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Fine structural aspects on the web glue production in the golden orb-web spider Trichonephila clavata Fine structural aspects on the web glue production in the golden orb-web spider Trichonephila...
Sun, Yan; Lee, Seung-Min; Ku, Bon-Jin; Moon, Myung-Jin
2023-12-11 00:00:00
ANIMAL CELLS AND SYSTEMS 2023, VOL. 27, NO. 1, 10–18 https://doi.org/10.1080/19768354.2023.2168753 Fine structural aspects on the web glue production in the golden orb-web spider Trichonephila clavata Yan Sun, Seung-Min Lee, Bon-Jin Ku and Myung-Jin Moon Department of Biological Sciences, Dankook University, Cheonan, Korea ABSTRACT ARTICLE HISTORY Received 25 October 2022 The water-soluble glue substance of the capture threads in Trichonephila clavata is solely produced Revised 31 December 2022 from two pairs of aggregate silk glands. During the web glue production, secretory vesicles were Accepted 8 January 2023 synthesized via the extensive rough endoplasmic reticulum of epithelial cells. Unlike the clearly described fibrous web production in spiders, the process of aqueous web glue production KEYWORDS appears to involve either a condensing or a packaging step by the Golgi complex. In particular, Spider; silk; fine structure; the fine structure of secretory vesicles varies from cell to cell and may represent the secretory web glue; Trichonephila cycle. The electron-dense multivesicular bodies were clearly visible as discrete droplets, and the clavata mature secretory product in the glandular epithelium appeared as a spherical vacuole grown by fusion with surrounding small vesicles. Our fine structural observation reveals that the secretion occurs when the release of secreted material involves the loss of part of the cytoplasm. The bleb along the luminal surface of the secretory cells and membrane-bound extracellular vesicles which pinched off from the cell suggests that the secretory product is released by the mechanism of apocrine secretion. Introduction of this aqueous gluey substances, the concentration of The viscous prey capture threads of the web-building related water-soluble organic compounds such as free spiders are produced from the substances of the aggre- amino acids, small peptides, and neurotransmitters gate silk gland (ASG) and flagelliform silk gland (FSG) was relatively high, while the concentrations of various (Peters and Kovoor 1991; Moon and Kim 2005). Previous inorganic salts and glycoproteins were relatively low research has shown that the capture thread of an orb- (Vollrath and Tillinghast 1991; Townley et al. 2006; web spider comprises only one type of silk fiber which Römer and Scheibel 2008). is originated from the FSG of spiders (Römer and Schei- Since the gluey substances in orb-web spiders are bel 2008). In addition, it has been widely known that reported as one of the strongest biological glue (Vollrath spider’s web glue is basically a viscous solution pro- et al. 1990; Tillinghast et al. 1993), spider web glues that duced from the ASGs and coats the spiral threads of coat the sticky spirals of the capture threads have spider web for prey capture (Choresh et al. 2009). attracted researchers to analyze their unique biochemi- Subsequent studies have confirmed that the main cal characteristics and industrial potential to create component of the glue contained within microscopic new biomaterials (Choresh et al. 2009). This biological nodules is made of a glycoprotein (Vollrath and Tillin- material that provides adhesion and thread viscosity is ghast 1991; Tillinghast et al. 1993). The supporting originated from regularly spaced droplets, whose size fibers of sticky capture threads are wrapped with a and spacing are determined by the diameters of the complex aqueous solution that integrate into droplets axial fibers, amount of depositions, and viscosity of the that obtain their adhesiveness from glycoprotein aqueous solution (Vollrath and Tillinghast 1991; Opell within nodules (Vollrath et al. 1990; Townley et al. and Hendricks 2010). 1991; Vollrath 1992). Hawthorn and Opell (2003) also In addition, the granular size of the glycoprotein pro- suggested that the content of this solution could duced from the ASG can affect not only the droplet size create hygroscopic forces, which could contribute to (Vollrath and Tillinghast 1991), but also the hydrophilic the stickiness of threads. As a result of chemical analysis compounds and atmospheric moisture that prevent CONTACT Myung-Jin Moon moonmj@dankook.ac.kr Department of Biological Sciences, Dankook University, Cheonan 31116, Korea © 2023 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. ANIMAL CELLS AND SYSTEMS 11 the droplets from drying out (Townley et al. 1991). With Ultrathin sections for TEM imaging were prepared the exception of some brief studies (Moon and Kim 2005; using a diamond knife (Ultra 45° Diatome, Hartfield, Park and Moon 2014; Moon 2018), fine structural visual- PA, USA). The specimens were stained with alcoholic ization of the ASG has been nearly ignored. So far, infor- uranyl acetate and lead citrate. The sections were then mation on the cellular process of web glue production in examined precisely with a transmission electron micro- the spider has been limited. Therefore, we describe here scope supplied by JEOL (JEM 100 CX-II, JEOL Ltd., the fine structural frameworks of the ASG cells that con- Tokyo, Japan) at an accelerating voltage of 80 kV. tribute to the production of massive amount of gluey materials in the spider, Trichonephila clavata with aid Results of high-resolution transmission electron microscope for biological sciences (Bio-TEM). The ASG of T. clavata is basically a sac. The opening of the gland is connected to an excretory duct leading to the spigot of the posterior spinneret. The secretory sac of the ASG is widely extended across the bordering Materials and methods area of the other opisthosomal tissues (Figure 1(A,B)). The golden orb-web spider, Trichonephila clavata Plastic-embedded sections stained with toluidine blue (Araneae: Nephilidae), were collected in a local area clearly show their convoluted morphology and histo- near the cheonan campus of Dankook University, logic organization. Histologically, the secretory sac is Cheonan, Korea. Trichonephila is a genus of orb-weaver consisted of inner epithelial cells and outer connective spiders belongs to the Araneidae family as a subgenus cells, and they are surrounded by a thin basal lamina of Nephila. Since Trichonephila was elevated to the (Figure 1(C,D)). In transverse section, the ASGs are con- level of genus in 2019 by Kuntner et al., this species sisted of a multi-lobed secretory region surrounded by was moved from the genus Nephila to Trichonephila. a single layer of the cuboidal epithelium and a widely All spiders were reared in an ambient environment dilated lumen that stores the secretory products. The with natural light in wooden frame enclosures (height × nucleus of epithelial cell is spherical in shape and it length × width = 50 × 50 × 10 cm) with front and back occupies about half of the volume of the cell (Figure 1 glass windows, and fed insect larvae and water. (E,F)). For transmission electron microscopic examination, Since the secretory cells of ASG are filled with cister- adult spiders were anesthetized with carbon dioxide nae of rough endoplasmic reticulum (rER), the limiting and dissected under a stereoscopic microscope with aid membranes between adjacent cells cannot be easily dis- of spider Ringer’s solution that contains 160 mM NaCl, tinguished. The plasma membrane at the base of cells is 7.5 mM KCl, 20 mM glucose, 4 mM CaCl ,4mM generally digitated. Deep and complex infoldings are NaHCO ,1mM MgCl , pH 7.4 (Moon and Tillinghast usually found near junctions between adjacent cells 3 2 2020). After dissection, specimens were prefixed using a (Figure 2(A)). The central part of the cell is occupied by 2% paraformaldehyde and 2.5% glutaraldehyde mixture a large nucleus, mitochondria, Golgi complexes, and solution buffered with 0.1 M phosphate buffer at pH large amounts of rER. The rER is uniformly distributed 7.4. The specimens were then postfixed with 1% OsO throughout the cytoplasm but is missing in areas near in the same buffer and rinsed repeatedly with 0.1 M phos- the apical and basal borders. The Golgi complex is also phate buffer (Sun et al. 2020). Following fixation, dehy- sparsely scattered near the apical cytoplasm of the dration procedure was performed in ascending series of cells (Figure 2(B)). ethanol concentrations and embedded in Poly/Bed 812- The cytoplasm below the apical surface is filled with a Araldite Embedding Media (Polysciences Inc., Warrington, variety sizes of secretory droplets ranging from 1.0 to PA, USA) via propylene oxide as an intermediary for 3.5 µm in diameter. These droplets gradually migrate infiltration (Kim and Moon 2018). into the apical cytoplasm and are finally extruded Semi-thin sections with the thickness of 0.5–1.0 µm towards the lumen of the ASG. Each droplet contains a for light microscopic observation were acquired with a low electron opacity material with a multivesicular LKB Ultratome V (LKB, Stockholm, Sweden), then cover appearance (Figure 2(C)). There are numerous microvilli sections with 1% toluidine blue staining solution and that protrude into the lumen of the gland along the heat on a hot plate at 60°C. Images were captured digi- apical border of the cell. The finger-like projections of tally on a Zeiss Axiophot microscope (Carl Zeiss, Jena, the microvilli are bounded by the continuation of cell Germany) using a Motic digital camera (Motic Instru- membranes. Secretory droplets are frequently found ments Inc., Richmond, BC, Canada) with on-chip migrating into the gland lumen across the apical integration. border of the cell (Figure 2(D)). 12 Y. SUN ET AL. Figure 1. Photo micrographs of the ASG in T. clavata. (A, B) The secretory sac of the aggregate gland is widely extended and the glandular epithelium (Ep) of the aggregate gland is basically composed of a single layer of cuboidal cells. Lu: lumen. (C, D) In trans- verse section, the glands show a wide lumen filled with secretions. The secretory sac is basically consisted of inner epithelial cells and outer connective cells. (E, F) The nuclei of the epithelial cells (arrows) are spherical and occupy more than half the width. Ct: connec- tive cell. Scale bars indicate 250 μm(A–C), 100 μm (D), and 20 μm (E, F), respectively. Because the glandular epithelial cells of the ASG rER cisternae accumulate in abundance from basal to actively synthesize and release specific gluey substances apex of the cells, it can be assumed that the major com- to the capture thread, each individual cell has an active ponent of the gluey substance contained in the cyto- cytoplasm accompanied by a spherical nucleus with plasm of ASG is derived from the rER of glandular condensed chromatin and a distinct contrasted nucleo- epithelial cells (Figure 3(E,F)). lus (Figure 3(A)). In particular, the entire remaining Compared to the early stage of cells, the epithelium at space in the cytoplasm is mostly occupied by the the later stages of extrusion exhibits thin columnar cells extended rER. Numerous secretory vesicles containing with indistinct cell membranes. There cells contain mul- high electron density presumably precursors of gluey tiple droplets of secretion, resulting in a much thinner substances can be seen in the apical cytoplasm of this staining of the area (Figure 3(G)). These secretory dro- epithelium (Figure 3(B)). plets migrate towards the apical border and are finally Our TEM results clearly show that extensive rER syn- released towards luminal cavity as a pinch-off portion thesize numerous secretory vesicles in the cytoplasm of the cell during the active process of web glue pro- and subsequent vesicular fusion of multiple vesicles duction. The plasma membrane on the apical pole of can create intensive production of secretory vacuoles the cell is transformed into small finger-like projections (Figure 3(C,D)). One of the prominent features of the of microvilli, and the final secretion of the cytoplasm is cell nucleus at this stage is electron-lucent chromatin anchored to the apical membrane of the microvilli and an enlarged nucleolus. Additionally, exocytotic (Figure 3(H)). release of individual droplets can be seen in this stage The main secretory products of the ASG can be of glandular epithelial cells. Since regularly oriented observed as large and round vacuoles approximately ANIMAL CELLS AND SYSTEMS 13 obvious that the cell involves budding of the apical surface and loses some part of its cytoplasm during this secretion process. Finally, part of the apical cyto- plasm of the secretory cells is released with secretion and then enters the lumen (Figure 4(C,D)). In addition, another type of silk precursor is also observed in the cytoplasm of ASG, where these secretory products are found to accumulate in the luminal cytoplasm of gland- ular epithelial cells in the form of electron-lucent spheri- cal granules. Apparently, the electron density of such granules is much lighter than that of the vacuoles con- taining multivesicular bodies (Figure 4(E,F)). The release pathway of the gluey substance across the cell is perceived from the fine structural modifi- cations of the secreted material. It has been observed that disorganization of the secretion finally occurs when the secretory product is extruded from the cell by a specific secretory process. It is observed that the apices of cells are surrounded by numerous microvilli with short and irregular shapes. With gradual maturation of secretory silk products, multivesicular bodies are progressively converted to more transparent secretory vesicles filled with fine fibrillar substructure. Thus, mature vesicles are much Figure 2. Transmission electron micrographs of the aggregate more electron-lucent than earlier stage vesicles (Figure gland in T. clavata. (A) Secretory cells at the basal portion are filled with abundant cisternae of rough endoplasmic reticulum 5(A,B)). (Er) and their membrane is generally digitated. Golgi appara- The total amount of fine fibrous substances gradually tuses (Go) appeared in the cytoplasm near the nucleus (Nu). increases while the gluey silk is actively released. Fre- (B) The cell at the middle portion is also occupied by a large quently, these vesicles appear to accumulate with amount of rER, mitochondria (Mt) and secretory granules (Sg) others to form amorphous deposits with high electron with multivesicular appearance. (C) Secretory droplets at densities (Figure 5(C,D)). These fine granular substances apical pole are moved towards the apical border of the cell. Each droplet contains a material of low electron opacity with likely migrated across the apical membrane by exocyto- a multivesicular appearance. (D) Along the apical border of tic activity, and can be added to the final secretory the cell, secretory granules and numerous microvilli (Mv) are product as another precursor for gluey substances projecting into the lumen. (Figure 5(E,F)). Our fine structural observation clearly shows the less than 2 µm in diameter. Some of these vacuoles secretory process of the glandular epithelum involves exhibit multivesicular properties. They contain multiple the loss of part of the cytoplasm during the web glue inner vesicles enclosed within a single outer membrane. production. Moreover, the secretory products accumu- Their electron density is relatively high and they remain lated in the secretory vesicles and bleb on the apical close to each other without fusion with others (Figure 4 cytoplasm of the cells which pinched off from the cell (A)). The structural analysis of secretory products can suggest that the web glue material of the aggregate represent the secretion process because it shows some gland is released from the glandular epithelium by the extent of morphologically pattern following the cell mechanism of apocrine secretion (Figure 6). cycle. Therefore, our current TEM investigations reveal the fine structural changes in the secretory material Discussion from the initial secretory vesicles to mature secretory vacuoles during web glue production in ASG (Figure 4 Although it is thought that the silk glands of invert- (B)). ebrates produce only physically fibrous silk, in fact It was first observed through this research that liquid silk material is also produced in web-building secretory substances produced from the ASG of spider spiders (Foelix 2010). However, a very limited part of located in the apical cytoplasm are released extracellular the liquid silk has been investigated to date to under- space by the mechanism of apocrine secretion. It is stand the effect of the adhesive droplets of capture 14 Y. SUN ET AL. Figure 3. Transmission electron micrographs of the aggregate gland in T. clavata. (A) Each epithelial cell shows a large nucleus (Nu) with fine granular chromatin and a prominent nucleolus. Ct: connective cell. (B) An extensive rER (Er) and numerous secretory granules (Sg) with electron-dense multivesicular bodies are observed in the cytoplasm. (C, D) Well-oriented rER cisternae are scattered from base to apex of the cells, particularly near the nucleus. (E, F) Secretory granules are clearly visible with appearance of multivesicular vesicles in the cytoplasm. (G, H) The luminal surface are modified into numerous microvilli (Mv) and the final electron-dense granules are attached to the microvilli. Scale bars indicate 5 μm (A, C–H) and 2 μm (B). threads in ecribellate spider. As far as the capture thread microscopic nodules, and this glue substance coats the is concerned, studies have been largely examined to prey-capturing threads of orb-web spiders (Park and stickness and extensibility of glue substance (Opell Moon 2014; Moon 2018). 2002), and the humidity effect of the sticky droplets Chemical analysis of the sticky and regularly spaced (Opell and Hendricks 2010; Opell et al. 2011). droplets of the capture threads has demonstrated that Considered one of most effective biological glues, ASG produces complex aqueous solution of organic spider silk glue is an aqueous solution produced by and inorganic compounds composed of various types the ASGs of orb weaving spiders (Moon and Kim 2005; of small proteins (Vollrath et al. 1990; Vollrath and Tillin- Choresh et al. 2009). Previous studies have reported ghast 1991) and high molecular weight glycoproteins that the glue of ecribellate spiders is composed of (Tillinghast 1981; Townley et al. 1991). ANIMAL CELLS AND SYSTEMS 15 Figure 4. Transmission electron micrographs of the secretory products of the aggregate gland in T. clavata. (A, B) The mature secretory granules (Sg) contain electron-dense multivesicular bodies. Er: rER, Mt: mitochondria. (C) A part of apical cytoplasm of the epithelial cell is pinched off and enters the lumen (black circle). (D) The secretory products are compactly aggregated as a single vacuole. (E, F) Another type of secretory silk products are accumulate in the luminal cytoplasm as a form of electron-lucent spherical granules (white arrows). Scale bars indicate 2 μm (C, D), 1 μm (A, B, E), and 0.5 μm (F), respectively. Tillinghast et al. (1993) purified a glycoprotein from glue production, small vesicles are formed by the rER Argiope aurantia and found a poly disperse linear macro- and these vesicles are packaged into secretory vacu- molecule that exhibits structural flexibility. Additionally, oles and travel through the Golgi complex before the glycoprotein shares some morphological features releasing secretory substances into lumen. These with mammalian secretory mucins as we also observed excessive contents of rER showed morphological in our electron microscopic examination. This is consist- signs suggestive of active synthesis of substances ent with other reports analyzing spider web glue pro- within cytoplasm (Nagashima et al. 1991)and mass teins (Vollrath et al. 1990). Proteins such as mucin are release of secretions through the luminal space known to have adhesive properties due to their highly (Locke and Huie 1976). glycosylated nature, and their elasticity is known to It is generally known that secretory granules are affect the formation of extended nodules (Choresh produced from ribosomes attached to the limiting et al. 2009). membranes of the rER in the exocrine cells (Siekevitz In T. clavata, each ASG showed a multi-lobed and Palade 1960). They are then transported across secretory region surrounded by a simple layer of the this membrane, segregated within the cisternae of cuboidal cells with large nucleus. These cells are pre- the rER (Redman et al. 1966), and move to small per- liminary filled with abundant cisternae of rER, but ipheral vesicles of the Golgi complex (Jamieson and the Golgi complex also appeared near the apical Palade 1967). They are then concentrated in con- surface of the cytoplasm. The highly developed rER densed vacuoles in the Golgi complex and finally occupies the whole area of the cytoplasm in the epi- formed as individual secretory granules (Caro and thelial cells of the ASGs. During the process of web Palade 1964). 16 Y. SUN ET AL. Figure 5. Transmission electron micrographs of the aggregate gland in T. clavata. (A, B) When the secretory products are extruded from the cells, the multivesicular vesicles are transformed into secretory vesicles filled with a fine fibrillar substructure. The apices of the glandular cells are fringed with short and irregular microvilli (Mv). (C, D) During the active release of secretory silk products, amor- phous electron-dense deposits appear to aggregate with several others. (E, F) The fine granular material is added to the luminal secretory products for the gluey substances. Scale bars indicate 1 μm(A–D) and 2 μm (E, F). In particular, previous researches have clearly shown be responsible for modifying and packaging steps of that the precursors of dragline silk are produced in a cell secretion. form of ready-to-secretion and do not undergo further However, the process of aqueous web glue pro- concentration process (Bell and Peakall 1969). It has duction in ASGs is different from the fibrous silk pro- been also reported that the secretory cells of spider duction in spiders. Our present study clearly showed silk glands may have developed a unique method to that the Golgi complex is also found near the apical more quickly produce large amount of protein by evol- surface of cytoplasm, and it is therefore likely that the ution (Moon et al. 1998). The secretory precursors of Golgi complex also plays an important role in the the major ampullate glands in the eccribellar spiders secretory process of web glue production. including Nephila (Moon and Kim 2005), Argiope (Moon Recently, the secretory function of the Golgi complex and Kim 2005), and Araneus (Moon and Tillinghast appears to be well-established experimentally. There- 2020) species showed exactly the similar characteristic fore, the Golgi complex is known to play a central role of secretion. In addition, Sasaki et al. (1981) studied mor- in protein synthesis controlling cargo-sorting and phological and biochemical traits of the glandular epi- trafficking. This is because these processes are function- thelial cells of the silk gland in the silk moth Bombyx ally important for cell polarity, motility, division, and mori. They reported that the secretory silk materials growth (Park et al. 2021). This is consistent with our were produced as small vesicles through the well-devel- fine structural observations of ASGs in T. clavata, but oped rER. In addition, they found that these secretory their contribution to web glue production seems to be cells lack the Golgi complex, a cell organelle known to very limited because the Golgi cisternae remain ANIMAL CELLS AND SYSTEMS 17 process is accompanied by the release of large frag- ments of cellular contents and loss of certain part of the cytoplasm. In particular, the small apical protrusions seen in the cytoplasm suggest that the secretory materials are finally released by the mechanism of apoc- rine secretion (Kurosumi and Kawabata 1976). Following the observations in Araneus sericatus (Bell and Peakall 1969), Candelas and Lopez (1983) reported their observations on the apocrine secretion in the process of spider silk production. In addition, Farkaš et al. (2014) also reported the apocrine secretion in Dro- sophila salivary glands, recently. It has been known that such apocrine secretion is more damaging than mero- crine secretion (Schneider and Paus 2010) but provides the en masse delivery of a protein mixture from polar- ized epithelial tissues (Farkaš et al. 2014). Comparisons of the results of this research with other studies on fibrous silk production, strengthen the premise that the aqueous web glue (liquid silk) pro- duction process is different from the fibrous silk pro- duction of spiders. Evolutionally, the orb-web spiders Figure 6. Schematic diagram of the apocrine secretion during produce a remarkable variety of webs (Hormiga and the web glue production in the aggregate gland of the orb- Griswold 2014) and contents of the ASG are known to web spider, T. clavata. The sequence of the process leading to have evolved later than other spider silk proteins as secretion occurs from A to C. well as other silk glands (Choresh et al. 2009). In addition, it has been previously noted that large multi-lobed ASGs unreactive and the condensed vacuoles in the trans may have been produced by the coalescence of multiple Golgi region lack dense cores. small silk glands (Kovoor 1987; Moon and Kim 2005). The apocrine secretion is an alternative extrusion These suggest that the secretory process within the mechanism of membrane-associated proteins (Aumüller ACG is more complex compared to the relatively et al. 1999) when secretory granules accumulate in the simple but more massive fibrous silk production. cytoplasm of a cell, a part of the cytoplasm surrounds and pinches off the granules (Farkaš et al. 2014). Although Acknowledgements exocytosis is commonly regarded as a basic type of secretion, the apocrine secretory mechanism has not In memory of Dr. Edward K. Tillinghast (1932–2021) at the Department of Biological Sciences of the University of New been properly described because the pathways that Hampshire, Durham, NH, USA. control the secretory process remain obscure (Gesase and Satoh 2003). The apocrine glands are found primarily in the mammary milk glands of breast and apocrine Disclosure statement sweat glands. Secretion from apocrine glands contains No potential conflict of interest was reported by the author(s). are made up of proteins and fatty acids, therefore they are viscid and odorous (Spielman et al. 1998). The ASG preparation in T. clavata, secretory products Funding are finally extruded into the gland lumen across the The present research was supported by the research fund of apical border of the cell after packaging steps of cell Dankook University in 2020. secretion. It is obvious that the cell involves the budding of apical surface and loses some of its cyto- plasm in this process of secretion. 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