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1 Department of Microbiology, Faculty of Science, Kasetsart University, 50 Paholyothin Road, Bangkok 10900, Thailand
2 Laboratory of Microbial Biotechnology, Division of Applied Life Sciences, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan
3 NITE Biological Resource Center, Department of Biotechnology, National Institute of Technology and Evaluation, 2-5-8 Kazusakamatari, Kisarazu, Chiba 292-0818, Japan
Correspondence
Savitree Limtong
fscistl{at}ku.ac.th
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; Barnett et al., 2000) and some genera that were separated from Pichia on the basis of differences in partial sequences of small-subunit (18S) and large-subunit (26S) rDNA, i.e. Ogataea (Yamada et al., 1994; Mikata & Yamada, 1995; Suh et al., 2006), Kuraishia (Yamada et al., 1994; Péter et al., 2005), Komagataella (Yamada et al., 1995; Dlauchy et al., 2003; Kurtzman, 2005), Ascoidea, members of which show only weak assimilation of methanol (de Hoog, 1998), and the heterogeneous anamorphic genus Candida (Meyer et al., 1998). Although most known methylotrophic yeasts are mesophiles, some are able to grow above 37 °C (Kurtzman & Fell, 1998; Barnett et al., 2000) and could therefore be either thermophilic or thermotolerant, e.g. Pichia angusta (Ogataea polymorpha), Ogataea henricii (Kurtzman, 1998), Candida methanosorbosa, Candida soronensis (Meyer et al., 1998), Candida thermophila (Shin et al., 2001), Ogataea falcaomoraisii (Morais et al., 2004), Pichia siamensis, Candida krabiensis, Candida sithepensis (Limtong et al., 2004) and Pichia thermomethanolica (Limtong et al., 2005).
The genus Ogataea was proposed by Yamada et al. (1994) on the basis of partial 18S and 26S rDNA sequences to accommodate hat-shaped ascospore-forming, nitrate-assimilating methylotrophic yeast species formerly classified in the genus Pichia, P. angusta, P. minuta var. minuta, P. minuta var. nonfermentans, P. philodendra, P. glucozyma and P. henricii. However, Kurtzman & Robnett (1998) suggested that a more robust dataset is required to substantiate the circumscription of the genus. Later, Morais et al. (2004) listed various teleomorphic species of methylotrophic yeasts as species belonging to the genus Ogataea, with the description of Ogataea falcaomoraisii as a novel sporogenous methylotrophic yeast. Thereafter Péter et al. (2007) proposed Ogataea thermophila sp. nov., the teleomorph of C. thermophila. Recently, Suh et al. (2006) accepted the genus Ogataea as a currently recognized genus in their study on the phylogenetics of the Saccharomycetales.
In the course of an investigation of thermotolerant methylotrophic yeasts in Thailand, 253 strains were isolated from 634 samples of soil and plant materials (e.g. flowers, fruits, barks and tree exudates) by a technique involving three consecutive methanol enrichments (Limtong et al., 2004). Fifty-four strains that showed good growth at 10 °C as well as at 37 °C were categorized as thermotolerant strains according to the definition of Arthur & Watson (1976), i.e. thermotolerant yeasts are strains that grow below 20 °C and up to a high temperature. Of these, seven strains have been reported previously as representing four novel species, P. siamensis, C. krabiensis, C. sithepensis (Limtong et al., 2004) and P. thermomethanolica (Limtong et al., 2005). In this study, we describe two additional strains of these yeasts, PT44T and S051T, respectively obtained from soil and a tree exudate, as representing two novel thermotolerant, methylotrophic species of the genus Ogataea. Moreover, we propose to transfer P. siamensis and P. thermomethanolica to the genus Ogataea.
Strain PT44T was isolated from soil in Chonburi Province and S051T was obtained from a tree exudate in Nakhon-Phanom Province. Isolation was carried out using a procedure involving three consecutive enrichments with 1 % methanol-YNB broth (0.67 % Difco yeast nitrogen base and 1 %, v/v, methanol) at room temperature as described previously (Limtong et al., 2004). The strains were categorized as thermotolerant, methylotrophic yeasts on the basis of good growth at 10 and 37 °C.
The strains were characterized morphologically, physiologically and biochemically by using standard methods described by Yarrow (1998). Assimilation of nitrogen compounds was examined on solid media with starved inocula according to the method of Nakase & Suzuki (1986). Growth at various temperatures was determined by cultivation in YM broth and on YM agar, using a water bath and an incubator, respectively. Ubiquinones were extracted from intact packed cells cultivated in YPD broth on a rotary shaker at 28 °C for 24–48 h and purified according to the method described by Yamada & Kondo (1973) and Kuraishi et al. (1985). Isoprenologues were identified by HPLC by using a Cosmosil (Waters 5C18) 4.6x250 mm column and methanol/2-propanol (2 : 1) at 1 ml min–1 as the elution system with spectrophotometric detection (wavelength 275 nm).
The sequences of the D1/D2 domains of the 26S rDNA of the two strains were determined by the National Collection of Industrial, Marine and Food Bacteria (Japan), as described previously (Limtong et al., 2004). The sequences were compared pairwise by using BLAST similarity searches (Altschul et al., 1997) and were aligned with the sequences of related species retrieved from GenBank by using the multiple alignment program CLUSTAL_X version 1.81 (Thompson et al., 1997). A phylogenetic tree was constructed from the evolutionary distance data with Kimura's two-parameter correction (Kimura, 1980) by using the neighbour-joining method (Saitou & Nei, 1987). Confidence limits for the phylogenetic tree were estimated from bootstrap analysis (1000 replicates) (Felsenstein, 1985).
The sequence of the D1/D2 domain of the 26S rDNA of strain PT44T differed from that of strain S051T by 25 nucleotide substitutions and 1 gap out of 565 nt. In the phylogenetic tree based on the D1/D2 domains of 26S rDNA sequences, strain PT44T clustered with the other methylotrophic yeast species Pichia (Ogataea) dorogensis, O. minuta var. minuta, O. minuta var. nonfermentans and Ogataea kodamae (Fig. 1). The closest relative of strain PT44T in terms of pairwise sequence similarity was P. (O.) dorogensis, with 2.3 % nucleotide substitutions (13 nucleotide substitutions and 1 gap in 554 nt) in the D1/D2 domain of the 26S rDNA. Strain S051T formed a separate cluster with P. thermomethanolica in the phylogenetic tree. P. thermomethanolica was the closest species in terms of pairwise sequence similarity to strain S051T, with 1.2 % nucleotide substitutions (7 nucleotide substitutions in 566 nt). According to Kurtzman & Robnett (1998), yeast strains that show nucleotide substitution greater than 1 % in the D1/D2 domain of the 26S rDNA are likely to represent different species.
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and 3), proliferated by multilateral budding, lacked arthroconidia and ballistoconidia, assimilated nitrate and nitrite, were negative for Diazonium blue B colour and urease reactions and had Q-7 as the major ubiquinone. These characteristics coincided well with those of the genus Ogataea. Strains PT44T and S051T were differentiated by some phenotypic characteristics (Table 1). We therefore conclude that strains PT44T and S051T represent two novel species of Ogataea, for which the names Ogataea chonburiensis sp. nov. (strain PT44T) and Ogataea nakhonphanomensis sp. nov. (strain S051T) are proposed.
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, 2005). In the phylogenetic tree based on the D1/D2 domain of the 26S rDNA sequence, P. siamensis and P. thermomethanolica clustered with other methylotrophic yeasts including O. thermophila, O. polymorpha, P. (O.) dorogensis, O. minuta var. minuta, O. minuta var. nonfermentans, O. kodamae and Ogataea philodendri. Since the genus Ogataea is currently recognized (Suh et al., 2006), we propose to transfer P. siamensis and P. thermomethanolica to the genus Ogataea as Ogataea siamensis comb. nov. and Ogataea thermomethanolica comb. nov.
Ogataea chonburiensis sp. nov. and Ogataea nakhonphanomensis sp. nov. can be distinguished from their closest phylogenetic relatives, P. (O.) dorogensis and O. thermomethanolica, respectively, by a number of phenotypic characteristics shown in Table 1
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Latin diagnosis of Ogataea chonburiensis Limtong, Srisuk, Yongmanitchai, Yurimoto et Nakase sp. nov.
In agaro YM post dies 3–5 ad 28 °C cellulae globosae aut subglobosae, (1.7–4.4x1.7–4.8 µm), singulae, aut binae, per germinationem multipolarem reproducentes. Cultura albida, glabra, nitida, butyrosa, margine glabra. In medio liquido carbone assimilatione pellicula non formatur. In agaro farinae Zea mays et YM post dies 7 ad 28 °C mycelium nec pseudomycelium non formatur. Ascosporae galeiformes aut pileiformes, 4 in ascum. Fermentatio nulla. Glucosum, L-sorbosum (exigue), D-xylosum, L-arabinosum (lente), trehalosum, cellobiosum, salicinum, glycerolum, erythritolum, glucitolum, D-mannitolum, glucono-
-lactonum, acidum succinicum, acidum citricum, methanolum, ethanolum, kalium nitricum, natrium nitrosum, ethylaminum, L-lysinum et cadaverinum assimilantur at non galactosum, D-ribosum, D-arabinosum, L-rhamnosum, sucrosum, maltosum, methyl-
-D-glucosidum, melibiosum, lactosum, raffinosum, melezitosum, inulinum, amylum solubile, ribitolum, galactitolum, inositolum, acidum 2-ketogluconicum, acidum 5-ketogluconicum, acidum D-gluconicum, acidum D-glucuronicum, acidum D-galacturonicum, nec acidum DL-lacticum. Vitamina externa crescentiae necessaria est. Crescere potest in temperatura 40 °C at non in 45 °C. Crescit in 0.1 % cycloheximidem. Non crescit in 50 % glucosum nec 10 % NaCl/5 % glucosum. Ureum non hydrolysatur. Diazonium caeruleum B non respondens. Ubiquinonum majus: Q-7.
Typus stirps PT44T (=BCC 21227T =NBRC 101965T =CBS 10363T) isolatus ex solo, in Chonburi Provincia, Thailandia, conservatur in collectionibus culturarum quas Centraalbureau voor Schimmelcultures (Utrecht, The Netherlands), NITE Biological Resource Center (Chiba, Japan) et BIOTEC Culture Collection, National Center for Genetic Engineering and Biotechnology, Thailand (Phatumthani, Thailand) deposita est.
Description of Ogataea chonburiensis Limtong, Srisuk, Yongmanitchai, Yurimoto & Nakase sp. nov.
Ogataea chonburiensis (chon.bu.ri.en'sis. N.L. fem. adj. chonburiensis referring to Chonburi Province, Thailand, where the type strain was isolated).
After growth on YM agar for 3–5 days at 28 °C, cells are globose to subglobose (1.7–4.4x1.7–4.8 µm) and occur singly or in pairs and proliferate by multilateral budding (Fig. 2). The streak culture is white, smooth, glistening and butyrous and has an entire margin. No pellicle is present on the surface of assimilation media. Pseudohyphae and true hyphae are not produced in Dalmau plate culture on cornmeal agar or YM agar after 7 days at 28 °C. Neither arthroconidia nor ballistoconidia are produced. Four helmet- or hat-shaped ascospores are formed in a deliquescent ascus that may be produced parthenogenetically or by conjugation between a cell and its bud or between independent cells (Fig. 2). Ascospores are observed on 5 % malt extract agar and YM agar after 3–7 days at 28 °C. The major ubiquinone is Q-7. Fermentation is negative. D-Glucose, L-sorbose (weak), D-xylose, L-arabinose (delayed), ,-trehalose, cellobiose, salicin, glycerol, erythritol, D-glucitol, D-mannitol, D-glucono-1,5-lactone, succinic acid, citric acid, methanol, ethanol, potassium nitrate, sodium nitrite, ethylamine hydrochloride, L-lysine hydrochloride and cadaverine are assimilated, but D-galactose, D-ribose, D-arabinose, L-rhamnose, sucrose, maltose, methyl -D-glucoside, melibiose, lactose, raffinose, melezitose, inulin, soluble starch, ribitol, galactitol, myo-inositol, 2-ketogluconic acid, 5-ketogluconic acid, D-gluconic acid, D-glucuronic acid, D-galacturonic acid and DL-lactic acid are not assimilated. No growth in vitamin-free medium. Grows at 40 °C but not at 45 °C. Grows with 0.1 % cycloheximide. No growth on medium containing 50 % (w/v) glucose or 10 % (w/v) sodium chloride/5 % (w/v) glucose. Diazonium blue B colour and urease reactions are negative.
Type strain PT44T (=BCC 21227T =NBRC 101965T =CBS 10363T) was isolated from soil collected in Chonburi Province, Thailand.
Latin diagnosis of Ogataea nakhonphanomensis Limtong, Srisuk, Yongmanitchai, Yurimoto et Nakase sp. nov.
In agaro YM post dies 3–5 ad 28 °C cellulae globosae aut subglobosae, (2.0–3.6x2.5–3.8 µm), singulae, aut binae, per germinationem multipolarem reproducentes. Cultura albida, glabra, nitida, impolita, margine glabra. In medio liquido carbone assimilatione pellicula non formatur. In agaro farinae Zea mays et YM post dies 7 ad 28 °C mycelium nec pseudomycelium non formantur. Ascosporae galeiformes aut pileiformes, 4 in ascum. Fermentatio nulla. Glucosum, L-sorbosum, D-ribosum, D-xylosum, L-arabinosum, D-arabinosum (exigue), L-rhamnosum, maltosum, trehalosum, -methyl-D-glucosidum, cellobiosum, salicinum, melezitosum, glycerolum, erythritolum, ribitolum, D-glucitolum, D-mannitolum, glucono--lactonum, acidum succinicum (lente), acidum citricum, methanolum, ethanolum, kalium nitricum, natrium nitrosum,ethylaminum, L-lysinum et cadaverinum assimilantur at non galactosum, N-acetyl-D-gluosaminum, sucrosum, melibiosum, lactosum, raffinosum, inulinum, amylum solubile, galactitolum, inositolum, acidum 2-ketogluconicum, acidum 5-ketogluconicum, acidum D-gluconicum, acidum D-glucuronicum nec acidum D-galacturonicum. Vitamina externa crescentiae necessaria est. Crescere potest in temperatura 40 °C at non in 45 °C. Crescit in 0.1 % cycloheximidem, 50 % glucosum et 10 % NaCl/5 % glucosum. Non crescit in 60 % glucosum. Ureum non hydrolysatur. Diazonium caeruleum B non respondens. Ubiquinonum majus: Q-7.
Typus stirps S051T (=BCC 21228T =NBRC 101966T =CBS 10362T) isolatus ex exudatum, in Nakhon-Phanom Provincia, Thailandia, conservatur in collectionibus culturarum quas Centraalbureau voor Schimmelcultures (Utrecht, The Netherlands), NITE Biological Resource Center (Chiba, Japan) et BIOTEC Culture Collection, National Center for Genetic Engineering and Biotechnology, Thailand (Phatumthani, Thailand) deposita est.
Description of Ogataea nakhonphanomensis Limtong, Srisuk, Yongmanitchai, Yurimoto & Nakase sp. nov.
Ogataea nakhonphanomensis (na.khon.pha.nom.en'sis. N.L. fem. adj. nakhonphanomensis referring to Nakhon-Phanom Province, Thailand, where the type strain was isolated).
After growth on YM agar for 3–5 days at 28 °C, cells are globose to subglobose (2.0–3.6x2.5–3.8 µm) and occur singly or in pairs and proliferate by multilateral budding (Fig. 3). The streak culture is white, smooth and glistening and has an entire margin. No pellicle is present on the surface of assimilation media. Pseudohyphae and true hyphae are not produced in Dalmau plate culture on cornmeal agar or YM agar after 7 days at 28 °C. Neither arthroconidia nor ballistoconidia are produced. Four helmet- or hat-shaped ascospores are formed in a deliquescent ascus that may be produced parthenogenetically or by conjugation between a cell and its bud or between independent cells (Fig. 3). Ascospores are observed on 5 % malt extract agar and YM agar after 7 days at 28 °C. The major ubiquinone is Q-7. Fermentation is negative. D-Glucose, L-sorbose, D-ribose, D-xylose, L-arabinose, D-arabinose (weak), L-rhamnose, maltose, ,-trehalose, methyl -D-glucoside, cellobiose, salicin, melezitose, glycerol, erythritol, ribitol, D-glucitol, D-mannitol, D-glucono-1,5-lactone, succinic acid (slow), citric acid, methanol, ethanol, potassium nitrate, sodium nitrite, ethylamine hydrochloride, L-lysine hydrochloride and cadaverine are assimilated, but D-galactose, N-acetyl-D-glucosamine, sucrose, melibiose, lactose, raffinose, inulin, soluble starch, galactitol, myo-inositol, 2-ketogluconic acid, 5-ketogluconic acid, D-gluconic acid, D-glucuronic acid and D-galacturonic acid are not assimilated. No growth in vitamin-free medium. Growth at 40 °C is weak; no growth at 45 °C. Grows on media containing 0.1 % cycloheximide, 50 % glucose and 10 % sodium chloride/5 % glucose but not on 60 % glucose. Diazonium blue B colour and urease reactions are negative. Gelatin liquefaction is positive.
Type strain S051T (=BCC 21228T =NBRC 101966T =CBS 10362T) was isolated from a tree exudate collected in Nakhon-Phanom Province, Thailand.
Ogataea siamensis (Limtong, Srisuk, Yongmanitchai, Kawasaki, Yurimoto, Nakase & Kato) Limtong, Srisuk, Yongmanitchai, Yurimoto & Nakase comb. nov.
Basionym: Pichia siamensis Limtong, Srisuk, Yongmanitchai, Kawasaki, Yurimoto, Nakase & Kato. J Gen Appl Microbiol 50 (2004), 121. Type strain: JCM 12264T =TISTR 5818T.
Ogataea thermomethanolica (Limtong, Srisuk, Yongmanitchai, Yurimoto, Nakase & Kato) Limtong, Srisuk, Yongmanitchai, Yurimoto & Nakase comb. nov.
Basionym: Pichia thermomethanolica Limtong, Srisuk, Yongmanitchai, Yurimoto, Nakase & Kato. Int J Syst Evol Microbiol 55 (2005), 2226. Type strain: BCC 16875T =JCM 12984T =CBS 10098T.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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