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Ultrastructure of the Malpighian Tubules with Enlarged Segments in the Alkali Fly Larva Ephydra Hians Say from Mono Lake, Califo

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Ultrastructure of the Malpighian Tubules with Enlarged Segments in the Alkali Fly Larva Ephydra Hians Say from Mono Lake, Califo THE WASMANN JOURNAL OF BIOLOGY 47(1-2), 1989, pp. 1ll-126 ULTRASTR UCTURE OF THE MALPIGHIAN TUBULES WITH ENLARGED SEGMENTS IN THE ALKALI FLY LARVA E PHYDRA HIANS SAY FROM MONO LAKE, CALIFORNIA Helen Yu, Eduardo A. C. Almeida a nd PaulK. Chien Abstract.-The fourth inst ar larvae of the Mono Lake alkali fl y Ephydra hians has two pairs of dissimilar Malpighian tubules (MT). The one studied here has enlarged segments that contain spherical mineral concretions. The MTs extends from between the mid and hind gut through a common ureter, which branches into two proximal segments. The ureter and proximal seg­ ment (about 90 ,urn in diameter) cells are ultrastructurally similar. Both conta in an elaborate basal labyrinth, intracellular electron dense vesicles, numerous m itochondria, glycogen granules, rough endoplasmic reticulum (RER) and a brush border wi th microvilli penetrated by mitochondria. The enlarged segm ent, about 350 .urn in diameter, is continuous with the proximal segment. The celJs of the enlarged segment are flattened, contain mitochon­ dria, RER, an ela borate basal labyrinth, and numerous m icrovilli. The lumen of the enlarged segment contains large quantities of concretions. This seg­ ment graduall y decreases in diameter to become the transition segment, wh ich bends and becomes the long main segment (about 90 ,urn in diameter). The terminal blind end of the main segment attaches to the rectum. The ultrastructure of the transition segment is intermediate between the main and enlarged segments. The celJs in the main segment exhibit welJ developed basal labyrinth, numerous mitochondria, and electron dense mineral de­ posits within vesicles between 0.3 and 0.5 .urn in diameter. In addition, RER and microvilli containing mitochondria are present. No accessory cells were fo und in MT from the fourth instar larvae. Introduction The larva of the alkali fly Ephydra hians is the major benthic metazoan found in Mono Lake, California. Mono Lake water is characterized by high osmolarity (1,900 mOsm) and extreme alkalinity (pH 10.5) due to its high carbonate a nd bicar bonate content. The osmotic concentration of the he­ molymph of the larvae (determined by the vapor pressure method) is 430 mOsm, and its pH is about 7.2 (Yu eta/., 1988). The fl y larvae that inhabit the lake must possess mechanisms to regulate both their hemolymph con­ centration and pH. Malpighian tubules in insects are believed to be the major organ in hemolymph osmoregulation. In E . hians, one of the two pairs of Malpighian tubules produce and store numerous spherical mineral concretions that are mostly composed of calcium carbonate (Yu eta/., 1988). 112 THE WASMANN JOURNAL OF BIOLOGY The general morphology and ultrastructure ofMalpighian tubules in other dipterans that produce mineral concretions, such as Drosophila melanogas­ ter, Drosophila hydei and Ephydra riparia, have been described by Wessing and Eichelberg (1975), in D. hydei by Revert (1975), and Wolburg et al. (1973), and in the brackish water mosquito Culiseta inornata by Garrett and Bradley ( 1984). The major morphological and ultrastructuraJ features of the Ma1pighian tubules of these dipterans are similar to those observed in E. hians. However, some differences exist. Drosophila spp., and E. riparia have distal en larged segments and proximal main segments (Eichel berg and Wess­ ing, 1975). This arrangement is reversed in E. hians. The proximal segments of the Malpighian tubules in E. hians are enlarged while the distal main segments are long and narrow (Yu et a/., 1988). The Malpighian tubules of the blowfly Calliphora erythrocephala (Berridge and Oschman, 1969) show many similarities to those of E. riparia. Accessory cells in the Malpighian tubules main segments have been found in both species (Eicbelberg and Wessing, 1975). The species that shows the most similarities at the gross morphological and ultrastructural level to E . hians is E. riparia, as described by Eichel berg ( 1979). However, because E. riparia is a eurybaune dipteran inhabiting coastal salt water marshes (Sutcliffe, 1960) as opposed to the alkaline environment which this E. hians inhabits, the specific adaptation of the Malpigbian tubules of E. hians may be quite different from E. riparia. This work describes the morphology and ultrastructure of the Malpighian tubules with enlarged segments in the alkau fly E. hians collected in Mono Lake, California. Materials and Methods Larvae of the alkali fly Ephydra hians were coUected from Mono Lake shores and kept at room temperature (Yu et a/., 1988). The fourth instar larvae, I 0 mm or greater in length were used in this study. For transmission electron microscopy (TEM), Malpighian tubules were dissected and fixed at room temperature for I hr in 5% glutaraldehyde (GA) in 360 mM cacodylate buffer, pH 7.5. The tissue was postfixed in I% osmium tetroxide. Samples were dehydrated in an acetone series and embedded in low viscosity epoxy resin (Spurr, 1969). Sections were obtained with a diamond knife, stained with uranyl nitrate and lead citrate (Reynolds, 1963) and photographed using a Zeiss EM-9S2 electron microscope. For freeze-fracture, Malpighian tubules were dissected in 25% glycerol in 360 mM cacodylate buffer at pH 7.5 and immediately frozen in liquid freon cooled by liquid nitrogen at - 170°C. The specimens were fractured at - l00°C and etched for 3 minutes in a Balzers freeze fracture apparatus. Platinum replicas were carbon stabilized, cleaned with 4% sodium hypochloride followed by I N HCI and supported on form­ var coated copper grids. VOLUME 4 7, NUMBERS I AND 2 113 MALPIGHIAN TUBULES WITH ENLARGED SEGMENTS ANTERIOR END : DORSAL SURFACE .. POSTERIOR END SEGMENT 2mm VENTRAL SURFACE Figure I. Diagrammatic representation of the pair of Malpighian tubules with enlarged segments. Results The Malpighian tubules of the fourth instar larvae of E. hians are about 13 mm in length. The Malpighian tubules of a I 0 mm larva have a ureter and proximal segment which makes up about 10% of the total length. The enlarged segment of the tubule comprises about 20% of the total length, while the transition segment represents about 20% and the main segment 50%. The pair of Malpighian tubules with enlarged segments (Fig. 1) branches from the ureter at the junction between the midgut and hindgut. The ureter (about 90 ,urn in diameter) splits into two short proximal segments which increase in diameter and become the enlarged segments. The enlarged seg­ ments, 350 ,urn in diameter, extend ventrally and toward the anterior. The enlarged segments decrease in diameter gradually to form the transition segment (180 ,urn in diameter). The transition segment bends posteriorly at the region marked by the presence of surrounding yellow fat bodies. The main segment measures about 90 ,urn in diameter and continues from the transition segment toward the posterior end of the gut, where its blind end attaches to the wall of the rectum. Small concretion cores (about 0.3 ,urn) containing mostly calcium and phosphorus with some magnesium (Yu et a/., 1988) are produced in and secreted from the cells throughout the length of the main segment. Concretions with a diameter up to 21 ,urn were found in the lumina ofthe main segment, transition segment, and enlarged segment. The concretions can be eventually discharged into the gut, a process con­ trolled by the musculature around the proximal segments and ureter. Freeze-fracture of cells from the main segment (Fig. 2) shows a brush border with two types of microvilli. One is penetrated by long, slender 114 THE W ASMANN JOURNAL OF BIOLOGY Figure 2. Freeze-fracture electron micrograph of a Malpighian tubule main segment in cross section. C, concretions; BL, basal lamina; M, mi tochondria; MI, mitochondrion within mi­ crovillus; MV, microvilli. VOLUME 47 , NUMBERS I AND 2 115 mitochondria measuring 0.2 JLm to 0.3 JLm in diameter, while the other type of microvilli are about 0.15 JLm and do not contain mitochondria. In the cytoplasm, numerous spherical vesicles containing mineral concretions can be observed. The size of the vesicles varies from 0.1 JLID to about 4 JLm, most of them range between 0.3 and 0.5 JLm. Many mitochondria are also present in the cytoplasm. Mineral concretions are also found between the basal folds in the basal lumen. Transmission electron micrographs from cells of the main segment show intracellular electron dense mineral deposits (Figs. 3 and 4). The brush border is similar to that observed in the freeze fracture preparation, with the two types of microvilli. However, the basal folds appear enlarged and lack the mineral concretions seen in freeze-fracture replicas. The basal lamina can be clearly distinguished in these transmission electron micrographs. Higher magnification of the cytoplasm reveals well-developed endoplasmic retic­ ulum in addition to numerous mitochondria and concretions (Fig. 4). The basic ultrastructure of the transition segment cells (Fig. 5) is very similar to that of the main segment (Figs. 2-4) cells. However, there are considerably less vesicle bound electron dense deposits. The brush border in the transition segment also shows two types of microvilli, one with mi­ tochondria another without (Fig. 6). Concretions can be seen nested in the brush border (Fig. 6). In this segment, the diameter of the Malpighian tubule increases relative to the main segment while the cells become thinner (Fig. 7). The Malpighian tubule attains maximum diameter in the enlarged segment (Fig. 1), while the cell thickness is at a minimum (Figs. 8 and 9). The cytoplasm (Fig. 8) has numerous mitochondria. Other organelles such as rough endoplasmic reticulum and golgi apparatus are also present but are less prominent than in the cells of the main segment. The majority of the microvilli in the brush border do not contain mitochondria. Luminal con­ cretions of varying sizes can also be seen nested among the microvilli (Fig.
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