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Modification of Lipid Composition in a Dimorphic Fungus, Candida Albicans During the Yeast Cell to Hypha Transformation

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Modification of Lipid Composition in a Dimorphic Fungus, Candida Albicans During the Yeast Cell to Hypha Transformation Jpn. J. Med. Mycol. Vol. 23, 159-165, 1982 ISSN 0583-0516 Modification of Lipid Composition in a Dimorphic Fungus, Candida albicans during the Yeast Cell to Hypha Transformation Koh Yano*, Tomiyasu Yamada, Yoshiko Banno, Takashi Sekiya and Yoshinori Nozawa Department of Biochemistry, Gifu University School of Medicine, Tsukasamachi-40, Gifu 500, Japan [Received for Publication: February 1, 1982] Alterations in phospholipid and fatty acid composition of Candida albicans were examined during the yeast cell to hypha transformation. The major phospholipids separated by thin layer chromatography were phosphatidylcholine, phosphatidyl- ethanolamine, and phosphatidylinositol/phosphatidylserine. Large increments of relative amounts of phosphatidylcholine and phosphatidylethanolamine with a pro- found decrement of phosphatidylinositol/phosphatidylserine were found to occur within 3 to 5 h after the induction of the conversion. There was a great increase in linoleic (18;2) acid in all phospholipids, especially in phosphatidylcholine, with a compensatory decrease in the monounsaturated fatty acids. These alterations were considered to be confluent in the direction of increasing the degree of unsaturation, as ascertained by measuring the unsaturation indices.These alterations in cellular lipid composition were observed to coincide with the rapid elongation of the germ tubes. These results suggest that modification of membrane lipid composition might be asso- ciated with the transformation from yeast cell to hypha in C. albicans. A number of studies on the analysis of fungal available in which modification of cellular lipid lipids have been made with special reference to ac- composition during transformation of dimorphic climation to environmental conditions1-4), in at- fungi was examined together with the morphologi- tempts to shed light upon a relationship between cal changes. In the present study, we studied phos- cellular lipid composition and morphogenesis5, 6). pholipid and fatty acid compositions of a dimor- In 1971, Gordon et al. 5)stated that in Mucor gene- phic fungus, Candida albicans, during the yeast vensis, a dimorphic fungus, its morphology is not cell to hypha conversion as related to the morpho- directly related to lipid composition. On the con- logical change observed with scanning electron trary, Manocha6) recently reported with another microscope, and found that cellular lipid composi- dimorphic fungus Paracoccidioides brasiliensis tion of C. albicans demonstrated profound fluc- that cellular lipid composition of the organism tuations during the morphological transition. may play a role in the dimorphic behaviour, show- MATERIALS AND METHODS ing differential distribution of the major phos- pholipids and fatty acids between the yeast and Organism. C. albicans strain 3125, which was mycelial forms of this fungus. These analyses were supplied by Dr. S. Watanabe, Shiga University of performed on lipids extracted separately from the Medical Science, was used throughout this investi- two forms of these fungi when they reached the gation. The organism was maintained on Sabou- same stage of growth and were in morphologically raud glucose (2%) agar slants by transfer every 2 stable conditions. To our knowledge, no report is weeks at 25C. Culture media. For growth of yeast-form cells, *To whom inquires should be addressed. Sabouraud broth with a slight modification 160 真 菌 誌 第23巻 第2号 昭和57年 (medium A) consisting of 4% glucose, 1 % poly- roform:acetone:methanol:acetic acid:water peptone and 1 % yeast extract was used. For induc- (3:4:1:1:0.5, v/v) in the second direction). After tion of hyphae, a chemically defined medium charring the developed plate with 50 % H2SO4, the (medium B) prepared as described by Tani et al. 7) areas corresponding to individual phospholipids modified by the substitution of L-methionine for were scraped off the plate and their phosphorus casamino acids was employed. This medium con- content was determined by the method of Rouser tained per 100 ml of distilled water: glucose 1. 65 g, et al. 12).For determination of phospholipid acyl L-methionine 100 mg, KH2PO4170 mg, MgSO4 chain composition, the developed plate was 7H2O 13 mg, KC 143 mg, FeC 13. 6H2O 0. 25 mg, sprayed with 8-anilino-l-naphthalenesulfonic acid MnSO4 4H2O 0, 25 mg, Na2HPO4 450 mg and magnesium salt (ANS-Mg), and spots of individual biotin 0, 6, ug. phospholipids were scraped and methylated with Preparation of cells. Stock cultures on Sabou- 1 ml of a 10 % boron trifluoride methanol complex raud glucose agar slants were diluted with medium in sealed ampoules at 100C for 10 min, Quantita- A to 2, 5-3. 0 x 104 per ml. One ml of the suspen- tive analysis of fatty acids was carried out by gas- sion was inoculated into 200 ml each of medium A liquid chromatography (Shimadzu GC-6A type gas in a 500 ml Erlenmeyer flask, and then incubated chromatograph) using a column of 10% diethy- at 37C with gentle shaking in an enclosed hori- leneglycol succinate (DEGS) al 175C. Weight per- zontal shaker for 10 h or to the early stationary centage was calculated by a Shimadzu chromato- phase. pac-EIA integration system. To transform to hyphae, 1. 2-1. 5 x 107 yeast Scanning electron microscope. Washed cells cells in the early stationary phase were transferred were immediately fixed for 1 h with a cold (4C) into 200 ml medium B, and then incubated at solution of 4% glutaraldehyde-2 % osmium tetro- 37C with gentle shaking. Aliquots were taken at xide (1:1) mixture, each solution being prepared selected intervals for morphological observation in 0.1M phosphate buffer (pH 7, 2). The fixed and lipid analysis. Cells were harvested by 5 min samples were subsequently washed in distilled centrifugation at 1, 500 x g and washed free of water and dehydrated in a graded acetone series. media with distilled water. The dehydrated cells immersed in absolute ace- Lipid extraction and analysis. Total lipids tone was quickly transferred to the specimen were extracted from the washed cells according to holder of a Hitachi HCP-1 critical point drying the method of Bligh and Dyer8) with chloro- device, dried using liquid CO2 and examined in a form/methanol (2:1, v/v). In order to obtain a JSM-U3 scanning electron microscope. maximum recovery of extraction, the suspension of washed cells in chloroform/methanol (2:1, v/v) RESULTS was incubated at 37C for 4 h under nitrogen be- Morphological changes during the Y-H, con- fore the chloroform layer was collected. Phospho- version. Morphological transition from the yeast lipid phosphorus content was determined by using cell to hypha was observed with the scanning elec- the method of Bartletts) with the modification of tron microscope and its process is displayed in Fig. decomposition in 70% perchloric acid as described 1, Fig. lA is a picture of typical yeast form cells in by Marinettila). Phospholipid composition was the early stationary phase. The yeast to hypha con- examined by two dimensional thin layer chro- version (Y-H conversion) was observed soon-after matography on 20x20 cm plates made of Silica yeast cells were transferred into medium B. First, a Gel H using the following solvent system; chloro- small projection emerged at one site of each form:methanol:7 N ammonium hydroxide solu- spherical yeast cell and then within 1 to 2 h a short tion (90:54:11, v/v) in the first direction and chlo- germ tube developed as an extention of the small roform :methanol :acetic acid:water (90:40:12:2, projection (Fig. 1B). Yeast cells were no longer ob- v/v) in the second direction. For better separation served at this time, indicating that they were of phosphatidylinositol from phosphatidylserine, almost synchronously transformed to hyphal cells. 2. 5% magnesium acetate impregnated Silica Gel The morphological transition was completed H plate (20 x 20 cm) was developed with chloro- within 4 to 5 h after the transfer, and the cells be- form:methanol:l3 N ammonium hydroxide solu- came the typical hyphae in appearance (Fig. 1C). tion (65:35:5. 5, v/v) in the first direction and chlo- With further incubation, the filamentous cells ap- Jpn. J. Med. Mycol. Vol. 23 (No. 2), 1982 161 Fig. 1. Scanning electron microscopic observations of Candida albicans. (A) Typical yeast form cells in the early stationary phase. Pictures of C. albicans taken at 1. 5 h (B), 4. 5 h (C), and 12 h (D) after the early stationary phase yeast cells were transferred into medium B illustrate the representative stages of the morphological transition from the yeast cell to hypha. Each bar indicates 10, um. peared to conglomerate with each other as shown thentic standards. Major phospholipid compo- in Fig. ID. nents of yeast cells were phosphatidylcholine (PC, Alteration in phospholipid content during the 28%), phosphatidylethanolamine (PE, 15%), and Y-H conversion. During the process of conver- a fraction (PI/PS, 33%) of phosphatidylinositol sion, as germ tubes developed and elongated, the (PI) plus phosphatidylserine (PS). Attempts were culture dry weight increased progressively (Fig. 2). made to separate PI from PS and it was found that In contrast, the phospholipid content decreased in the former comprised approximately 70% of the a reciprocal manner. This may be in part due to total of these two phospholipids. Phosphatidic acid an increment in weight of cell walls primarily com- and cardiolipin were minor constituents. posed of glycoproteins such as glucomannan-pro Fig. 3 illustrates changes in the percentage com- n teinn and glucan-protein 13). position of major phospholipids during the Y- H Alterations in phospholipid polar head group conversion. The levels of both PC and PE in- composition. Individual phospholipids separated creased by approximately 10% within 3 to 5 h on thin layer chromatographic plates were identi- after the transfer while that of PI/PS declined fied by comparing their Rf values with those of au- from 33% to 7% in a reciprocal fashion.
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