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A New Pleomorphic Ascomycete, Calyptrozyma Arxii Gen. Et Sp. Nov., Isolated from the Human Lower Oesophagus

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A New Pleomorphic Ascomycete, Calyptrozyma Arxii Gen. Et Sp. Nov., Isolated from the Human Lower Oesophagus Mycol. Res. 99 (ID): 1239-1246 (1995) Printed in Great Britain 1239 A new pleomorphic ascomycete, Calyptrozyma arxii gen. et sp. nov., isolated from the human lower oesophagus TEUN BOEKHOUT!, HENRI ROElJMANS' AND FRANS SPAAy3 1 Centraalbureau voor Schimmelcultures, Yeast Division, ]ulianalaan 67, 2628 BC Delft, The Netherlands 2 Centraalbureau voor Schimmelcultures, P.o. Box 273, 3740 AG Baarn, The Netherlands 3 Lehrstuhl Spezielle Botanik und Mykologie, Universitiit Tabingen, 72076 Tabingen, Germany A new pleomorphic ascomycete, Calyptrozyma arxii, isolated from the human lower oesophagus, is described. Initial growth results in yeast cells, followed by formation of hyphae. Asexual reproduction occurs by blasto-, aleurio- and arthroconidia. In addition, unicellular to multicellular conidia-like cells occur, which initially are somewhat thick-walled. Finally, the outer wall layers of these cells become loose. Sexual reproduction is by eight-spored asci formed on aggregations of generative hyphae. Although no ascomata are formed, the fungus belongs to the Euascomycetes, as was deduced from septal ultrastructure and partial ribosomal RNA sequences. A fungus isolated from a patient with oesophagitis and white agar, and oatmeal agar (Gams et al., 1987). Preparations and exudate, turned out to represent a new pleomorphic yeast-like measurements were made in water. ascomycete. It was isolated together with species of Penicillium Nuclei were stained using 4'-6' -diamidino-2-phenylindole and Aureobasidium and probably grows saprotrophically. (DAP!) according to Coleman et al. (1981) and examined using Initially, only vegetative growth was observed, revealing a Zeiss AXioskop epifluorescence microscope with filter 01. the highly pleomorphic nature of the fungus. Its asexual stage Cell walls were stained using 5 % aqueous ca!cofluor white and comprised yeast cells, pseudohyphae, true hyphae, blasto-, examined using the same microscope with filter 05. aleurio- and arthroconidia, and unicellular to multicellular, Nutritional physiological tests were performed as described branched and somewhat thick-walled conidium-like structures by Van der Walt & Yarrow (1984). Assimilation of carbon with a loosening outer cell wall. The sexual stage of the life sources was tested in liquid medium, whereas assimilation of cycle, observed on diluted yeast extract-malt extract agar, nitrogen compounds was investigated using auxanograms. consisted of naked asci, formed on aggregations of ascogenous For electron microscopy, cells were fixed in 0'5 % w / v hyphae, occurring along conjugating hyphae. potassium permanganate, stained with 1'5 % uranyl acetate in As the fungus could not be identified with any described 50% ethanol, dehydrated through a graded series of ethanoL genus of endomycetalean yeasts, nor with little-developed and embedded in Spurr's resin. taxa belonging to the Euascomycetes, it is described here as For analysis of cell wall carbohydrates, whole-cell hydro• a new genus and species. lyzates were analysed using gas-liquid chromatography/mass spectroscopy as described by Weijman et al. (1982) and Weijman & Golubev (1987). MATERIALS AND METHODS Coenzyme Q was extracted and purified as described by Yamada & Kondo (1971,1973). The number of isoprenologues Strain studied was determined with reverse-phase thin-layer chromatography The strain, CBS 354.92, was isolated from the lower using Merck HPTLC RP-18 F254s plates and a mixture of oesophagus of a 67-year-old woman from Lake Placid, New acetone and acetonitrile (80:20, v/v) as the developing York u.s.A., suffering from oesophagitis and white exudate. It solvent (Nakase & Suzuki, 1985). The separated components was maintained on 1% w/v yeast extract-D'5% w/v were detected under ultraviolet light at 254 nm. peptone-4% w/v glucose agar (YPGA) slants at 10°C. DNA was isolated from three to five day-old, rotary-shaken Morphology was studied on a variety of media at room cultures (150 rpm), grown at 25° in YPG-broth. Cells were temperature: yeast morphology agar (YMoA, Difco), com washed in tap water and saline EDTA (0'1 M NaCl, meal agar (CMA, Difco), yeast extract-malt extract agar 0'15 M EDTA) and broken with a French Press. DNA was (YMA, Difco), 10 times diluted YMA, YPGA, potato-dextrose isolated and purified using the method of Britten et a!. (1970). agar (PDA, Oxoid), 5 % malt extract agar (MEA, Difco), V8• Molar percentage G + C was analysed according to Owen & juice agar (Gams et a!', 1987), ten times diluted V8-extract Lapage (1976), using a Perkin and Elmer UV/Vis spectro- New pleomorphic ascomycete, Calyptrozyma arxii 1240 3 4 7 10 IJ-rn Figs 1-7. Morphology of Calypfrozymaarxii. Fig. 1. Yeast cells on YMoA. Fig. 2. Hyphae with aleurioconidia on YPGA. Fig. 3. Yeast cell growing into hypha on YMoA. Fig. 4. Blasto- and arthroconidia-like cells on 2% MEA. Fig. 5. Thick-walled conidia-like cells with a loosening outer cell wall on YMA. Fig. 6. Asci on globules of gametangial coils and conjugating hyphae on 10 times diluted YMA. Fig. 7. Conjugating yeast and hyphal cells on 10 times diluted YMA (bar indicates 10 ~m). 1. Boekhout, H. Roeijmans and F. Spaay 1241 Figs 8-18. Fig. 8. Budding yeast cells (YPGA. 24 h, bar = 10 ~m). Fig. 9. CalcoAuor white-stained yeast cells (YPGA. 24 h, bar = 10 ~m). Fig. 10. Blastoconidia and arthroconidia-like cells (YPGA, 8 wk bar = 10 j.lm). Fig. 11. DAPI stained nucleus in mother cell (YPGA, 24 h, bar = 10 ~). Fig 12. DAr! stained nucleus in bud (YPGA, 24 h, bar = 10 ~m). Fig. 13. DAr! stained nuclei in bud and mother cell (YrGA, 24 h, bar = 10 ~m). Fig. 14. Conidia-like cells with a loosening outer cell wall (10 times diluted YMA, 25 d, bar = 10 ~m). Fig. 15. Young vacuolated asci on globule of ascogenous hyphae. (10 times diluted YMA, 25 d, bar = 10 ~m.) Fig. 16. Asci with clusters of ascospores (10 times diluted YMA, 25 d, bar = 10 >-1m). Fig. 17. Cluster of germinating ascospores (10 times diluted YMA, 25 d, bar = 10 ~m). Fig. 18. Septal ultrastructure (KMnO4' bar = 1 j.lm). New pleomorphic ascomycete, Caiyptrozyma arxii 1242 photometer. Temperature increase was 0'5° min-1 and the Tm Table 1. Nutritional physiology of Calyptrozyma arrii value was calculated automatically using the first derivative of Fermentation (25°): absent the melting curve. Candida parapsilosis (CBS 604) was used as a reference. Assimilation of Assimilation of Isolation of ribosomal RNA (rRNA) was performed as carbon compounds (25 0) nitrogen compounds follows. Cells grown in 2 % YPG-broth on a rotary shaker for o.glucose + nitrate + 2 d at 25° were broken in 4 M guanidinium thiocyanate using o-galactose + nitrite + a French Press. The rRNA was purified by centrifugation in a o-sorbose d ethylamine + caesium chloride gradient as described by Maniatis et ai. o.glucosamine -,w L.lysine (1982). The rRNA subunits were separated by non-denatur• o-ribose - .w cadaverine + o-xylose + creatine ating 3'2% acrylamide gel electrophoresis. Sequencing of L-arabinose + creatinine the region of the small subunit rRNA was accomplished with o-arabinose - ,w imidazole a specific primer 5'-ACGGGCGGTGTGTAC (position 1627) L-rhamnose d (Kurtzman & Liu, 1990) and the dideoxynucleotide chain sucrose + termination method (Sanger et al., 1977; Lane et al., 1985). maltose + a,a trehalose + Nucleotide fragments were separated on 8 %-8 M urea gels methyl a-glucoside + and visualized by autoradiography. cellobiose + Sequences (position 1320-1619) were aligned using Align salicin + Plus 2'0 (Scientific & Educational Software) and corrected with arbutin + a word processor. Data from additional species were obtained melibiose + lactose from a database (De Rijk et ai., 1992). raffinose + Reconstruction of the phylograms was done using melezitose + neighbour-joining (Saitou & Nei, 1987) and maximum inulin d,w parsimony using MEGA 1'0 (Kumar et al., 1993). Confidence starch + values for individual branches were determined by bootstrap glycerol d meso-erythritol analysis using 1000 replications (Felsenstein, 1985). ribitol xylitol L-arabinitol RESULTS o-glucitol + o-mannitol + Morphology galactitol +,d myo-inositol +,d After 10 d on YMoA, colonies were ca 6 mm diam. (14 mm glucono a-lactone +,d after 2 I d), flat, with the surface slightly pustulate, wrinkled or 2-keto-o-gluconate ridged, somewhat shiny, pale yellowish, yellowish brown to o-gluconate cream, moist to tough, and with a narrow flattened, sharply o-glucuronate + o-galacturonate + delimited, crenulate margin. The reverse was concolorous. On oL-lactate + YPGA the surface was dull, irregular, with transverse ridges succinate + and locally with white hirsute pustules. On MEA, CMA and citrate YMA submerged mycelial sectors occurred at the margin of methanol the colony. On PDA, V8-juice, and diluted V8-juice agars ethanol + propane 1,2 dial + colonies were yeast-like and formed submerged mycelium at butane 2,3 dial the margin. (+ = growth, - = no growth, w = weak growth, d = delayed Three-day-old colonies at YMoA consisted mainly of yeast growth after 2 or 3 wk) cells, which were ellipsoidal, cylindrical, allantoid, somewhat Growth without vitamins +; resistance to 0'01 % cycloheximide dumb-bell-shaped or ogival, 6-9'5 x 2-4 11m (3-5-8 x 2-5 11m growth with 50% glucose -; starch production -; acetic acid production on YPGA) Figs 1, 8). Budding occurred enteroblastically at the -; urease activity + ; reaction with Diazonium Blue B-; growth between poles of the cells, usually on short denticles, but also on a 4 and 30° +; growth at 35° slow, no growth at 37°. broad base. Proliferation was sympodial, leaving visible scars. The buds were frequently elongate forming branched hyphae (Fig. 3). Subglobular, uninucleate cells, 6-10 11m diam. were After ca 10 days, clavate aleurioconidia, 6-10 x 3-4 IJm, present, which germinated to form uninucleate ellipsoidal had formed laterally along the hyphae (Fig. 2). The aleurio• yeast cells. During initial growth of the bud, the nucleus conidia were observed to germinate while still attached to remained in the mother cell.
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