Redrawn after Raikov et al., 1976.) 5.3 Somatic Structures 125 126 5. Subphylum 1. POSTCILIODESMATOPHORA: Class 1. KARYORELICTEA – The “Dawn” the cell to become banana-shaped or roll up. In some species, transverse myonemes occur, possibly ensuring an even longitudinal contraction. The contractile vacuole system is not well- developed, except in freshwater Loxodes species, and is often absent. Extrusomes in the karyorelicteans are very diverse. Rhabdocysts have been recorded in Tracheloraphis and Kentrophoros (Raikov, 1974b), ampullocysts in Kentrophoros (Raikov), and cnidocysts and orthonematocysts in Remanella (Foissner, 1996a; Raikov, 1978, 1992, 1993). The aberrant character of karyorelictean extrusomes in relation to those of other ciliates and the apparent similarities of the cnidocysts of some karyorelicteans to the extrusomes of dinoflagellates, another alveolate group, have been used as another feature to indicate the ancestral nature of the karyorelicteans (Raikov, 1992). 5.4 Oral Structures The taxa in this class are distinguished from each other primarily on the basis of oral structures, which, as we learn more about the detailed cyto- anatomy of this group, are quite diverse. Oral kinetosomes bear cilia that are usually slightly longer than the somatic cilia, and may have simple nematodesmata,which reinforce the cytopharyn- geal walls. Protostomatids have a dome-like oral region surrounded by circumoral dikinetids , which may form an uninterrupted ring around the cytostome or which may be interrupted by brosse kineto- fragments (Fig. 5.1). Until electron microscopy demonstrates otherwise, we assume that the glabrous stripe is delimited by two kineties, one on its left and one on its right (Fig. 5.1). Foissner and Dragesco (1996b) interpreted these as the bris- tle kinety , which they assumed to be continuous around the glabrous stripe . Protostomatids may ingest food through the anterior end (Al-Rasheid & Foissner, 1999) or along the glabrous stripe (Lenk, Small, & Gunderson, 1984; Lenk, Hollander, & Small, 1989). We place Kentrophoros in this group because it has two kineties bordering the glabrous stripe and it ingests the symbiotic bacteria from its glabrous stripe (Raikov, 1974b) in a fashion similar to that reported for ingestion by Tracheloraphis (Lenk et al., 1984, 1989). Foissner and Dragesco (1996b) argued that protostomatids are derived with respect to their oral region, which they regarded as having become apicalized from that of a ventrostomous ancestor, based on the arguments of Eisler (1992). Loxodids have a slit-like ventral oral region that is bordered by files of dikinetids (Fig. 5.1). There is a paroral of dikinetids bordering the right side of the oral region. Slightly inside of this is a file of dikinetids that extends into a posterior extension of the oral cav- ity. This file has been called an intravestibular kinety (Bardele & Klindworth, 1996) or an intrabuccal kinety (Foissner, 1995/1996). Since these oral struc- tures are derived from buccal structures (see below), this oral cavity is not a vestibulum (see Glossary ); therefore, we prefer the term intrabuccal kinety . The cytostome may be placed between the paroral and this kinety (Klindworth & Bardele, 1996). The left side of the oral region is bordered by the left pseu- dobuccal kinety , which may have been derived from somatic kinety 1 (Foissner, 1995/1996), since it is an inverted kinety based on the inverted orientation of its fibrillar associates (Bardele & Klindworth, 1996). Just interior to this, is a file of several anterior left oral dikinetids. A ventral kinetofragment of several dikinetids extends posterior from the ventral slit; it behaves like a scutica during stomatogenesis (Bardele & Klindworth, 1996). Protoheterotrichids have been recently described in detail by Dragesco (1999). Their oral region varies from slit-like to almost rounded, and is bordered by more complex oral structures than found in the previous two orders (Fig. 5.1). The cytostome is bounded on its right side by a paroral of dikinetids to the right of which are right paroral polykinetids . The structure of these polykinetids appears variable at the light microscopic level: files of closely spaced monokinetids lie perpendicular to the paroral (e.g., Geleia , Avelia , Parduczia ); and files of dikinetids lie parallel to the paroral (e.g., Gellertia ). Adoral polykinetids are arrayed perpen- dicular to the longitudinal axis of the cell to the left of cytostome in all genera but Parduczia , which has oralized somatic kineties on this side of the oral region. When present, the adoral polykinetids appear to be composed of files of dikinetids (e.g., Geleia , Gellertia ) or monokinetids ( e.g ., Avelia ). Confirmation of Dragesco’s interpretation from these protargol-stained specimens must await elec- tron microscopic examination. 5.5 Division and Morphogenesis Karyorelicteans divide while swimming freely. They also have considerable powers of regenera- tion, like the heterotrichs . Thus, they may increase in numbers by fragment regeneration when they become severed by sediment action in their natural habitat. Foissner and Al-Rasheid (1999) have classified stomatogenesis in the protostomatid Sultanophrys as parakinetal . The proter oral apparatus does not reorganize. The oral primordium of the opisthe is apparently derived from proliferation of kine- tosomes in the somatic kinety to the right of the glabrous stripe (Fig. 5.3). The subequatorial pri- mordium differentiates from an anarchic field of kineto somes into kinetofragments of dikinetids. These kinetofragments assemble as circumoral dikinetids and three small brosse kinetofragments. Bardele and Klindworth (1996) concluded that stomatogenesis in Loxodes is buccokinetal . The parental oral apparatus is only slightly reorgan- ized. Stomatogenesis begins with proliferation of kinetosomes from the ventral kinetofragment, just posterior to the oral region, and this is fol- lowed by proliferation of kinetosomes from the paroral and the left pseudobuccal kinety . The ventral kinetofragment gives rise to the opisthe paroral while the proliferation of the proter left pseudobuccal kinety gives rise to that of the opisthe. The intrabuccal kinety and the anterior left oral dikinetids, whose origin is not yet resolved, appear later in stomatogenesis at the anterior end of the opisthe oral region, as the oral anlagen reach the cell equator. Thus, stomatogenesis among the karyorelictean orders demonstrates different modes: parakinetal in protostomatids and buccokinetal in loxodids . What mode the protoheterotrichs demonstrate awaits the results of further investigations. However, it is clear that there is as much diversity in stomatogenesis in this class as can be found in other classes of ciliates (e.g., Class OLIGOHYMENOPHOREA , Foissner & Al-Rasheid, 1999). Stomatogenesis is therefore not likely to be an indicator of deep phylogenetic relationships. Fig. 5.3. Stomatogenesis of the protostomatid Sultanophrys. (a) The process begins in the mid-region of the body as kinetosomes proliferate, forming an anarchic field to the right of the ventral (?) or right bristle kinety. (b–d) The process continues until a ring of circumoral dikinetids forms accompanied by 3 minute brosse kinetids. (from Foissner & Al-Rasheid, 1999.) 5.5 Division and Morphogenesis 127 128 5. Subphylum 1. POSTCILIODESMATOPHORA: Class 1. KARYORELICTEA – The “Dawn” 5.6 Nuclei, Sexuality and Life Cycle As discussed above, the karyorelicteans have the simplest form of nuclear dimorphism in the phylum: the macronucleus is diploid or paradiploid and non-dividing. It is rich in RNA with a conspicuous nucleolus and may have proteinaceous inclusions (Raikov, 1982). Since it does not divide, the macronucleus(ei) must be replaced at each cell division by differentiation of the products of micro- nuclear division. The micronucleus is presumed to be diploid and is capable of mitosis and meiosis. Both nuclei are small in size, typically globular or ellipsoid. They may be found in a variety of close associations: a single micronucleus and one macro- nucleus (e.g., Loxodes ), a single micronucleus and two associated macronuclei (e.g., some protosto- matids ), or present in clusters or complexes of several micronuclei and several macronuclei with or without a surrounding envelope. It is not clear what factors stimulate conjuga- tion in karyorelicteans . Raikov (1972) reviewed the general features of conjugation in kary- orelicteans, based on observations of Loxodes and Tracheloraphis , and summarized it thus. Preconjugants differ from vegetative cells by the incomplete differentiation of the nuclei, especially the macronuclei. Meiosis is typical but it may lead to the formation of multiple pronuclei and, ultimately after exchange of migratory gametic nuclei, multiple synkarya in Tracheloraphis spe- cies. Thus, genetic identity of the two separating exconjugants is not assured. After separation, the “parental” macronuclei do not degenerate. Thus, the exconjugant is presumed to be a genetic chimaerawith a “parental” phenotype expressed by the old macronuclei and a developing phe- notype expressed by the genome residing in the “new” macronucleus. Replacement of the “paren- tal” macronuclei occurs over several cell divisions following conjugation , and the new phenotype presumably becomes established as the “paren- tal” macronuclei are diluted out by cell division cycles. Since renewal of the macronuclei is not directly connected with conjugation, Raikov sup- poses this to be an ancestral feature of the conjuga- tion process (see also Orias, 1991a, 1991b). 5.7 Other Features Gram-negative bacteria are commonly associated with karyorelicteans . Geleia species may have perhaps 10,000 bacteria as epibionts on their cell surface (Epstein, Bazylinski, & Fowle, 1998). Other Gram- negative bacteria are found in the cytoplasm. Since they are often not bounded by a ciliate vacuolar mem- brane, it is assumed that they are endosymbionts. Their functional relationship to their hosts is unknown. A novel feature restricted to the loxodid karyo- relicteans is the organelle known as Müller’s vesicle . The vesicle, about 7 µm in diameter, encloses the Müller’s body , which itself is bounded by a cell membrane that encloses barium salt-dominated crystals in the freshwater Loxodes and strontium salt- dominated crystals in the marine Remanella (Rieder, Ott, Pfundstein, & Schoch, 1982). Movements of the Müller’s body , in response to gravity and the orientation of the ciliate, may deform ion channels on the cell surface and thereby modulate cell move- ment. Movement in Loxodes is also dependent on external oxygen concentration in the water: Loxodes swim faster upward when the water is anoxic and faster downward when the water is oxygen-saturated (Fenchel & Finlay, 1984, 1986b). Müller’s body is suspended in the vesicle by a stalk that is a supported by postciliary microtu- bules from an adjacent dorsal left somatic dikinetid (Fenchel & Finlay, 1986a). These dikinetids com- prise the loxodid dorsolateral kinety that Foissner (1998b) has presumed to be homologous to a somatic kinety of kentrophorids that is in a similar position but does not “bear” Müller’s vesicles. Foissner (1998b) thus argues that loxodids and kentrophorids are sister taxa. We remain skeptical until ultrastructural homologies of the kinetids are proved or until gene sequence data confirm these two groups as sister taxa.
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