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Protistology the Taxonomic Position of Klosteria Bodomorphis Gen. and Sp. Nov. (Kinetoplastida) Based on Ultra Structure And

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Protistology the Taxonomic Position of Klosteria Bodomorphis Gen. and Sp. Nov. (Kinetoplastida) Based on Ultra Structure And Protistology 3 (2), 126-135 (2003) Protistology The taxonomic position of Klosteria bodomorphis gen. and sp. nov. (Kinetoplastida) based on ultra- structure and SSU rRNA gene sequence analysis Sergey I. Nikolaev1, Alexander P. Mylnikov2, Cedric Berney3, Jose Fahrni3, Nikolai Petrov1 and Jan Pawlowski3 1 A. N. Belozersky Institute of Physico-Chemical Biology, Department of Evolutionary Biochemistry, Moscow State University, Moscow, Russia 2 Institute for Biology of Inland Water RAS, Borok, Russia 3 Department of Zoology and Animal Biology, University of Geneva, Switzerland Summary A small free-living marine bacteriotrophic flagellate Klosteria bodomorphis gen. and sp. nov. was investigated by electron microscopy and molecular methods. This protist has paraxial rods of typical bodonid structure in the flagella, mastigonemes on the anterior flagellum, two nearly parallel basal bodies and discoid mitochondrial cristae. The flagellar pocket and cytostome/cytopharynx complex are supported by two microtubular roots and reinforced microtubular band (mtr). These features confirm that K. bodomorphis is a bodonid related to Bodo. However, the presence of a layer of dense glycocalyx on the flagella and one battery of cylindrical trichocysts with reticular walls makes it more similar to Rhynchobodo/Phyllomitus, although this flagellate characterized by pankinetoplasty. Phylogenetic analysis using the SSU rRNA gene is congruent with the ultrastructural studies and strongly confirms the close relationship of K. bodomorphis to the genus Rhynchobodo within the order Kinetoplastida. Key words: Bodonidae, Klosteria bodomorphis, evolution, 18S rDNA, phylogeny Introduction of kinetoplastid and related flagellates have been reinvestigated by electron microscopy (Brugerolle et al., Free-living kinetoplastids, especially bodonids 1979; Brugerolle, 1985; Mylnikov, 1986; Mylnikov et al., (Bodonidae Hollande), are an important component of 1998; Elbrächter et al., 1996; Simpson et al., 1997; marine ecosystems. In spite of the broad diversity and Frolov et al., 1997, 2001). frequent occurrence of free-living kinetoplastids, their The definition of even such a well-known and valid biodiversity and taxonomy are still poorly known. kinetoplastid taxon like Bodo, comprising an assem- Recently some well-known and new species and genera blage of free-living kinetoplastids with a more or less © 2003 by Russia, Protistology Protistology · 127 oval body, apical rostrum, two free heterodynamic Pratt medium for 15-30 min at 1°C. Then the prepa- flagella, and single kinetoplast (Vickerman, 1991), is rations were treated as in Mylnikov with coauthors (1998). unclear. In 1994 one of the authors (A.P. Mylnikov) DNA was extracted using the DNeasy Plant isolated a small bacteriotrophic flagellate from the Minikit (Qiagen, Basel, Switzerland). One microlitre littoral of the South Baltic. Originally, it was referred to (1 µl) of DNA extract was added for each PCR probe. the genus Bodo due to its cell shape, arrangement of PCR amplifications were done in a total volume of 50 flagella and behaviour, but subsequent ultrastructural µl with an amplification profile consisting of 40 cycles investigation demonstrated that a new genus should be with 30 s. at 94°C, 30 s. at 50°C, and 2 min. at 72°C, erected for this bodonid (Burzell, 1975; Brugerolle et followed by 5 min. at 72°C for the final extension. The al., 1979; Brugerolle, 1985) amplified PCR products were purified using the High However, ultrastructural studies did not clarify the Pure PCR Purification Kit (Roche, Rotkreuz, Switzer- taxonomic position of this flagellate within the bodonids land), then ligated into pGEM-T Vector System as its cell organization combines features of Bodo and (Promega, Wallisellen, Switzerland), cloned in XL-2 Rhynchobodo. Ultra-competent Cells (Stratagene, Basel, Switzer- There is a large SSU rRNA database for repre- land), sequenced with the ABI-PRISM Big Dye sentatives of Kinetoplastida. The monophyly of Terminator Cycle Sequencing Kit, and analysed with kinetoplastids was confirmed by molecular phylo- an ABI-377 DNA sequencer (Perkin-Elmer, Rotkreuz, genetic methods in spite of the high rate of SSU rRNA Switzerland), all according to the manufacturer’s gene sequence divergence within the group (Dolezel et instructions. The complete SSU rRNA gene of K. al., 2000; Maslov et al., 2001; Callahan et al., 2002; bodomorphis was amplified using the universal primers Hughes et al., 2003). The high level of genus divergence sA (5' ACCTGGT TGATCCTGCCAGT 3') and sB (5' complicates the phylogenetic comparison of kineto- TGATCCTTCT GCAGGTTCACCTAC 3'). The plastids with other groups of protists including their length of the amplified sequences of SSU rRNA of K. closest relatives, diplonemids and euglenids. Moreover, bodomorphis was 2072 nucleotides. there is a problem with the choice of an appropriate The complete SSU rRNA gene sequence from K. outgroup for kinetoplastids, because all available close bodomorphis was manually aligned with sequences from relatives are highly divergent, and this causes the biases diverse kinetoplastids, diplonemids and euglenids. of Long Branch Attraction artifact and partial loss of Preliminary phylogenetic analises were used to confirm phylogenetic signal. the grouping of K. bodomorphis within the bodonids (data In this study, we represent the ultrastructural not shown). Because of their extremely long branches, definition of the new genus and species Klosteria the diplonemids, euglenids, Ichtiobodo and Paradobodo bodomorphis. To confirm the phylogenetic position of were excluded from the alignment. The final alignment K. bodomorphis we compare its SSU rRNA gene comprised 19 sequences, including the sequence sequence to a representative data set including all genera obtained in this study. 1826 unambiguously aligned in the order Kinetoplastida. positions were used in the phylogenetic analyses. The sequence has been submitted to GenBank under Material and methods accession number AY268046. Phylogenetic trees were inferred using the maxi- A clonal culture of Klosteria bodomorphis sp. nov. mum likelihood (ML) method (Felsenstein, 1981). The was isolated from littoral samples of the Baltic Sea near reliability of internal branches was assessed using the the town of Kloster, Germany, in December of 1994. bootstrap method (Felsenstein, 1985) with 50 replicates. Cultures of K. bodomorphis were maintained in a ML analysis was performed using PAUP (Swofford Schmaltz-Pratt medium (add the following to 1 L of 1998) under the GTR model of sequence evolution water: 28.15 g NaCl, 0.67 g KCl, 5.51 g MgCl2·6H2O, (Lanave et al., 1984; Rodriguez et al., 1990), taking into 6.92 g MgSO4·7H2O, 1.45 g CaCl2·H2O, 0.1 g KNO3, account a proportion of invariable sites, and a gamma 0.01 g K2HPO4·3H2O) with salinity adjusted to 20‰ distribution of the rates of substitution for the variable and inoculated with bacteria Aerobacter (Klebsiella) positions, with 8 rate categories. All parameters for ML aerogenes as food. Cultures of this flagellate can be analysis were estimated from the dataset using obtained from the culture collection maintained at the Modeltest (Posada and Crandall, 1998). Starting trees Institute for Biology of Inland Waters, Russian were obtained via NJ, and then swapped using the tree- Academy of Sciences (Borok). bisection-reconnection algorithm. For electron microscopy a suspension of cells was ABBREVIATIONS collected and fixed with a mixture of 2% OsO4 and 0.6 % glutaraldehyde (final concentrations) on Schmaltz- af - anterior flagellum, amt - additional micro- 128 · Sergey I. Nikolaev et al. tubules, b - bacterium, bp - basal plate, c - cytostome, cp near the basal bodies. The dorsal root of 2-3 microtubules - cytopharynx, db - dorsal band of microtubules, dr - dorsal begins from the basal body of the anterior flagellum and microtubular root, f - fibril, fp - flagellum pocket, fv - food goes up to form the dorsal submembrane band of more vacuole, ga - Golgi apparatus, m - mitochondrion, mn - than 25 microtubules (Figs 4, 5, 7-10). The dorsal root mastigonemes, mtr - reinforced band of microtubules, pf is associated with the electron dense lamina (Figs 5, 8). - posterior flagellum, ss - storage substance, tc - trichocyst, The ventral root of the flagella begins as 6 microtubules v - vesicle, vb - ventral band of microtubules, vr - ventral near the posterior flagellar basal body and goes behind microtubular root. to form the ventral band of 27 microtubules (Figs 6, 8, 9, 13). Additionally, the two microtubules can be seen Results between the basal bodies (Fig. 11, arrow). On the cross section of flagellar pocket the band of 4-5 microtubules have been found (Figs 8-10). These microtubules are ELECTRON MICROSCOPY connected with the surface of the flagellar pocket by K. bodomorphis has bean-shaped, slightly flattened fibrillar bridges (Fig. 13). This band forms the so-called cells. The cell body is of 5.4-9.0 µm (usually 6.5-7.0 MTR band sensu Brugerolle with coauthors (1979) as a µm) in length. Two heterodynamic flagella emerge from reinforced band of microtubules. It goes along the wall the shallow flagellar pocket which occupies subapical of the flagellar pocket and turns to the cytopharynx (Fig. position. The anterior flagellum is of 12 µm and is 12), where the band is supplemented with additional directed ahead forming a flexible hook. The posterior microtubules (Figs 14-16). Assemblages of microtubules flagellum is of 17 µm and is derected backwards. Both such as the
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