First Record of Two Urostyloid Ciliates (Spirotrichea: Urostylida: Urostyloidea) from Brackish Water in Korea
- Author: Choi Jung Min, Kim Ji Hye, Shin Mann Kyoon
- Organization: Choi Jung Min; Kim Ji Hye; Shin Mann Kyoon
- Publish: Animal Systematics, Evolution and Diversity Volume 27, Issue3, p228~238, 30 Dec 2011
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ABSTRACT
Two urostyloid ciliates, collected from brackish water in Korea, were identified as
Diaxonella pseudorubra pseudorubra (Kaltenbach, 1960) Berger, 2006 andPseudokeronopsis flava (Cohn, 1866) Wirnsberger, Larsen and Uhlig, 1987. The description was based on living, protargol impregnated specimens. These species are described as follows:Diaxonella pseudorubra pseudorubra : body sizein vivo 145-230 × 40-60 μm, elongated ellipsoidal in shape. Cytoplasm reddish and flexible. Adoral zone of membranelles occupied 30-40% of the body; composed of 33-44 membranelles; 1-3 frontoterminal cirri, 1-4 frontal row cirri, 4-6 buccal cirri, 6-10 transverse cirri. Midventral rows composed of 14-24 cirri, four left marginal rows, one right marginal row. Two kinds of cortical granules; the larger one is yellowish and the smaller one is reddish.Pseudokeronopsis flava : body sizein vivo 150-210 × 30-45 μm, elongated ellipsoidal shape. Cytoplasm yellowish and flexible. Adoral zone of membranelles occupied 25-30% of body; composed of 44-58 membranelles in number. Frontal cirri forming bicorona composed of 5-7 cirral pairs, 2-3 frontoterminal cirri, one buccal cirrus, and 2-3 transverse cirri. Midventral rows composed of 18-33 cirri, 34-53 left marginal cirri, and 40-58 right marginal cirri. Two kinds of cortical granules; the larger one is colorless and “blood-cell-shaped,” and the smaller one is yellowish. Diaxonella pseudorubra pseudorubra is different from the most similar subspecies,D. pseudorubra pulchra , in cytoplasmic color and number of midventral cirri.Pseudokeronopsis flava is different from its most similar congeners in pigment granular color, number of bicorona, number of midventral cirri, and position of the con-tractile vacuole.
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KEYWORD
Diaxonella , Pseudokeronopsis , hypotrichs , redescription , estuary , brackish water , morphology
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The urostyloid ciliates are composed of a large group of hy-potrichs,
sensu lato , which belong to the superfamily Urosty-loidea, and more than 2,000 species have been described (Ber-ger, 2006; Lynn, 2008). Since the superfamily Urostyloidea was established by Butschli (1889), its definition has been improved as usually having an ellipsoidal, middle to large sized body and a midventral complex between the marginal rows (Corliss, 1979; Lynn and Small, 2002; Berger, 2006;Lynn, 2008). The systematics of genusDiaxonella has a comparatively complex history, including many synonyms (Jankowski, 1979; Foissner, 1987; Oberschmidleitner and Aescht, 1996; Berger, 2006; Shao et al., 2007).Diaxonella pseudorubra (Kaltenbach, 1960) was a monotypic species of the genusDiaxonella , but three subspecies,D. pseudoru-bra pseudorubra, D. pseudorubra polystylata, andD. pseudorubra pulchra , have been recognized recently by Berger (2006). The genus Pseudokeronopsis includes 10 species and is usually found in marine environments (Song et al., 2002, 2004, 2006). MostPseudokernopsis species have co-rtical granules colored red, yellow, or orange-yellow, which can be used to distinguish the species. In this study, we pro-vide morphological redescriptions and variations in two urostyloids from Korea.> Sample collection and enrichment
Diaxonella pseudorubra pseudorubra andPseudokeronopsis flava were collected from brackish waters in Korea.Diaxo-nella pseudorubra pseudorubra : (October, 2010; salinity 2‰) downstream of the sewage treatment plant (N34? 55′ 23′ ′, E128? 07′ 07′ ′) located in Sadeung-dong, Sacheon-si, Gyeong-sangnam-do. The water samples including the ciliates were collected with twigs, leaves, wood, and mud.P. flava : (Ja-nuary, 2010; salinity 20‰) in the Soesokkak estuary (N33? 15′ 7.19′′, E126? 37′ 24.59′′), Seogwipo-si, Jeju-do. The spe-cimens were transferred to a Petri dish (87 mm in diameter)or a cell culture dish (150 mm in diameter). These ciliates have been cultured at room temperature in the laboratory with collected water, enriched with dried wheat grain to supply fungal and bacterial nutrientsThe morphology of living specimens was observed under low (50-400×) and high (1,000×; immersion oil) magnifi-cations using a light microscope with a DIC device (Axio Imager A1; Carl Zeiss, Oberkochen, Germany) and their images were captured using a CCD camera (Axio Cam MRc; Carl Zeiss). The infraciliatures were observed after impre-gnation using the protagol method (Wilbert, 1975; Foissner, 1992). Terminology and taxonomic classification are accord-
ing to Berger (2006) and Lynn (2008).
Order Urostylida Jankowski, 1979
Superfamily Urostyloidea Butschli, 1889
Family Holostichidae Faure-Fremiet, 1961
Genus 1*Diaxonella Jankowski, 1979
2* Diaxonella pseudorubra pseudorubra (Kaltenbach, 1960) Tables 1, 2, Figs. 1-3)
Keronopsis pseudorubra Kaltenbach, 1960 (cited from Berger, 2006: 470).Keronopsis rubra Jerka-Dziadosz and Janus, 1972: 249.Diaxonella trimarginata Jankowski, 1979: 83; Oberschmi-dleitner and Aescht, 1996: 21; Shao et al., 2007: 25.Holosticha pseudorubra : Foissner, 1987: 225; Berger, 2001: 44.Diaxonella pseudorubra pseudorubra : Berger, 2006: 468.Description. General morphology and behavior : Bodysize 145-230 × 40-60 μm, usually about 170× 40 μm, length: width ratio about 4 : 1 on average in live specimens. Body shape elongated and ellipsoid with rounding at both ends(Figs.1 A, 2A, 3A), dorsoventrally flattened about 2 : 1, ven-tral side slightly concave, dorsal side convex (Figs.1 D, 2B). Cytoplasm reddish to wine color and flexible (Fig.2 D). Sin-gle contractile vacuole spherical and above the mid-body near the left margin (Figs.1 A, 2C). Locomotion usually crawl-ing on substrate. Omnivorous feeding (Fig.2 J-L).
Buccal field and oral infraciliature: Adoral zone of mem-branelles occupies 30-40% of body length (Figs.1 G, 3A), distal to proximal continuously semicircular, consists of 33-44 adoral membranelles (Fig.3 B), widest membranelle about 10 μm in length. Buccal area narrow and rather deep. Undu-lating membranes intersecting to half of the membranes, endoral membrane slightly curved and longer, paroral mem-brane anteriorly curved and shorter, distal end of paroral beyond endoral, about 45 μm in total length (Figs.1 G, 3B).Somatic infraciliature: Usually, four frontal cirri slightly enlarged, lying on front of the anterior region but one frontal cirrus near the distal end of the adoral zone of membranelles(Figs.1 G, 3C), about 17μm long. One to three frontoterminal cirri located on the right side of frontal cirri, about 12μm long (Fig.3 D). Four to six buccal cirri arranged along paroral membrane, about 8 μm long (Figs.2F, 3B). Inconspicuous, usually four frontal row cirri starting at the same level at the distal end of the paroral membrane and terminating at the same level at intersecting point of the undulating membranes(Figs.1 G, 3E). Midventral complex composed of 14-24 pairs of midventral cirri, continued frontoterminal cirri, arranged in a zigzag pattern, terminating at the posterior half but most cirri separated from others (Figs.1 G, 3G). Six to ten trans-verse cirri arranged in a J-shape, about 18 μm long (Figs.2 I, 3H). Two pretransverse cirri located near right transverse cirrus (Fig.3 H). One right marginal row consisting of 30-50 cirri (Figs.1 G, 3G). Four left marginal rows that graduallyshorten from right to left composed of 21-38, 20-33, 18-28,and 4-15 cirri, respectively (Figs.1 G, 3F). Three dorsal kine-ties complete, but some cases of extra dorsal bristles present,bristle about 3-4 μm in length (Figs.1 H, 2H, 3I).
Cortical granules: Two kinds of cortical granules present on both sides and pigmented: larger one greenish yellow about 1 μm in diameter, arranged linearly in short groups beside the cirral rows on the ventral side and densely arranged on the dorsal side but loosely around each kineties (Fig.1 B, C). Smaller one red wine colored, about 0.3μm in diameter, scat-tered around the whole body and arranged linearly in short groups between larger granules or around each cirrus (Figs.1E, 2G).Nuclear apparatus: Various shaped which elongated ellip-soidal to ovoid macronuclear nodules throughout the whole body, about 120 in number with several nucleoli. Spherical shaped micronuclei scattered body and 2.5 μm in diameter(Figs.1 H, 3A, J).Distribution. Europe (Austria, Germany, and Poland), Africa (Burundi) and Asia (China, Korea [present study]).Remarks. The taxonomy of the genusDiaxonella is relatively complicated. According to a review by Berger (2006) on this subspecies, Kaltenbach (see Berger, 2006) described original population that had two frontal rows, a reddish body color, several buccal cirri, and one left marginal row. Berger (2006) consideredKeronopsis pseudorubra sensu Kaltenbach in 1960 as a senior synonym ofDiaxonella trimarginata sensu Jankowski (1979) which was renamed as a new species and new genus based onKeronopsis rubra sensu Jerka-Dziadosz and Janus (1972), because they misidentified it. Furthermore, he changed the name fromKeronopsis pseudorubra toDiax-onella pseudorubra . Berger (2006) also suggested that the genusDiaxonella is monotypic and dividedD. pseudorubra into three subspecies, which are distinguished by body color, number of midventral pairs, and habitat. However, Shao et al. (2007) did not mention this suggestion of Berger (2006), because their publications overlapped in time.Consequently, this Korean population of
Diaxonella pseu-dorubra pseudorubra agrees with the original description except in the number of left marginal rows (4 vs. 1) and frontal cirri (3-5 vs. forming bicorona), which were intensively considered by Berger (2006). Additionally, our population agrees well with subsequent redescriptions of Austrian, Chi-nese, and Polish populations (Jerka-Dziadosz and Janus, 1972; Jankowski, 1979; Oberschmidleitner and Aescht, 1996; Shao et al., 2007). The Korean population differs slightly from the Austrian population ofD. pseudorubra pseudorubra in shape of micronuclei (spherical vs. ellipsoidal), number of frontal cirri (3-5 vs. 2-3), canals in the contractile vacuole (absent vs. present), number of pretransverse cirri (2 vs. 3-4), and position of the last midventral cirrus (posterior half vs. pos-terior) (Oberschmidleitner and Aescht, 1996). Furthermore, the Korean population differs from the Chinese population at the intersecting point (middle vs. posterior) of the undulat-ing membranes, the arrangement of reddish small cortical granules (linearly grouped vs. sparsely scattered), and the shape and diameter of micronuclei (spherical, about 2.5 μm vs. ovoid, about 5 μm) (Shao et al., 2007). Moreover, several populations (Europe, Asia, and Africa) ofD. pseudorubra pseudorubra have been found in freshwater but this Korean population was recovered from brackish water of an estuarinelittoral zone (Berger, 2006).
Family Pseudokeronopsidae Borror & Wicklow, 1983
Genus Pseudokeronopsis Borror & Wicklow, 1983
1*Pseudokeronopsis flava (Cohn, 1866) (Tables 3, 4, Figs. 4-6)
Oxytricha flava Cohn, 1866: 288.Holosticha flava Kent, 1882: 769.Keronopsis rubra Kahl, 1932: 571.Pseudokeronopsis flava : Wirnsberger et al., 1987: 79; Berger, 2001: 55; Song et al., 2004: 1137; Sun and Song, 2005:81; Berger, 2006: 940; Song et al., 2006: 272.Description. General morphology and behavior: Body size 150-210× 30-45 μm, usually about 180× 40 μm, length : width ratio about 5 : 1 in live specimens. Body shape elon-gated elliptical, both ends narrowly rounded, anterior portion usually concave leftwards (Figs.4 A, 5A), dorsoventrally flat-tened about 2 : 1 (Fig.5 B). One contractile vacuole located below the mid-body near the left cell margin about 13 μm in diameter (Figs.4 A, 5E). Cytoplasm very flexible but not con-tractile(Fig.5 C), almost yellowish at low magnification. Locomotion usually crawling on substrate, wrapping to change direction (Fig.5 C). Omnivorous feeding (Fig.5 J, K).Buccal field and oral infraciliature: Adoral zone of mem-branelles occupies 25-30% of body length, composed of 44-58 adoral membranelles (Figs.4F, 6A). Buccal area narrow and rather deep. Paroral and endoral membranes slightly curved, intersecting to half of the membranes, endoral longer than paroral, about 35 μm in length (Figs.4F, 6A, D).
Somatic infraciliature: Frontal cirri arranged in two arcs forming bicorona comprising 5-7 cirral pairs, bicorona con-nect to midventral complex (Fig.6 E). Midventral complex extended to subposterior and consisting of 18-33 cirri; distance between posterior most cirrus of midventral cirri and upper-most transverse cirrus about 20 μm (Figs.4F, 6A). Two orthree frontoterminal cirri located at the right side of the right-most bicorona pair (Fig.6 C, E). Buccal cirrus located near the intersecting point of the undulating membranes (Fig.6 D).Two to four transverse cirri located posteriorly and distinctly separated by marginal rows (Figs.5 I, 6F). Right marginal row commenced at level of the down most bicorona cirrus,terminated at the posterior part and comprising 40-58 cirri (Figs.4F, 6A, E), left marginal row with 34-53 cirri; posterior
ends of marginal rows distinctly separated (Figs.4F, 6A). Dorsal bristles length 5-10 μm (Fig.5 D), three arranged kine-ties, dorsal kineties extending to entire dorsal surface (Figs.4G, 6B).
Cortical granules: Two types of cortical granules present on both sides (Figs.4 D, 5H); yellowish cortical granules form-ing four rows with cirral rows on ventral side (Figs.4 B, 5F), small groups with dorsal bristles on dorsal side and 0.8-1 μm in diameter (Figs.4 C, 5G, H), colorless cortical granules shaped ellipsoidal and “blood-cell-shaped” under both cortex and about 2×1.5 μm in size (Fig.5 G, H).Nuclear apparatus: 70-100 ovoid to ellipsoidal macronuclear nodules, size 5-10 μm long in protargol-impregnated speci-mens. Micronucleus inconspicuous, about 3 μm in diameter(Figs.4 G, 6A).Distribution. Europe (England, France, Denmark, Germany, Italy, and Poland), North America (USA), and Asia (China and Korea [present study]).Remarks . The Korean population ofPseudokeronopsis flava closely matched the original and subsequent redescriptions. However, the Korean population differs from the other populations in the pattern of undulating membranes. The undu-lating membranes of the Korean population usually have one intersecting point at the mid part, whereas those of the Chinese population have no intersecting point at the mid part. The length of the endoral membrane is usually longer than that of the paroral in the Korean population, whereas that of both membranes is equal in the Chinese population. However, the lengths of the endoral and paroral membranes of the Danish population are similar to those of the Korean popula-tion (Cohn, 1866; Song et al., 2004, 2006; Sun and Song, 2005; Berger, 2006). The size of the pigment granules is slightly different in the Korean and Chinese populations (0.8-1 μm vs. 0.5 μm) (Song et al., 2004, 2006).Closely-related species of
Pseudokeronopsis flava areP.carnea, P. flavicans, andP. rubra , but they can be distin-guished from each other as follows.Pseudokeronopsis flava is different fromP. carnea in terms of pigment granule color (yellow vs. red), number of bicorona (5-7 vs. 9-11), number of midventral cirri (ca. 25 vs. ca. 40), number of transverse cirri (2-4 vs. 8-9), number of dorsal kineties (3 vs. 7-8), and number of adoral membranelles (ca. 50 vs. ca. 70).Pseudokeronopsis flava is different fromP. flavicans in posterior body shape (slightly narrow vs. distinctly narrow), position of the contractile vacuole (posterior half vs. anterior half),number of dorsal kineties (3 vs. 5), and the gap between the posterior of the midventral row and transverse cirri (wide vs.narrow).Pseudokeronopsis flava is different fromP. rubra in pigment granule color (yellow vs. red) and number of dorsal kineties (3 vs. usually 4-6) (Song et al., 2002, 2004, 2006, Berger, 2006).Korean name: 1*쌍열충속, 2*붉은쌍열충 Korean name: 1*노랑위각모충
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[Table 1.] Morphometric data of Diaxonella pseudorubra pseudorubra
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[Table 2.] Comparisons of Diaxonella pseudorubra pseudorubra which has different names
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[Fig. 1.] Diaxonella pseudorubra pseudorubra from live (A-F) and impregnated specimens (G H). A Ventral view of a typical individual; B C Arrangement of cortical granules on ventral and dorsal sides; D Flattened lateral view; E Two kinds of cortical granules ondorsal side; F Various body shapes; G Somatic and oral infraciliature of ventral side; H Dorsal kineties and nuclear apparatus.AZM adoral zone of membranelles; BC buccal cirrus; DK dorsal kineties; EM endoral membrane; FC frontal cirri; FRC frontalrow cirri; FTC frontoterminal cirri; LMC left marginal cirri; Ma macronuclear nodules; Mi micronuclei; MVC midventral cirri; PM paroral membrane; PTC pretransverse cirri; RMC right marginal cirri; TC transverse cirri. Scale bars: A D G=50 μm E=5 μm.
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[Fig. 2.] Photomicrographs of Diaxonella pseudorubra pseudorubra from live specimens. A Ventral view of a typical individual; B Flattened lateral view; C Contractile vacuole (arrowhead); D Somatic ciliature of the ventral side; E Arrangement of corticalgranules on the ventral side (arrowheads); F Buccal cirri (arrows) and undulating membranes (arrowhead); G Patterns of corticalgranules: larger (arrowhead) and smaller (arrow) arrangement around dorsal bristle of smaller cortical granules (double arrowhead); H Dorsal bristles (arrowhead); I Pretransverse cirri (arrow) and transverse cirri (arrowhead); J-L Various food vacuoles; J Diatom Pleurosigma sp.; K Aspidisca sp.; L Small particle of wheat grain. Scale bars: A=50 μm G H=5 μm.
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[Fig. 3.] Photomicrographs of Diaxonella pseudorubra pseudorubra from impregnated specimens. A Ventral view of a typical individual; B Buccal cirri (arrowhead) and undulating membranes (arrow); C Four frontal cirri (arrowheads); D Two frontoterminal cirri (arro-wheads); E Frontal row cirri (arrowheads); F Four left marginal rows (arrowheads); G Right marginal row (arrowhead) and midventralcomplex (arrow); H Pretransverse cirri (arrow) and transverse cirri (arrowhead); I Dorsal kineties (arrowheads) and extra dorsalbristles (arrow); J Macronuclear (arrowhead) and micronuclei (arrows). Scale bars: A=50 μm J=10 μm.
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[Table 3.] Morphometric data of Pseudokeronopsis flava
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[Table 4.] Comparisons of different populations of Pseudokeronopsis flava
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[Fig. 4.] Pseudokeronopsis flava from live (A-E) and impregnated specimens (F G). A Ventral view of a typical individual; B Arrange-ment of cortical granules on the ventral side; C Three cortical granular rows on the dorsal side; D E Cortical granule groups (arrowhead) and “blood-cell-shaped” granules (arrow) apparatus; F Somatic and oral infraciliature of the ventral side; G Threedorsal kineties and nuclear apparatus. AZM adoral zone of membranelles; BC buccal cirrus; Bicorona FC arranged in arcs formingcirri; DK dorsal kineties; EM endoral membrane; FTC frontoterminal cirri; LMC left marginal cirri; Ma macronuclear nodules; MVCmidventral cirri; PM paroral membrane; RMC right marginal cirri; TC transverse cirri. Scale bars: A G=50 μm E=2 μm.
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[Fig. 5.] Photomicrographs of Pseudokeronopsis flava from live specimens. A Ventral view of a typical individual; B Flattened lateralview; C Showing flexible body; D Dorsal kineties (arrowheads); E Contractile vacuole (arrowhead); F Arrangement of corticalgranule on ventral side; G H Cortical granule groups (arrowheads) and “blood-cell-shaped” granules (arrow) apparatus on dorsalside; I Three transverse cirri (arrowhead); J K Various food vacuoles; J One kind of Chlorophyta; K Coleps sp. Scale bar: A=50 μm.
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[Fig. 6.] Photomicrographs of Pseudokeronopsis flava from impregnated specimens. A Ventral view of a typical individual; B Dorsalkineties (arrowheads); C Two frontoterminal cirri (arrowheads); D Buccal cirrus (arrowhead) and undulating membranes; E Infracil-iatureof bicorona (arrows); F Three transverse cirri (arrowhead). Scale bar: A=50 μm.