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A New Anamorphic Yeast Species, Candida Fragi Suzuki, Nakase Et

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A New Anamorphic Yeast Species, Candida Fragi Suzuki, Nakase Et J. Gen. Appl. Microbiol., 37, 423-429 (1991) CANDIDA FRACI, A NEW SPECIES OF ANAMORPHIC YEAST ISOLATED FROM FERMENTING STRAWBERRY MOTOFUMI SUZUKI,* TAKASHI NAKASE, ANDYOSHIMURA FUKAZAWA' Japan Collection of Microorganisms, The Institute of Physical and Chemical Research (RIKEN), Hirosawa 2-1, Wako 351-01, Japan 'Department of Microbiology, Yamanashi Medical College, Tamaho-cho, Yamanashi 409-38, Japan (Received August 7, 1991) A new anamorphic yeast species, Candida fragi Suzuki, Nakase et Fukazawa, is proposed for a strain isolated from fermenting strawberry that was formerly identified as C. sake, or C. natalensis. Candida fragi resembles Cnatalensis. C. oleophila, and C. sake but is clearly differen- tiated from these species by DNA-DNA relatedness, electrophoretic enzyme patterns, and the proton magnetic resonance spectra of cell wall mannans. Practically, C. fragi is distinguished from C. natalensis by its inability to assimilate trehalose, mannoheptulose, and DL-glyceraldehyde; from C. sake by its inability to assimilate trehalose and a-methyl-D- glucoside and its ability to assimilate 5-ketogluconic acid and xylitol; and from C. oleophila by its inability to assimilate trehalose, to ferment galactose, and to grow in 100 ppm of cycloheximide. In 1962, one of the authors (T. Nakase) isolated a strain of anamorphic yeast from fermenting strawberry collected at a market in Tokyo. This strain showed characteristics similar to those of Torulopsis sake Saito et Oda, which was recog- nized in "The Yeasts, a Taxonomic Study," published in 1952 (4) but it could not be assigned to this species because it produced pseudomycelia. Later, with the transfer of TTsake into the genus Candida by van Uden and Buckley (10), it could be identified as Candida sake (Saito et Oda) van Uden et Buckley. In the 2nd edition of "The Yeasts, a Taxonomic Study," published in 1970, van Uden and Buckley (10) regarded Candida natalensis van der Walt et Tscheuschner, Candida vanriji Capriotti, Candida cloacae Komagata, Nakase et Katsuya, and Candida maltosa Komagata, Nakase et Katsuya as synonyms for C. sake because * Address reprint requests to: Dr . Motofumi Suzuki, Japan Collection of Microorganisms, The Institute of Physical and Chemical Research (RIKEN), Hirosawa 2-l, Wako 351-01, Japan. 423 424 SUZUKI, NAKASE, and FUKAZAWA VOL. 37 they showed similar physiological characteristics to one another. Meyer et al. (5), however, separated C. maltosa from C. sake on the basis of DNA-DNA reasso- ciation experiments. They regarded C. cloacae and Candida subtropicalis Nakase, Fukazawa et Tsuchiya as synonyms for C. maltosa; and C. natalensis, Candida tropicalis (Castellani) Berkhout var. lambica (Harrison) Diddens et Lodder and CC vanriji as those for C. sake. In 1975, Fukazawa et al. (1) carried out extensive taxonomic studies on C. sake and related species, including C. tropicalis var. lambica, C. maltosa, C. vanriji, Candida salmonicola Komagata et Nakase, C. cloacae, Candida parapsilosis (Ashford) Langeron et Talice var. intermedia van Rij et Verona, and C. natalensis. They classified these yeasts into four groups, I, II, III, and IV, based on the proton magnetic resonance (PMR) spectra of purified cell wall mannans and the sero- logical analysis of cell surface antigens. Groups I, II, III, and IV were represented by C. sake, C. maltosa, C. parapsilosis var. intermedia (=C: oleophila Montrocher), and C. natalensis, respectively. They suggested that the four groupings represented at least fourr species. According to them, C. natalensis should form an independent species comprising the two strains, the type strain and a strain isolated from strawberry as mentioned above. In 1980, Montrocher (6) suggested the validity of C. natalensis based on the serological characteristics of cytoplasmic protein antigens. This observation sup- ports the classification by Fukazawa et al. (1) but not that by Meyer et al. (5). In a previous paper (9), we confirmed the distinctness of C. natalensis from C. sake on the basis of DNA-DNA reassociation experiments, electrophoretic patterns of seven enzymes, and the proton magnetic resonance (PMR) spectra of cell wall mannans. Further, we suggested the distinctness of a strain isolated from straw- berry from C. natalensis. This strain showed little DNA relatedness to the type strains of C. natalensis and C. sake. The PMR spectra of mannans and the electrophoretic enzyme patterns correlated well with DNA relatedness. This paper proposes a new species, Candida fragi, for a strain isolated from strawberry that was formerly assigned to C. sake or C. natalensis, with several supplemental data confirming the validity of a new species. MATERIALS AND METHODS Strains examined. A strain (JCM 1791) to be described as a new species was isolated from fermenting strawberry by one of the authors (T. Nakase) at a market at Yodobashi in Tokyo, in May 1962, and has been maintained at the Central Research Laboratories, Ajinomoto, Co., Inc., Kawasaki, Japan, as AJ 4616. Candida natalensis JCM 1445T,C. oleophila JCM 1620T,C, sake JCM 2951T, and C. parapsilosis JCM 1785Tare employed for comparative study. Strains marked with a superscript "T" represent the type strain. Examination of taxonomic characteristics. Most of methods employed for the examination of morphological, physiological, and biochemical characteristics were 1991 Candida fragi sp. n. 425 those described by van der Walt and Yarrow (11). The maximum growth tem- perature was determined in YM broth (Difco Labs) using metal block baths. Vitamin requirements were investigated according to Komagata and Nakase (3). Assimilation of nitrogen compounds was investigated on solid media with starved inoculum as described in a previous paper (8). Chemotaxonomic characteristics were examined by the method previously reported (9). DNAs were extracted and purified according to the method described in the previous papers (7, 9). DNA-DNA hybridization was carried out using the membrane filter technique of Kaneko (2), as described by Nakase and Suzuki (7). RESULTS AND DISCUSSION Candida fragi Suzuki, Nakase et Fukazawa, sp. nov. In liquido "YM," post dies 3 ad 25°C, cellulae rotundae, ovales vel elong- atae, 2.0-5.2 X 4.4-11.2 ,am, singulae, binae, aut in catenis simplicibus aut ramosis. Pellicula et sedimentum formantur. In agaro "YM," post unum mensem ad 17°C, cultura cremea, butyracea, non nitida, elevata et rugosa, margine pilosa. Pseudo- mycelium bene formatur. Glucosum, sucrosum (tardum et exiguum) et maltosum (tardum et exiguum) fermentantur at non galactosum, lactosum, raffinosum nec melibiosum. Glucosum, galactosum, L-sorbosum, sucrosum, maltosum, cellobi- osum, melezitosum, amylum solubile (tardum et exiguum), D-xylosum, D-ribosum (lente), ethanolum (lente), glycerolum, ribitolum, D-mannotolum, D-glucitolum, salicinum (lente), glucono-b-D-lactonum, acidum 2-ketogluconicum, acidum 5 -ketogluconicum, acidum succinicum et acidum citricum assimilantur at non tre- halosum, lactosum, melibiosum, rafpinosum, inulinum, L-arabinosum, D- arabinosum, L-rhamnosum, erythritolum, galactitolum, a-methyl-D-glucosidum, acidum DL-lacticum, inositolum, mannoheptulosum, DL-glyceraldehydum nec xy- litolum. Kalium nitricum non assimilatur. Maxima temperatura crescentiae: 31- 32°C. Ad crescentiam biotinum necessarium est. Diazonium caeruleum B nega- tivum. Proportio molaris guanini + cytosini in acido deoxyribonucleinico: 37.1 mol% (ex Tm). Ubiquinonum majus: Q-9. Teleomorphosis ignota. Holotypus: Isolatus ex frago (Fragaria chiloensi var. ananassa), Tokyo, v. 1962, T. Nakase, JCM 1791 (originaliter ut AJ 4616) conservatur in collectionibus culturarum quas `Japan Collection of Microorganisms, Wako, Saitama 351-01,' sustentat. Growth in YM broth: After 3 days at 25°C, cells are round, oval, or elongate, 2.0-5.2 X 4.4-11.2 ,um, single, in pairs or in simple or branched chains (Fig. 1). A dull creeping pellicle and a sediment are formed. Growth on YM agar: After one month at 17°C, the streak culture is cream-colored, butyrous, dull, raised, and rugose. The margin is fringed with pseudomycelia. Dalmau plate culture on corn meal agar: Well developed pseudomycelia are 426 SUZUKI, NAKASE, and FUKAZAWA VoL. 37 Fig. 1. Vegetative cells of Candid a fragi grown in YM broth for 3 days at 25°C. A, cells in pellicle; B, cells in sediment. Scale= l0,um. Fig. 2. Pseudomycelia of Candida fragi produced on corn meal agar after 7 days at 25°C. Scale= 20,um. produced (Fig. 2). Fermentation: Glucose + Lactose Galactose Raffinose Sucrose + (slow and weak) Melibiose Maltose + (slow and weak) Assimilation of carbon compounds: Glucose + Glycerol + Galactose + Erythritol L-Sorbose + Ribitol + 1991 Candida fragi sp, n. 427 Sucrose + Galactitol Maltose + D-Mannitol + Cellobiose + D-Glucitol + Trehalose a-Methyl-D-glucoside Lactose Salicin + (latent) Melibiose Glucono-o-D-lactone + Rafpinose 2-Ketogluconic acid + Melezitose + 5-Ketogluconic acid + Inulin DL-Lactic acid Soluble starch + (slow and weak) Succinic acid + D-Xylose + Citric acid + L-Arabinose Inositol D-Arabinose Mannoheptulose D-Ribose + (latent) DL-Glyceraldehyde L-Rhamnose Xylitol Ethanol + (latent) Assimilation of nitrogen compounds: Ammonium sulfate + Ethylamine hydrochloride + Potassium nitrate - L-Lysine hydrochloride + Sodium nitrite - Cadaverine dihydrochloride + Maximum growth temperature: 31-32°C. Vitamin required at 25°C: Biotin. Production of starch-like substances: Negative. Growth on 50% glucose-yeast extract agar: Negative. Liquefaction of gelatin: Negative. Hydrolysis
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