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Protistology Serotypes in the Ciliate Dileptus Anser: Epigenetic

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Protistology 2 (3), 142–151 (2002) Protistology Serotypes in the ciliate Dileptus anser: epigenetic phenomena Alexander L. Yudin and Zoya I. Uspenskaya Institute of Cytology, Russian Academy of Sciences, St. Petersburg, Russia Summary This review presents some data obtained by the authors in their study of the serotype system in the lower ciliate Dileptus anser, a species that has not been explored previously in this aspect. These data show many features similar to those described in serotype systems of higher ciliates, Paramecium and Tetrahymena. At the same time, some of the results do not agree with conventional patterns generally accepted for these classical objects. The authors discuss the data obtained in dilepti in terms of epigenetic variation and inheritance. Key words: ciliates, Dileptus anser, serotypes, immobilization antigens, nonMendelian inheritance, serotype transformation, regulation of serotype expression, epigenetic variation and inheritance In the ciliates Paramecium and Tetrahymena, their at any one time, only one iantigen is detectable on the serotype systems have long been studied and were cell surface of all genotypically available antigens. In a revealed to have a diversity of peculiar properties. number of cases, this rule is followed not only by The ciliate serotype is principally defined through different genes, but also by different alleles of the same the use of immunological techniques and depends on a gene. Exceptional cases (in which two or more i certain class of proteins distributed all over the surface antigens are revealed simultaneously on the cell surface) of the external cell membrane and cilia (Beale and Mott, occur very seldom. When cultural conditions are 1962; Doerder, 1981). These proteins are referred to as changed or some treatments are used, a replacement immobilization antigens, or iantigens, as ciliates of one surface protein with another (of all proteins treated with the homologous immune serum (IS) at coded in the cell genome) takes place, which is referred specific concentrations turned out to be immobilized. to as the cell serotype transformation. This alteration So far, functions of iantigens are not known. Their usually involves most or even all cells in the clone and peculiar feature is their great diversity and variability appears to be totally reversible. Thus, different serotypes that were first noted as early as in the 1940s (see one of are expressed under different conditions of temperature, the first reviews by Beale, 1954). The ciliates that belong salinity, feeding, etc., and each set of conditions is to the same clone can express various iantigens. To characteristic of the expression of a specific iantigen illustrate this, in the best studied species of the P. aurelia over some range, these ranges being sometimes more complex, the genome of each cell contains up to 12 non or less overlapping. linked genes that code different iantigens. This gene Once established, a particular serotype tends to be system operates on the principle of «mutual exclusion»: inherited (the socalled «functional inertia» Nanney, © 2002 by Russia, Protistology Protistology · 143 1980). More specifically, it is not infrequent that ciliates Sciences, St. Petersburg, and the prime objective of the with the same genotype (for instance, from the same present paper is to review and to systematize these clone) that were cultured under different conditions experiments, the primary emphasis being focused on and, therefore, expressed different serotypes, maintain epigenetic phenomena. these specific serotypes through cell generations, when Methods for cultivation, cloning, and crossing of transferred to a «zone of overlapping». In other words, Dileptus anser (Ciliata, Holotricha, Gymnostomatida) under the same conditions, ciliates of the same genotype (= D. margaritifer Wirnsberger et al., 1984) at the are capable of expressing and inheriting more than one Laboratory were developed quite recently. D. anser distinct phenotype. Therefore, phenomena of epi seems to be a very promising laboratory model due to genetic variation and inheritance are very typical of some peculiar features of this ciliate (Yudin et al., 1988). serotype systems in ciliates. It is to be recalled that one Unfortunately, data on its nuclear apparatus, conju of the first hypothetical models for epigenetic control gation, and conjugation cycle are as yet rather scant, of characters in Paramecium was proposed to explain although it is the nuclear apparatus that allows to peculiarities of the genetic control and inheritance of consider D. anser a lower ciliate. Some earlier data on its serotypes (Delbrück, 1949); this hypothesis provided the nuclear apparatus were reviewed by Dragesco a basis for numerous subsequent ideas of the kind (1963). Small spherical micronuclei (6 to 20) divide by (reviews: Olenov, 1965; Golubovsky, 1996; Golubovsky mitosis at the beginning of cell division. Immediately and Tchuraev, 1997; Riggs and Porter, 1996; Russo et afterwards the macronucleus that consists of numerous al., 1996; and some others). fragments (the socalled «fragmented», or «pulverized», It is generally agreed that the most exciting issues macronucleus) starts its division. The sexual process in serotype systems of ciliate are the mechanisms of has the form of conjugation. Three mating types (I– regulation of the genes coding iantigens under normal III) were discovered. Usually, conjugation occurs only conditions and during serotype transformation, which between cells of complementary mating types (Yudin provide their expression in accordance with the and Afon’kin, 1987; Yudin et al., 1988, 1990; Afon’kin, principle of «mutual exclusion» and the tendency of 1990). There is no autogamy in the D. anser life cycle the once established serotype towards inheritance in (it is to be recalled that, in Paramecium aurelia species, subsequent cell generations. These problems were the autogamy settles homozygosity for all genes!). On the objective of many studies (the review of their current whole, the pioneering studies of nuclear behavior during status and the basic literature — Bleyman, 1996). In conjugation (Vinnikova, 1974a, 1974b, 1975, 1976; the most advanced cases, not only surface proteins that Karadzhan, 1985; Golinska and Afon’kin, 1993) allow determine various serotypes were thoroughly charac a preliminary conclusion that D. anser are diplonts with terized, but also corresponding genes were isolated and gametic reduction of the chromosome number and sequenced (Preer, 1986; Schmidt, 1996). Nonetheless, classical (metazoan) meiosis (the same being true of the abovementioned special features of serotype all ciliates — Raikov, 1972). systems in ciliates remain unexplained, even though A set of D. anser clones was used in our experi numerous hypotheses are proposed and verified ments, each clone being derived from cells isolated at experimentally (Capdeville, 1979; Finger et al., 1995, different time from several ponds of the Leningrad 1995/1996; Leeck and Forney, 1996). District. The ciliates were cultivated in Prescott’s salt It is important that a large body of data on the ciliate solution at 25°C and fed with Tetrahymena pyriformis serotypes accumulated so far were obtained almost (Nikolaeva, 1968). For special purposes, some clones exclusively on a few higher ciliates — 3 to 4 species of were incubated at 17, 19, 21 or 23°C. Immune sera (ISs) the Paramecium aurelia complex and, to a lesser extent, were raised against some of the clones by immunization on several other Paramecium species and Tetrahymena of rabbits with the whole cell homogenates. The thermophila (Bleyman, 1996). Needless to say, these antiserum was referred to as homologous with respect welldeveloped model objects enable performing to the clone used for immunization, and as hetero modern molecular genetic studies but, at the same time, logous, for all other clones. The serotype of cells was it makes it difficult to discriminate between more determined mainly from their immobilization by native general and more special phenomena and patterns. ISs (the socalled standard immobilization test). Therefore, it is tempting to recruit some novel species Additionally, a method of indirect immunofluorescence for studies — it may also provide a fresh knowledge of was also periodically used. Occasionally, concentrated the serotype systems. For the last few years, serotypes IS (specifically, their gammaglobulin fractions) were of a lower ciliate, Dileptus anser, have been examined obtained for tests with reaction of precipitation in agar. at the Laboratory of Cytology of Unicellular Orga In one of our earlier experiments, 20 D. anser clones nisms, Institute of Cytology, Russian Academy of of various origin were tested with two ISs obtained 144 · Alexander L. Yudin and Zoya I. Uspenskaya against two of the clones; the total of 38 heterologous are expressed simultaneously at both temperatures — combinations «cells — ISs» were thereby tested contrary to the principle of mutual exclusion. (Uspenskaya, 1988). The dilepti similar to Paramecium As to inheritance of serotypes during agamic and Tetrahymena showed an effective capability of reproduction of D. anser, the serotype of each clone inducing specific antibodies in immunized rabbits: both usually remained invariable in successive cell gene the ISs had high titers and produced a quite evident rations, if the clone was cultivated under invariable immobilization reaction with homologous cells, which conditions. Some clones were
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