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Observations on the ultrastructure of extrusomes in the hypotrichous ciliate Architricha indica (Protist, Ciliophora) Observations on the ultrastructure of extrusomes in the hypotrichous ciliate Architricha indica...
Zhang, Xiaocui; Yang, Linying; Wang, Yiwen; Ni, Bing; Al-Farraj, Saleh A.; Fan, Xinpeng; Gu, Fukang
2014-03-04 00:00:00
REVIEW Animal Cells and Systems, 2014 Vol. 18, No. 2, 83–92, http://dx.doi.org/10.1080/19768354.2014.906500 Observations on the ultrastructure of extrusomes in the hypotrichous ciliate Architricha indica (Protist, Ciliophora) a a a a b a* a Xiaocui Zhang , Linying Yang , Yiwen Wang , Bing Ni , Saleh A. Al-Farraj , Xinpeng Fan and Fukang Gu a b School of Life Sciences, East China Normal University, Shanghai 200062, China; Department of Zoology, College of Science, King Saud University, Riyadh 11451, Saudi Arabia (Received 6 January 2014; received in revised form 16 March 2014; accepted 16 March 2014) Extrusomes of different categories in ciliates have been suggested to have different structures and functions. To investigate the characteristics of extrusomes in the hypotrichous ciliate, we examined Architricha indica using scanning and transmission electron microscopy and electron microscopic enzymo-cytochemistry. The results showed that the mature extrusomes were ellipsoidal vesicles with structureless cavities on their anterior parts and arranged in rows beneath the pellicle; the extruded structures of extrusomes were cyathiform and can remain outside of the cell surface after extrusion. These findings differ distinctly from that of previously reported extrusomes in other ciliates and thus suggest a new type of extrusomes. These organelles originated from endoplasmic reticulum in the deeper part of the cytoplasm, underwent a serious of development, gradually migrated to the cortical cytoplasm and finally positioned in their functional areas. In contrast with lower forms of ciliates, density, arrangement, and localization of extrusomes in A. indica showed obvious differences between the ventral and dorsal surface of cells. This may be in some way related to the differentiation of the dorsoventral cortex, and functional ciliature happened to the hypotrichous ciliates. In addition, the extrusomes may perform protective or defensive function, which associates with the activity of mitochondria and contributes to the pellicle retrieval or renewal. Keywords: Architricha indica; extrusomes; morphology; localization; origin Introduction different from the extrusomes reported in other ciliates; additionally, their origin, morphogenesis and possible Extrusomes are membrane-bounded extrusive organelles functions were also discussed. widely owned by ciliated protozoa. They are considered to mainly play a defensive role by discharging their internal content to the outside of the cell in response to some Materials and methods mechanical, electrical, or chemical stimulus (Hausmann Materials 1978; Kugrens et al. 1994; Rosati & Modeo 2003; Buonanno et al. 2013). The previous researches mainly Architricha indica was collected from a pond in Chang- feng Park, Shanghai, China, in September, 2012. Isolated focused on some classical types of extrusomes, such as ciliates were cultivated in Petri dishes with filtered pond trichocysts, mucocysts, and toxicysts, which occurred in water at room temperature, and sterilized wheat grains most groups of lower forms of ciliates (Raikov 1992; were added weekly to support continuous bacterial food. Rosati & Modeo 2003). However, in recent years, several types of extrusomes were found successively in some hypotrichous ciliates, a more advanced ciliate group, for Identification instance, mucocysts in Urostyla grandis (Zhang et al. Living ciliates were observed using bright field and 2007) and in Diaxonella pseudorubra (Liu et al. 2009), differential interference contrast microscope (Olympus trichocyst-like extrusomes in Pseudourostyla cristata BX 51). Staining with protargol was performed to reveal (Zhang et al. 2011), and mushroom-like extrusomes in infraciliature as described by Wilbert (1975). The living Pseudourostyla nova (Zhou et al. 2011) and in Anteho- cells possess flexible body and cortical granules on both losticha monilata (Zhang et al. 2012). In this study, the sides (Figure 1A and 1B). Infraciliature comprises 18 cyathiform extrusomes of hypotrichous ciliate A. indica frontal-ventral-transverse cirri, three right and two left were investigated using electron microscopy and electron marginal rows on ventral side, and six dorsal kineties microscopic enzymo-cytochemistry. Their morphology, and three caudal cilia on dorsal side. Two macronu- extrusion mechanism, and localization were obviously clear nodules are constantly present (Figure 1C). All *Corresponding author. Email: xpfan@bio.ecnu.edu.cn © 2014 Korean Society for Integrative Biology 84 X. Zhang et al. prefixed in a 1:1 mixture of 2% O O and 2.5% S 4 glutaraldehyde at 4°C for 10 min, rinsed with 0.1 M phosphate buffer, and postfixed in buffered 1% O O at 4°C S 4 for 60 min. The fixed cells were dehydrated in a graded series of acetone and embedded with Epon 812. Ultrathin sections were stained with uranyl acetate and lead citrate and observed with TEM (JEM-2100) at an accelerating voltage of 120 KV. Electron microscopic enzymo-cytochemistry Specimens for glucose-6-phosphatase (G-6-Pase) cyto- chemistry were prepared according to the method described by Gu et al. (2002). Ciliates were prefixed in 1.25% glutaraldehyde with 0.1 M sodium cacodylate buffer (pH 6.8) at 4°C for 5 min, rinsed in the same buffer, and then incubated in G-6-Pase incubating buffer at 37°C for 30 min. The incubated cells were washed in 0.1 M sodium cacodylate buffer (pH 7.2) and postfixed in buffered 1% O O at 4°C for 60 min. The postfixed S 4 cells were finally dehydrated, embedded, sectioned, and observed as routine TEM methods. Control cells were incubated in the reaction medium without substrate (potassium G-6-Pase). Results SEM observation Figure 1. Photographs of living and protargol-impregnated cells of A. indica. Scales are 10 µm. (A) The flexible body at low The cells of A. indica were dorsoventrally flattened, magnification. (B) Cortical granules on ventral side. (C) Ventral measuring 90–130 × 30–35 µm (Figure 2A and 2B). view of general infraciliature. AZM, adoral zone of membra- Adoral zone of membranelles (AZM) occupied ⅓ of cell nelles; FC, frontal cirri; LMC, left marginal cirri; Ma, macro- length; undulating membranes (UM) were located to the nuclear nodules; RMC, right marginal cirri; TC, transverse cirri; UM, undulating membranes. right of the AZM and extended to the cytostome. Eighteen frontal-ventral-transverse cirri were arranged characterist- ically as 8-5-5 type: eight frontal cirri (FC) were arranged characteristics correspond well with those of original in the anterior area of cell; five ventral cirri (VC), three report in Gupta et al. (2006), and the identification is postoral VC were forming a narrow group close to the with no doubt. proximal end of the AZM, and the remaining two pre- transverse VC were locating in the posterior quarter of the Scanning electron microscopy (SEM) cell; five transverse cirri (TC) were present in a tick mark configuration. There were two left and three right rows of Specimens for SEM were prepared according to the marginal cirri (LMC and RMC). Three dorsal kineties method described by Gu and Ni (1993). Ciliates were fixed in a 1:6 mixture of 1% O O and saturated solution (DK ) were extending the entire cell length. DK started 1–3 4 S 4 of HgCl at 4°C for 10 min and rinsed with 0.1M from the posterior ⅓ of the body; DK were posteriorly 5, 6 shorter. Three caudal cirri (CC) were located at the phosphate buffer. The fixed cells were then dehydrated posterior ends of DK , respectively. in a graded series of ethanol, dried with a critical point 1, 2 and 4 dryer (Hitachi HCP-2), and coated with gold with a Low magnification SEM revealed a great number of sputter coater (Cressington 108auto). Observation was granules distributed in different patterns on the ventral and performed using a scanning electron microscope (Hitachi dorsal surface of the cells (Figure 2A and 2B). On the S-4800) at an accelerating voltage of 10 KV. ventral surface, the granules were distributed irregularly in the anterior and the posterior parts of the cell, particularly near the FC and TC (Figure 3A and 3B); in the remaining Transmission electron microscopy (TEM) part, granules were mainly arranged in longitudinal rows Specimens for TEM were prepared according to the in the area of the LMC and RMC, and few of them were method modified by Gu et al. (2002). Ciliates were found between two cirri of the same row. It was worth to Animal Cells and Systems 85 Figure 2. SEMs of ventral and dorsal surface of A. indica. Scales are 10 µm. (A) Ventral surface showing granules irregularly dense in the anterior and posterior parts and in longitudinal rows in the remaining parts except the elongated cortical area (arrow). (B) Dorsal surface, showing granules distributed mainly in short linear rows and converged in curved shape at the forefront. AZM, adoral zone of membranelles; CC, caudal cirri; DK , dorsal kineties ; FC, frontal cirri; LMC, left marginal cirri; RMC, right marginal cirri; TC, 1–6 1–6 transverse cirri; UM, undulating membranes; VC, ventral cirri. mention that no granules can be seen in elongated cortical the structure was cyathiform, 1 µm in length and 0.5 µm area between the postoral VC and pretransverse VC in width. Its anterior end was truncated with a clearly visible cavity of about 0.3 µm in diameter, and the (Figure 2A). On the dorsal surface, the number of granules posterior end was tapered (Figure 4D). was quite extensive; they were arranged in short linear rows with 8–10 granules in most areas and were confluent in curved shape at the forefront (Figure 3C). Similar TEM observation pattern of granules arrangement was observed in the two Large number of mature extrusomes in A. indica were dividing cells (Figure 3D). In addition, the granules were arranged in longitudinal rows in their functional area also found at the cortical surface of the encysting cells but under the cell pellicle (Figure 5A). These organelles with reduced number on dorsal area (Figure 3E). were organized as membrane-bounded vesicles, ellipsoid Higher magnification SEM showed that the granules, shaped, about 1 µm in length and 0.5 µm in width as stated above, were extruded structure of extrusomes (Figure 5B). Two parts can be recognized according to its during or after extrusion. The extrusomes were found internal structure: a spherical cavity possibly containing accidentally in broken cells and distributed regularly some structureless substance, occupied about ¼ of the beneath the pellicle with the size of about 1 × 0.5 µm extrusomes volume, while the rest part was filled with (Figure 4A). In general, these organelles discharged different electron dense materials, and the density of the through the pellicle, and their extruded content can keep materials near the center appeared lower than the outer a uniform structure without significant change during area (Figure 5C). The process of ejection was shown in extrusion (Figure 4B and 4C). After being fully extruded, Figure 5D–H. The extrusomes expanded gradually to 86 X. Zhang et al. Figure 3. SEMs of nondividing (A–C), dividing (D), and encysting (E) cells of A. indica. Scales are 5 µm. (A, B) Granules distributed irregularly near the frontal cirri and transverse cirri on the ventral surface. (C) Granules converged in a curved shape at the forefront on the dorsal surface. (D) Granules distributed mainly in longitudinal rows in the area of left and right marginal cirri. (E) The number of granules was reduced on dorsal area of encysting cell (arrow). AZM, adoral zone of membranelles; FC, frontal cirri; LMC, left marginal cirri; RMC, right marginal cirri; TC, transverse cirri; VC, ventral cirri. separate its membrane from internal content and then the represent the initial stage of extrusomes (Figure 6B). membrane fused with the pellicle, and the internal content These small vesicles ranged from 0.15 to 0.35 µm in size broke through the pellicle and ejected out. The morpho- and may eventually attain a diameter as much as about logy of the content did not change during ejection. 0.5 µm (Figure 6C). Only after reaching such a size range, Besides, the mature extrusomes, the cytoplasm of the vesicles start to organize and develop. We arbitrarily A. indica was rich in many organelles such as mitochon- separated these developing vesicles into four stages for dria, endoplasmic reticulum, and different kinds of vesicles sake of clear description: (1) inside the vesicles, filament- (Figure 6A and 6B). The appearance of some irregular ous materials clustered in periphery near the smooth vesicles occurred near endoplasmic reticulum and may membrane (Figure 6C and 6D); (2) the filamentous Animal Cells and Systems 87 Figure 4. SEMs of intracellular extrusomes (A) and extracellular extruded structure of extrusomes (B–D) in A. indica. Scales are 0.5 µm. (A) Extrusomes distributed regularly beneath the pellicle in broken cells. (B, C) Extrusomes were discharged through the pellicle with uniform structure during extrusion. (D) Fully extruded structure of extrusomes appear to be a cyathiform, about 1 × 0.5 µm, the anterior end truncated with a cavity about 0.3 µm in diameter, and posterior end was tapered. materials further increased and formed a noncontinuous these developing extrusomes, the reactive granules mainly layer of high electron-dense materials among them; demonstrated in the peripheral region near the membrane, meanwhile, the vesicles adopted a asymmetric form with especially in its anterior end (Figure 7C). No reactive one end truncated and the other tapered (Figure 6E granules were found in the control samples (Figure 7D and 6F); (3) as the filamentous materials nearly filled the and 7E). whole vesicles except a cavity located at the truncated end, the high electron-dense materials become thickened and evident (Figure 6G and 6H); (4) the high electron- Discussion dense materials were closely packed and occupied more The structure and extrusion mechanism of the percentages of the vesicles except the central part and extrusomes in A. indica finally, the vesicles become mature extrusomes located Gupta et al. (2006) has reported that A. indica possesses beneath the pellicle (Figure 6I and 6J). cortical granules that arrange in short linear rows using protargol staining. Our study, by means of electron microscopy, showed similar characteristics of those gran- G-6-pase cytochemistry observation ules with the description of original report. Furthermore, Electron microscopic enzymo-cytochemistry observation these granules were identified as special extrusive orga- revealed that the cytoplasm of the cell contained nucleus, nelles. Their morphology and extrusion mechanism were mitochondria, endoplasmic reticulum and many different distinctly different from the extrusomes reported in other kinds of vesicles, etc. Endoplasmic reticulum and ciliates. some irregular vesicles with few internal materials were both found and labeled by G-6-Pase reactive granules Morphology (Figure 7A and 7B). Other vesicles contained inhomo- The mature extrusomes of A. indica were mainly char- geneous filamentous materials, i.e., the developing extru- somes were also found commonly in the cytoplasm. In acterized by containing different electron-dense materials 88 X. Zhang et al. Figure 5. TEMs of mature extrusomes (A–C) and their ejection process (D–H) of A. indica. Scales in (A, B) are 0.5 µm, in (C–H) are 0.2 µm. (A) Longitudinal section through the cell cortex, showing the extrusomes arranged in longitudinal rows. (B) Extrusomes were membrane-bounded vesicles and with the size about 1 × 0.5 µm. (C) The extrusome had a structureless cavity, and the remaining part was filled with different electron-dense materials. (D) The membrane of extrusome was separated from internal content and formed an interval (arrow). (E, F) The interval became larger, and the membrane started to fuse with the pellicle (arrows). (G, H) The internal content broke through the pellicle and ejected out. MIT, mitochondria; P, pellicle. and having a structureless cavity. They clearly differ from also distinguish from the toxicysts which are characterized the trichocysts and trichocysts-like extrusomes both of by having a thick external capsule and an internal tube which consisted a body, tip, and cap (Bannister 1972; (Rosati & Modeo 2003; Foissner & Oertel 2009). In their Beisson et al. 1976; Zhang et al. 2011), and from the morphogenetic processes, the filamentous substance in mucocysts that contained a dense crystalline substructure vesicles of A. indica clustered and condensed gradually (Tokuyasu & Scherbaum 1965; Satir et al. 1973). They from outer to center area, while in other types of Animal Cells and Systems 89 Figure 6. TEMs of endoplasmic reticulum (A), small vesicles (B) and development of extrusomes (C, E, G and I are transverse sections; D, F, H and J are longitudinal sections) in Architricha indica. Scales in (A, B) are 0.5 µm, in (C–J) are 0.2 µm. (A) Endoplasmic reticulum was shown in clustered or scattered form. (B) Small vesicles may be the initial stage of extrusomes. (C, D) Beginning of the development of extrusomes characterized by filamentous materials clustering in periphery of vesicles (arrow). (E, F) A noncontinuous layer of high electron dense materials emerged (arrow) and the vesicles adopted a asymmetric form. (G, H) Further growth and development of the vesicles with formation of a distinct cavity. (I, J) The vesicles became mature extrusomes located beneath the pellicle. ER, endoplasmic reticulum; MIT, mitochondria; V, vesicle. extrusomes, the internal substance grew outward from the during discharge, such as trichocysts changing from spindle center and formed solid structure (Yusa 1963, 1965; organelles to elongated needle-like structures (Hausmann & Zhang et al. 2011). Mignot 1975), mucocysts turning into amorphous mate- rials from crystalline contents ( Tokuyasu & Scherbaum 1965; Satir et al. 1973), and toxicysts changing from rod- Extrusion mechanism shaped structures into curved hollow tubes (Wessenberg & During ejection, the entire internal content of extrusomes Antipa 1970; Hausmann & Wohlfarth-Bottermann 1973), in A. indica was ejected out without any morphological and their fully ejected structure were rarely observed on change. After extrusion, the extruded structure appeared to the body surface. be a cyathiform similar to the mature extrusomes, and they With the above comparisons, the extrusomes of remain outside of the cell surface. However, the other A. indica show obvious different features and thus extrusomes may undergo a morphological transformation suggests new type of extrusomes in ciliates. 90 X. Zhang et al. Figure 7. TEMs of G-6-Pase cytochemistry of A. indica. Scales are 0.5 µm. (A) Reactive granules were present on the endoplasmic reticulum and some vesicles (arrows). (B) Higher magnification of endoplasmic reticulum and vesicles with reactive granules. (C) Reactive granules were mainly demonstrated in the peripheral region near the membrane of the developing extrusomes (arrows). (D, E) The absence of reaction granules of vesicles and developing extrusomes in the control section. ER, endoplasmic reticulum; MIT, mitochondria; NU, nucleus; V, vesicle. The localization of the extrusomes in A. indica arrangement of extrusomes on ventral and dorsal surface were different, and the location on ventral surface was The previous studies focused on the lower forms of related to the arrangement of cirri. In contrast with the ciliates and showed that extrusomes were generally lower forms of ciliates mentioned above, highly differ- distributed with a homonomous pattern and occupied a entiated and specialized hypotrichous ciliate represented specific position near the cell pellicle. For example, the by A. indica has apparent dorsal and ventral sides and trichocysts in Paramecium were distributed regularly their cirri differentiate into different functional ciliature alternating with single or paired basal bodies (Allen & such as AZM and undulating membranes, frontal-ventral- Hausmann 1976; Hausmann & Allen 1976). Mucocysts in transverse cirri, left and right marginal cirri, and dorsal Tetrahymena were arranged in longitudinal rows, half of them along the “primary meridians,” and the other bristle. Therefore, although there are no further studies of half along “secondary meridians” (Allen 1967; Satir & other members, we can conclude that the localization of Wissig 1982). However, in A. indica, density and extrusomes might be in some way related to the Animal Cells and Systems 91 differentiation of the dorsoventral cortex and ciliature Acknowledgements occurred in the hypotrichous ciliates. This work was supported by the National Natural Science Foundation of China [No. 31172042] and the Deanship of Scientific Research at King Saud University. Origin and possible function of the extrusomes in References A. indica Allen RD. 1967. 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