Abstract. In this study, morphology of a Brazilian population of Eschaneustyla terricola Foissner, 1982 and a Chinese population of E. lugeri Foissner, Agatha & Berger, 2002 were studied based on living observation and protargol impregnation. Several stages of morphogenesis in E. lugeri were reported and the most remarkable features are characterized as follows: (1) partly renewal of adoral zone of membranelles in the proter and the parental midventral cirri do not join the construction of the opisthe's oral primordium; (2) three or four buccal cirri each develop from one frontoventral cirral anlage and undulating membranes anlage generates two frontal cirri; (3) frontoventral cirral anlagen n and n-1 develop de novo and in the frontoterminal cirral row, respectively; (4) intrakinetal development of marginal and dorsal kineties anlagen; (5) fusion of macronuclear nodules into a single mass.
Key words: Ciliates; infraciliature; ontogenesis; urostylid
INTRODUCTION
The hypotrichs s. l. are one of the most diverse and speciose ciliate groups with about 700 valid species described so far (Berger 1999, 2006, 2008, 2011; Foissner et al. 2002; Foissner 2016). Recently, much work has been carried out on the morphological and molecular diversity of hypotrichs, helping to improve the knowledge on their phylogeny, even though it remains unresolved at various levels (Shao et al. 2011, 2013a, b, 2014; Li et al. 2013; Heber et al. 2014; Paiva et al. 2014, 2016; Jo et al. 2015; Luo et al. 2015; Singh and Kamra 2015; Bharti et al. 2016; de Castro et al. 2016, 2017; Wang et al. 2016, 2017; Chen et al. 2017).
Among hypotrichs, the urostylid genus Eschaneustyla, established by Stokes (1886) with E. brachytona as the type species, is mainly characterized by the following features: (1) several frontal cirri arranged in two or more rows (multi-corona); (2) more than two frontoterminal cirri forming distinct row; (3) transverse cirri absent; (4) four dorsal kineties; (5) number of caudal cirri distinctly increased. Since then, two other species were established in Eschaneustyla, namely E. terricola Foissner, 1982 and E. lugeri Foissner, Agatha and Berger, 2002. Due to the lack of thorough studies, Eschaneustyla has been placed in rather different taxa or even misclassified repeatedly in the past (for revision, see Berger 2006). Based on the similarity in frontal ciliature (multi-corona) and midventral complex (composed of midventral rows only), Berger (2006) assigned Eschaneustyla in Epiclintidae alongside Epclintes, but he claimed that further data are needed to evaluate this classification. Lyu et al. (2018) found that Eschaneustyla and Epiclintes are distantly separated in phylogenetic trees, and classified Eschaneustyla as incertae sedis within Urostylida.
This study contributes to the knowledge on Eschaneustyla by characterizing a population of E. terricola from the Brazilian Amazonia, and another of E. lugeri from China. The divisional morphogenesis of the latter is described.
MATERIALS AND METHODS
Sampling and identification
Eschaneustyla terricola was obtained from samples of soil with litter collected from a forest area (3°05'S 59°58'W) in Manaus, Amazonas, Brazil, in November 2014, and E. lugeri was obtained from the moss scrapped from a damp rock in Mount Zhongnan (33°59'N, 108°59'E), Xi'an, China, in March 2016.
Ciliates were made to excyst by employing the non-flooded Petri dish method (Foissner, 1992). Raw cultures were established at room temperature (about 24°C) using Petri dishes filled with filtered soil percolate. Some squashed wheat grains were added to support microbial growth. Although we could not establish a clonal culture for Eschaneustyla terricola and E. lugeri, the specimens used for morphological and molecular analyses were very likely conspecific because no other Eschaneustyla-like morphospecies were found during live observations and in the protargol preparations. This population of E. lugeri is identical with Eschaneustyla lugeri KY874005 sequenced by Lyu et al. (2018).
Isolated ciliate cells were observed in vivo using bright-field and differential interference contrast microscopy. Infraciliature was revealed using the protargol preparation method of Wilbert (1975). Counts and measurements of impregnated specimens were performed at a magnification of 1250×. Drawings of stained cells were made with the help of a camera lucida. To illustrate the changes occurring during morphogenetic process, old (parental) structures are depicted by contour, whereas new ones are shaded black (Shao et al. 2007, 2012). Terminology follows Berger (2006) and systematics is mainly based on Adl et al. (2012) (for the use of 'Hypotrichia') and Lynn (2008) (for classification under subclass-level).
Voucher slides containing both species were deposited in Lab of Protozoology, Xi'an Jiaotong University, China, with E. terricola under the registration number LEO20150421011/2 and E. lugeri under the registration numbers DYF2016031701A-G.
RESULTS
Morphology of Brazilian population of Eschaneustyla terricola Foissner, 1982 (Figs 1A, B, 2D, E; Table 1)
Body outline long oval with anterior end broadly rounded and posterior end narrowly rounded, very flexible but not contractile, size in vivo about 170 × 50 µm. Contractile vacuole at leftbody margin slightly ahead of mid-body (Fig. 2E). Cortical granules colorless, about 0.5 µm across, grouped or arranged in longitudinally oriented short rows throughout body (Fig. 2D). Cytoplasm colorless. 59-106 macronuclear nodules, scattered throughout cell body; one to five micronuclei (Fig. 1B). Cirral pattern and number of cirri of usual variability, basically as depicted in Fig. 1A, B. Adoral zone of membranelles (AZM) with 35-47 membranelles of ordinary composition, occupies ca. 30% of body length in protargol preparation; DE-value ca. 0.32. Paroral and endoral short, slightly curved and intersected. Invariably one buccal cirrus. Five to seven oblique cirral rows in frontal field, each composed of three to five, usually four cirri, except the anteriormost one which comprises seven to nine cirri. Frontal cirrus isolated in leftanterior corner of adoral zone, slightly enlarged. Anteriormost cirri in anteriormost two rows as large as the frontal cirri isolated in right anterior corner of adoral zone. Two to four long cirral rows in postoral region extend to about posterior third of cell. Frontoterminal row composed of 20-28 cirri, commences near distal end of AZM and terminates at or behind mid-body (on average 60% of body length). One leftand one right marginal row; leftrow slightly curved rightwards anteriorly (Fig. 1A). Transverse cirri absent (Fig. 1A). Invariably four rows of dorsal kineties with rows 1 and 3 slightly shortened anteriorly, each with two to four caudal cirri, thus eight to 14 in total (Fig. 1B). Length of dorsal bristles is about 5 µm.
Morphology of Chinese population of Eschaneustyla lugeri Foissner, Agatha and Berger, 2002 (Figs 1C-E, 2A-C; Table 1)
Body outline elongate elliptical and often slightly sigmoidal with anterior end broadly rounded and posterior end narrowly rounded, very flexible but not contractile, size in vivo about 200 × 60 µm. Contractile vacuole at leftbody margin slightly ahead of mid-body (Figs 2A, B). Cortical granules were failed to observe during living observation, but globular extrusomes were found after protargol impregnation. Extrusomes arranged around cirri and dorsal bristles, and irregularly scattered (Fig. 2C). Cytoplasm colorless, without conspicuous inclusions (Figs 2A, B). Nuclear apparatus occupying whole cell body, composed of 97-149 macronuclear nodules and three to 11 micronuclei (Fig. 1E). Cirral pattern and number of cirri of highly variability. AZM with 47-74 membranelles of ordinary composition, occupies 20%-37%, on average 28% of body length (DE-value on average 0.42). 25-43 frontal cirri form distinct short rows composed of 4 or 5 cirri each, except the leftmost one that composed of only two cirri. Paroral and endoral intersect optically after protargol impregnation. Usually three or four buccal cirri right of mid-portion of paroral (Fig. 1D). The majority of the specimens observed have one long, slightly oblique midventral row (as shown in Fig. 1D). However, a small number of specimens (about 4 in 60 specimens observed) have a cirral pattern composed of two long midventral rows: the leftone (midventral row 1 = MV1) and the right one (midventral row 2 = MV2) (Fig. 1C). The length of MV2 could be as similar to that of MV1, or rather short. MV2 could commence at the same level as frontoterminal row, or slightly behind anterior end of frontoterminal row, or at around onethird of body length (Fig. 1C). Specimen on the lower right in Fig. 1C shows a rather special cirral pattern that MV2 terminates near rear body end as frontoterminal row in other specimens, whereas frontoterminal row terminates quite ahead. One leftand one right marginal row, leftrow distinctly curved rightwards anteriorly; transverse cirri absent (Fig. 1D). Usually four rows of dorsal kineties, each with one to three, thus totally seven to 11 caudal cirri (Fig. 1E). Length of dorsal bristles is about 5 µm.
Morphogenesis in Eschaneustyla lugeri (Figs 1F-L, 2F-M)
Stomatogenesis. In the proter, the oral primordium commences in deep of the cortex independently, at around the proximal portion of AZM. Undulating membranes anlage that develops on the surface found to the right of oral primordium at the same time (Figs 1F, G; 2G). Specimen in Fig. 2G somewhat twisted at anterior portion, thus the undulating membranes anlage presented to the leftof the oral primordium. Parental undulating membranes not observed in this stage, we speculate that it disorganized into undulating membranes anlage. Parental buccal cirri might be absorbed in earlier stage due to their absence in this stage. Stomatogenesis of the opisthe commences with the proliferation of basal bodies around and on the leftof midventral row 1, in which posterior cirri gradually absorbed (parental cirri become smaller without any sign of disaggregation, thus absorption is supposed) (Figs 1F, 2F).
The proter's oral primordium subsequently moves to the proximal end of AZM and develops in the shape of a round concavity. The central part still remains in the depth of the cortex while the surrounding portion gradually migrates to the surface (Fig. 1H). Basal bodies then move along the leftmargin of AZM and engage in the renewal of membranelles with dissolving of parental membranelles (Fig. 1I). Undulating membranes anlage elongates anteriorly and connects with the oral primordium at the posterior end (Figs 1H, I; 2H).
Membranelles begin to differentiate at the right anterior part of opisthe's oral primordium (Figs 1F, H). Meanwhile, undulating membranes anlage for the opisthe appears, with differentiation commencing at the anterior end to form the leftmost frontal cirri (Fig. 1H).
In the mid-to-late stage, renewal of posterior portion of parental AZM continues on, which will eventually result in a partly renewed AZM of the proter. It should be noted that except for the few most proximal membranelles replaced by the new structure, others only slightly renewed at leftsides. Specimen observed reveals that residual oral primordium of the proter has all migrated to the surface by this stage. As for the opisthe, membranelles continue to differentiate posteriad. Note that two leftmost frontal cirri of the opisthe have already formed from frontoventral cirral anlage I (Fig. 1K).
Development of frontoventral cirri. In early dividers, posterior portion of the parental frontal cirri dissolve into basal bodies, which begin to form the frontoventral cirral anlagen of the proter (Figs 1F, H; 2H). A few frontoterminal cirri near proximal end of AZM disaggregate to develop the penultimate frontoventral cirral anlage. A small field of basal bodies, regarded as the frontoventral cirral anlage n, develop on the right side of frontoterminal row de novo. Opisthe's frontoventral cirral anlagen appear on the right side of frontoventral cirral anlage I. Due to the hypochromatism after protargol impregnation, a small field around frontoterminal row in mid-body region was difficult to see (dashed circle in Fig. 1H). Only a few cluttered basal bodies develop around this field. It is not known whether these basal bodies completely come from dissolving frontoterminal cirri (Fig. 1H). In the next stage, frontoventral cirral anlagen develop into distinct streaks and elongate posteriad in both daughter cells. About 9-11 frontoventral cirral anlagen, including the last and the penultimate anlagen, eventually formed (Figs 1I, 2L). In some filial products, several small anlagen formed on the leftof penultimate frontoventral cirral anlage, and these anlagen will possibly be absorbed subsequently (Fig. 2L). In the mid-to-late stage, frontoventral cirral anlagen segment and cirri gradually formed. The rightmost and the penultimate frontoventral cirral anlage eventually develops into the new frontoterminal row and MV1 respectively, while the rest of frontoventral cirral anlagen each splits to form about 4-6 cirri (Figs 1K, 2K, M). Although late dividers not found, we could believe that formation and migration of new cirri, and absorption of old ones are the main events during the rest of the morphogenetic process.
Marginal and dorsal anlagen. Two separate marginal anlagen develop intrakinetally within both leftand right marginal rows. Cirri adjacent to anterior end of each marginal row and cirri slightly behind mid-body differentiate to form these two anlagen, respectively (Figs 1I, K; 2K). These anlagen then increase in size and develop into new cirri that eventually replace the old ones.
During the formation of dorsal kineties, two anlagen develop intrakinetally in each parental row. These anlagen then elongate and develop into new structures, along with the incorporation or absorption of parental structures (Figs 1J, 2I).
Division of the nuclear apparatus. Macronuclear nodules fuse into many masses during early stage (Fig. 1J) and eventually fuse into a single mass that divides subsequently during mid-to-late stage (Figs 1L, 2J). Micronuclei divide mitotically during cell division (Fig. 1J).
DISCUSSION
Identification
Eschaneustyla terricola was described by Foissner (1982) based on live and protargol-impregnated specimens. Until the present study, two other populations have been reported, one by Eigner (1994), who identified it as E. brachytona and considered E. terricola as its junior synonym, and another by Foissner et al. (2002). Compared with the type population, the Brazilian population has a longer frontoterminal row (terminating behind mid-body vs. terminating at about buccal vertex) as in Eigner's (1994) population, and more macronuclear nodules (59-106 vs. 45-75). However, we consider these to be population-specific differences, as conspicuous variability among populations, perhaps due to cryptic speciation, has been noticed by Foissner et al. (2002). The most important difference consists of the cortical granules, which are colorless and arranged in groups or longitudinally oriented short rows in Brazilian population, while yellowish in the others. The colorless granules might be indicative that the Brazilian population belongs to E. brachytona, which is colourless (Stokes, 1886). However, it is not known if the limnetic E. brachytona, has actual colorless cortical granules or if the granules are absent. Thus, regarding the synonymy with E. terricola, we agree with Foissner et al. (2002) that confirmation must wait for new data of a limnetic Eschaneustyla, as the other known populations are terrestrial. Since most morphological characters of the Brazilian population are within the range of the original description, we consider it conspecific with E. terricola.
Eschaneustyla lugeri was described by Foissner et al. (2002) based on live and protargol-impregnated specimens, and one Korean population (Kim and Min 2015) has been reported after the original description. The Chinese population is virtually identical to the original population in terms of infraciliature and most living features, except for a greater number of macronuclear nodules (97-149 vs. 49-76), however such difference might be population-dependent. Rare specimens with two long midventral rows, namely MV1 (= rightmost midventral row in Foissner et al. 2002, Kim and Min 2015) and MV2 (= rightmost midventral row in our population), were found in Chinese population, indicating a level of variability. Since the Chinese population accords well with the type population in most features, their conspecificity is assumed.
Morphogenesis in Eschaneustyla lugeri
The most notable feature of Eschaneustyla lugeri is that the frontal area is densely covered by cirri forming distinct rows. Morphogenetic data shows that these cirri develop in the same way as midventral rows in other urostylids, i.e. two leftmost frontal cirri are formed by frontoventral cirral anlage I and the others are formed in rows of 4 or 5 cirri within frontoventral cirral anlagen II to n-2.
It is remarkable that proter's frontoventral cirral anlage n, which eventually becomes frontoterminal row, develops de novo, while frontoventral cirral anlage n-1, which forms MV1, comes from dissolving parental frontoterminal cirri.
It also should be noted that the number of cirri formed by frontoventral cirral anlage II is about 4. Therefore, the possibility is rather high that anterior 3 or 4 frontoventral cirral anlagen (excluding frontoventral cirral anlage I) contribute their last segments to form the buccal cirri. This was observed in Apokeronopsis bergeri (Li et al. 2008).
Hitherto, only one Eschaneustyla species, namely E. terricola, has been studied morphogenetically (Eigner 1994). Based on the current observation, these two species have several morphogenetic features in common: (1) the parental AZM is partly renewed at the proximal end; (2) the old undulating membranes completely disorganize into anlage; (3) marginal anlagen and dorsal anlagen develop intrakinetally within parental structures; (4) macronuclear nodules fuse into a single mass during morphogenetic process; and (5) many oblique frontoventral cirral anlagen appear during morphogenesis, and parental cirri contribute to the formation of proter's frontoventral cirral anlagen. These are also plesiomorphies occurring in many other urostyloids. Besides, based on the dividers depicted by Eigner (1994), we speculate that proter's frontoventral cirral anlagen n and n-1 in E. terricola possibly share the same origins as those in E. lugeri, that anlage n develops de novo while n-1 comes from parental frontoterminal cirri. We deduce that Eigner might misinterpret the origins of these two anlagen.
Meanwhile, some differences exist between Eschaneustyla lugeri and E. terricola: (1) anlage I develops into 2 frontal cirri in E. lugeri but only 1 cirrus in E. terricola; (2) in E. lugeri, oral primordium forms in the proter and engages in the renewal of membranelles, while no oral primordium is formed in proter and basal bodies from the dissolved parental undulating membranes and proximal membranelles contributes to the renewal of proximal membranelles in E. terricola.
Acknowledgements. This study was supported by Natural Science Foundation of China (31872190, 31660620); Conselho Nacional de Desenvolvimento Científico e Tecnológico (Universal 485974/2013-4), Brazil; and Programa de cooperação técnico científico e pedagógico (PROTEC UERJ-UEA), Brazil.
Address for correspondence: Sang Ba, School of Sciences, Tibet University, Lhasa 850000, China; Tel./Fax: +86 0891 640 5211; E-mail: [email protected]
Thiago da Silva Paiva, Laboratório de Protistologia, Dept. de Zoologia, Inst. de Biologia, CCS, Universidade Federal do Rio de Janeiro - UFRJ. CEP: 21941-092 Ilha do Fundao, Rio de Janeiro, RJ, Brazil; Tel./Fax: +55 21 3938 6363; E-mail: [email protected]; [email protected]
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Received on 17th, December, 2017; revised on 27th April 2018; accepted on 1st May, 2018
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Abstract
In this study, morphology of a Brazilian population of Eschaneustyla terricola Foissner, 1982 and a Chinese population of E. lugeri Foissner, Agatha & Berger, 2002 were studied based on living observation and protargol impregnation. Several stages of morphogenesis in E. lugeri were reported and the most remarkable features are characterized as follows: (1) partly renewal of adoral zone of membranelles in the proter and the parental midventral cirri do not join the construction of the opisthe's oral primordium; (2) three or four buccal cirri each develop from one frontoventral cirral anlage and undulating membranes anlage generates two frontal cirri; (3) frontoventral cirral anlagen n and n-1 develop de novo and in the frontoterminal cirral row, respectively; (4) intrakinetal development of marginal and dorsal kineties anlagen; (5) fusion of macronuclear nodules into a single mass.
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1 School of Sciences, Tibet University, Lhasa, China
2 Institute of Evolution and Marine Biodiversity, Ocean University of China, Qingdao, China
3 Key Laboratory for Space Bioscience and Biotechnology, Institute of Special Environmental Biophysics, School of Life Sciences, Northwestern Polytechnical University, Youyi Xilu 127, Xi'an, Shaanxi, China
4 Laboratório de Protistologia, Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro-RJ, Brazil