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Japan Collection of Microorganisms, RIKEN BioResource Center, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan
Correspondence
Takuji Kudo
kudo{at}jcm.riken.jp
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Published online ahead of print on 13 October 2005 as DOI 10.1099/ijs.0.63862-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains 2-25(1)T, 2-29(17)T and 2-70(23)T are AB200231, AB200232 and AB200233, respectively.
SEM images of Catellatospora chokoriensis sp. nov., Catellatospora coxensis sp. nov. and Catellatospora bangladeshensis sp. nov. are available as a supplementary figure in IJSEM Online.
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for actinomycete strains that produce short chains of non-motile spores borne directly on the substrate mycelium without the formation of aerial mycelium. This genus originally contained two species, Catellatospora citrea and Catellatospora ferruginea. Subsequently C. citrea subsp. methionotrophica (Asano & Kawamoto, 1988), Catellatospora matsumotoense, Catellatospora tsunoense (Asano et al., 1989) and Catellatospora koreensis (Lee et al., 2000) were added. Of these species, it has been proposed that C. matsumotoense be transferred to the genus Micromonospora as Micromonospora matsumotoense, based on 16S rRNA gene sequence analysis and phenotypic characteristics (Lee et al., 1999). Recently, C. ferruginea (Asano & Kawamoto, 1986) was transferred to the genus Asanoa as Asanoa ferruginea (Lee & Hah, 2002). The emergence of molecular systematics, numerical phenetic classification and chemotaxonomy has led to the assignment of species of the genus Catellatospora to three species, C. citrea (with C. citrea subsp. citrea and C. citrea subsp. methionotrophica), C. tsunoense and C. koreensis. In the course of investigation of novel actinomycetes from soil in the southern area of Bangladesh, we isolated strains 2-25(1)T, 2-29(17)T and 2-70(23)T that showed the typical morphological characteristics of the genus Catellatospora. In this paper, we describe the characterization and classification of these strains and propose three novel species, Catellatospora chokoriensis sp. nov., Catellatospora coxensis sp. nov. and Catellatospora bangladeshensis sp. nov. We also propose the elevation of C. citrea subsp. methionotrophica to a separate species as C. methionotrophica comb. nov. on the basis of DNA–DNA relatedness and physiological and biochemical characteristics.
Strains 2-25(1)T, 2-29(17)T and 2-70(23)T were isolated from sandy soil collected at a forest-side waterfall in Chokoria, Cox's Bazar, Bangladesh. Strains were isolated using the standard dilution plate method and grown on humic acid-vitamin agar (HV; Hayakawa & Nonomura, 1987) supplemented with cycloheximide (50 mg l–1), nystatin (50 mg l–1) and nalidixic acid (20 mg l–1). After 21 days of aerobic incubation at 30 °C, the strains were transferred and purified on yeast extract-malt extract agar (medium 2 of the International Streptomyces Project) and maintained as working cultures on yeast extract-starch agar containing, l–1 distilled water (pH 7·2), 15·0 g soluble starch, 4·0 g yeast extract, 0·5 g K2HPO4, 0·5 g MgSO4.7H2O and 15·0 g agar. For comparative purposes, the following type strains of the genus Catellatospora were used in this study: C. citrea subsp. citrea JCM 7542T, C. citrea subsp. methionotrophica JCM 7543T, C. tsunoense JCM 9105T and C. koreensis JCM 10976T.
Strains 2-25(1)T, 2-29(17)T and 2-70(23)T were grown on tap-water agar and sucrose nitrate agar (Waksman no. 1) media at 30 °C for 21 days and then observed by light microscopy and scanning electron microscopy (SEM) (model S-2400; Hitachi). The sample for SEM was prepared as described by Itoh et al. (1989). Phenotypic properties were examined by several standard methods. For cultural characterization, the isolates were grown for 21 days at 30 °C on various agar media as described by Waksman (1950, 1961), Shirling & Gottlieb (1966) and Asano & Kawamoto (1986) (Table 1). The names and designations of colony colours were determined according to Jacobson et al. (1958). The temperature range and NaCl tolerance for growth were determined on yeast extract-starch agar. Utilization of carbohydrates as sole carbon sources was tested by using neutralized yeast nitrogen base without amino acids as a basal medium according to the method of Stevenson (1967). Production of melanoid pigments was examined using tyrosine agar.
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. Reducing sugars from whole-cell hydrolysates were analysed using the HPLC method of Mikami & Ishida (1983). The technique of Uchida & Aida (1984) was used to determine the N-acyl group of muramic acid present in the peptidoglycan. Cell phospholipids were extracted and identified by the method of Minnikin et al. (1984). Methyl esters of cellular fatty acids were prepared and analysed according to the instructions for the Microbial Identification System (Sherlock Microbial Identification System; Hewlett Packard) (Sasser, 1990). Isoprenoid quinones were extracted by the method of Collins et al. (1977, 1984) and were analysed by an HPLC equipped with a Cosmosil 5C18 column (4·6x150 mm; Nacalai Tesque) (Tamaoka et al., 1983) and mass spectrometry (GCMS QP5050; Shimadzu). Preparation and detection of methyl esters of mycolic acids were carried out as described by Tomiyasu (1982).
Genomic DNA extraction, PCR-mediated amplification of the 16S rRNA gene and sequencing of the PCR products were carried out as described by Nakajima et al. (1999). The sequences were multiply aligned with selected sequences (Fig. 1) obtained from the GenBank/EMBL/DDBJ databases by using the CLUSTAL_X package (Thompson et al., 1997). The alignment was verified manually and adjusted prior to the construction of a phylogenetic tree. A phylogenetic tree constructed by the neighbour-joining method (Saitou & Nei, 1987) in the PAUP package (version 4.0b10) (Swofford, 2001) was based on a comparison of 1355 nucleotides present in all of the strains as a result of elimination of gaps and ambiguous nucleotides from the sequences between positions 34 and 1491 (Escherichia coli position number). Micromonospora chalcea was used as an outgroup. Confidence values for the branches of the phylogenetic tree were determined using bootstrap analyses based on 1000 resamplings (Felsenstein, 1985). The values for sequence similarity among Catellatospora strains were calculated manually after pairwise alignment using the CLUSTAL_X package.
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and Saito & Miura (1963) with minor modifications as follows: crude achromopeptidase (Wako Pure Chemicals), N-acetylmuramidase SG (Seikagaku Kogyo) and lysozyme were used for lysing cells (Kudo et al., 1998). In case cells were not lysed by these enzymes, the cells were freeze-dried and mechanically ground as described by Raeder & Broda (1985). The DNA G+C content was determined using the HPLC method of Tamaoka & Komagata (1984). An equimolar mixture of nucleotides for analysis of DNA base composition (Yamasa Shoyu) was digested by bacterial alkaline phosphatase and used as the quantitative standard. DNA–DNA relatedness was measured fluorometrically using the microplate hybridization method devised by Ezaki et al. (1989). Hybridization was carried out at 55 °C for 2 h.
Strains 2-25(1)T, 2-29(17)T and 2-70(23)T produced well-developed and branched substrate mycelium, which was about 0·3–0·6 µm in diameter and did not fragment into bacillary or coccoid elements. Straight to flexuous chains composed of about 5–13 non-motile spores were borne directly on substrate mycelium, singly or in clusters. Each spore was cylindrical to ovoid, 0·5–0·7x0·9–1·1 µm in size and had a smooth surface (see Supplementary Fig. S1 in IJSEM Online). These morphological characteristics are shared with the genera Catellatospora and Asanoa (Asano & Kawamoto, 1986; Lee & Hah, 2002). Table 1
shows the cultural characteristics of strains 2-25(1) T, 2-29(17)T and 2-70(23)T on various media. The results of physiological and biochemical tests are shown in Table 2.
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), phospholipid type II (Lechevalier et al., 1977) and cellular fatty acid type 3b (Kroppenstedt, 1985) (Table 3). The major menaquinone of strains 2-25(1)T, 2-29(17)T and 2-70(23)T was MK-9(H4) and was identical to that of C. citrea subsp. citrea and C. citrea subsp. methionotrophica (Asano & Kawamoto, 1986; Asano et al., 1989). Lee et al. (2000) reported heterogeneity of menaquinone composition in the genus Catellatospora, showing that C. koreensis and C. tsunoense contained MK-10(H4). In this study, all of the data were in agreement with the previous data except that C. tsunoense contained MK-9(H6) as a major component (63 %), accompanied by MK-9(H4) (11 %) and MK-9(H8) (11 %). The DNA G+C content of strains 2-25(1)T, 2-29(17)T and 2-70(23)T was 71 mol%, as shown in Table 4.
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). The levels of sequence similarity among these strains ranged from 98·5 to 99·7 %. Strain 2-25(1)T is most closely related to the type strain of C. citrea subsp. methionotrophica and the two organisms share 99·7 % 16S rRNA gene sequence similarity. Strains 2-29(17)T and 2-70(23)T are most closely related to the type strain of C. citrea subsp. citrea and share 99·5 and 98·5 % 16S rRNA gene sequence similarity, respectively, with C. citrea subsp. citrea. On the basis of the phylogenetic data, as well as the morphological and chemotaxonomic data, it is evident that the three novel strains should be classified in the genus Catellatospora.
The DNA–DNA hybridization technique is used to resolve taxonomic relationships at the species level. In the present study, the levels of DNA–DNA relatedness between strains 2-25(1)T, 2-29(17)T and 2-70(23)T and the other type strains ranged from 3 to 58 % (Table 4). These values are lower than the 70 % cut-off point for the delineation of genomic species proposed by Wayne et al. (1987). On the basis of physiological, biochemical, chemotaxonomic and DNA–DNA hybridization data, as well as 16S rRNA gene sequence analysis, strains 2-25(1)T, 2-29(17)T and 2-70(23)T can be readily differentiated from one another and from the previously recognized species of the genus Catellatospora. On this basis, the names Catellatospora chokoriensis sp. nov., Catellatospora coxensis sp. nov. and Catellatospora bangladeshensis sp. nov. are proposed for strains 2-25(1)T, 2-29(17)T and 2-70(23)T, respectively.
In 1988, the name C. citrea subsp. methionotrophica was proposed for a methionine-deficient auxotroph of the Actinomycetales (Asano & Kawamoto, 1988). On the basis of chemotaxonomy, morphology and carbohydrate utilization data, this strain was classified as a novel subspecies of C. citrea. Later, according to Asano et al. (1989), Lee et al. (2000) and this study (Table 2), this subspecies showed dissimilarities in carbohydrate utilization when compared with C. citrea. Furthermore, the results of DNA–DNA hybridization experiments showed that the relatedness values between C. citrea subsp. citrea and C. citrea subsp. methionotrophica were 52–53 % (Table 4). These values are thought to be sufficiently low for C. citrea subsp. methionotrophica to be considered as a separate species. C. citrea subsp. methionotrophica also showed low DNA–DNA relatedness with our isolates (33–46 %) (Table 4) and the type strains of C. tsunoense (15–18%) and C. koreensis (13–15 %) (data not shown). Therefore, we propose that C. citrea subsp. methionotrophica be elevated to an independent species of the genus Catellatospora as Catellatospora methionotrophica sp. nov., comb. nov.
Description of Catellatospora chokoriensis sp. nov.
Catellatospora chokoriensis (cho.kor.i.en'sis. N.L. fem. adj. chokoriensis pertaining to Chokoria, Bangladesh, the origin of the soil from which the type strain was isolated).
Forms a well-developed, branched substrate mycelium. An aerial mycelium is absent. Sporulation is abundant and short chains of spores are borne directly on substrate mycelium. Spores are spherical to cylindrical and non-motile. Spore surface is smooth. The substrate mycelium is light yellow to bright yellow on yeast extract-starch agar. A soluble pigment is not produced. Aerobic. Gram-positive. Grows at pH 6–9. The temperature range for growth is between 15 and 30 °C. Utilizes D-glucose, L-arabinose, D-xylose, D-galactose, D-mannose, salicin, lactose, 
-D-melibiose, sucrose, maltose and trehalose. No utilization of glycerol, erythritol, adonitol, D-ribose, D-fructose, L-rhamnose, myo-inositol, D-mannitol, methyl -D-glucoside or D-raffinose. No production of melanoid pigments. No growth on 2 % NaCl. The A2pm isomer is of the meso type and is accompanied by its 3-hydroxy derivative and arabinose, xylose, galactose, rhamnose, ribose, mannose and glucose in whole-cell hydrolysates. The muramic acid N-acyl type is glycolyl. Mycolic acids are absent. Contains phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylinositol and phosphatidylinositol mannosides. Glucosamine-containing phospholipid and phosphatidylcholine are absent. The major menaquinone is MK-9(H4), with minor amounts of MK-9(H6) and MK-9(H2). The fatty acid profile is characterized by significant amounts of iso-C15 : 0 (30·3 %), iso-C16 : 0 (23·0 %) and C17 : 0 (11·0 %). Small amounts of anteiso-C17 : 0 (8·0 %), anteiso-C15 : 0 (6·3 %), iso-C17 : 0 (6·0 %), C18 : 0 (4·3 %), iso-C14 : 0 (4·0 %), C17 : 1
8c (3·5 %), iso-C16 : 1 (2·5 %) and C15 : 0 (2·2 %) fatty acids are also present. The DNA G+C content is 71 mol%.
The type strain, 2-25(1)T (=JCM 12950T=DSM 44900T), was isolated from sandy soil collected at a forest-side waterfall, Chokoria, Bangladesh.
Description of Catellatospora coxensis sp. nov.
Catellatospora coxensis (cox.en'sis. N.L. fem. adj. coxensis pertaining to Cox's Bazar, Bangladesh, the origin of the soil from which the type strain was isolated).
Forms a well-developed, branched substrate mycelium. An aerial mycelium is absent. Short chains of non-motile spores arise singly or in tufts from vegetative hyphae on the surface of agar medium. Spores are spherical to cylindrical and spore surface is smooth. The substrate mycelium is light yellow to bright yellow on yeast extract-starch agar. A soluble pigment is not produced. Aerobic. Gram-positive. Grows at pH 6–9. The temperature range for growth is between 20 and 30 °C. Utilizes D-glucose, glycerol, L-arabinose, D-ribose, D-xylose, D-galactose, D-mannose, L-rhamnose, lactose, -D-melibiose, sucrose, maltose and trehalose. No utilization of salicin, erythritol, adonitol, D-fructose, myo-inositol, D-mannitol, methyl -D-glucoside or D-raffinose. No production of melanoid pigments. No growth on 1 % NaCl. The A2pm isomer is of the meso type and is accompanied by its 3-hydroxy derivative and arabinose, xylose, galactose, rhamnose, ribose, mannose and glucose in whole-cell hydrolysates. The muramic acid N-acyl type is glycolyl. Mycolic acids are absent. Contains phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylinositol and phosphatidylinositol mannosides. Glucosamine-containing phospholipid and phosphatidylcholine are absent. The major menaquinone is MK-9(H4), with minor amounts of MK-9(H6) and MK-9(H2). The fatty acid profile is characterized by significant amounts of iso-C15 : 0 (22·2 %), iso-C16 : 0 (19 %) and C17 : 0 (14·4 %). Small amounts of C17 : 1 (8·0 %), anteiso-C15 : 0 (7·4 %), C15 : 0 (4·9 %), iso-C14 : 0 (4·8 %), anteiso-C17 : 0 (4·5 %), iso-C17 : 0 (2·3 %), C18 : 0 (1·8 %), C16 : 0 (1·6 %), C18 : 18c (1·6 %) and C19 : 0 (1·2 %) fatty acids are also present. The DNA G+C content is 71 mol%.
The type strain, 2-29(17)T (=JCM 12951T=DSM 44901T), was isolated from sandy soil collected at a forest-side waterfall, Chokoria, Cox's Bazar, Bangladesh.
Description of Catellatospora bangladeshensis sp. nov.
Catellatospora bangladeshensis (ban.gla.desh.en'sis. N.L. fem. adj. bangladeshensis pertaining to Bangladesh, the origin of the soil from which the type strain was isolated).
Forms a well-developed, branched substrate mycelium. An aerial mycelium is absent. Short chains of non-motile spores arise singly or in tufts from vegetative hyphae on the surface of agar medium. Spores are spherical to cylindrical and spore surface is smooth. The substrate mycelium is light yellow to bright yellow on yeast extract-starch agar. A soluble pigment is not produced. Aerobic. Gram-positive. Grows at pH 6·8–7·2. The temperature range for growth is between 25 and 30 °C. Utilizes D-glucose, L-arabinose, D-xylose, D-galactose, D-mannose, L-rhamnose, salicin, lactose, -D-melibiose, sucrose, maltose and trehalose. No utilization of glycerol, erythritol, adonitol, D-ribose, D-fructose, myo-inositol, D-mannitol, methyl -D-glucoside or D-raffinose. No production of melanoid pigments. No growth on 1 % NaCl. The A2pm isomer is of the meso type and is accompanied by its 3-hydroxy derivative and arabinose, xylose, galactose, rhamnose, ribose, mannose and glucose in whole-cell hydrolysates. The muramic acid N-acyl type is glycolyl. Mycolic acids are absent. Contains phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylinositol and phosphatidylinositol mannosides. Glucosamine-containing phospholipid and phosphatidylcholine are absent. The major menaquinone is MK-9(H4), with minor amounts of MK-9(H6) and MK-9 (H2). The fatty acid profile is characterized by significant amounts of iso-C16 : 0 (35·3 %), iso-C15 : 0 (19·8 %) and C17 : 18c (8·8 %). Small amounts of iso-C14 : 0 (5·2 %), iso-C16 : 1 (3·7 %), C17 : 0 (3·2 %), C14 : 09c (3·1 %), iso-C15 : 0 (2·5 %), anteiso-C17 : 0 (2·3 %), anteiso-C17 : 0 (2·1 %), iso-C17 : 19c (1·8 %), C15 : 0 (1·7 %) and iso-C18 : 0 (1·2 %) fatty acids are also present. The DNA G+C content is 71 mol% (determined by HPLC).
The type strain, 2-70(23)T (=JCM 12949T=DSM 44899T), was isolated from sandy soil collected at Chokoria, Bangladesh.
Description of Catellatospora methionotrophica (Asano and Kawamoto 1988) sp. nov., comb. nov.
Catellatospora methionotrophica (me.thi'o.no.tro'phi.ca. N.L. fem. adj. methionotrophica methionine auxotroph).
Basonym: Catellatospora citrea subsp. methionotrophica Asano & Kawamoto 1988.
The description is based on data taken from earlier studies (Asano & Kawamoto, 1988; Lee et al., 1999, 2000) and our own studies. According to Asano & Kawamoto (1986), most of the characteristics are similar to those of C. citrea except for an absolute requirement for methionine, which can not be replaced by cysteine or homoserine, and no utilization of melibiose. Forms a well-developed, branched substrate mycelium. An aerial mycelium is absent. Forms straight chains of smooth-surfaced spores and has light yellow to bright yellow vegetative hyphae without any soluble pigment production. Aerobic. Gram-positive. Grows at pH 6·8–7·2. The temperature range for growth is between 20 and 34 °C. Production of melanin is negative. No growth on 1 % NaCl. Susceptible to novobiocin (50 µg ml–1), vancomycin (50 µg ml–1), gentamicin (50 µg ml–1) demethyltetracycline (500 µg ml–1) and streptomycin (100 µg ml–1). Utilization of carbon compounds is positive for D- and L-arabinose, cellobiose, D-galactose, D-glucose, lactose, maltose, D-mannose, L-rhamnose, salicin, starch, trehalose, sucrose and D-xylose and negative for ethanol, meso-erythritol, erythritol, adonitol, D-ribose, D-fructose, gluconate, myo-inositol, D-mannitol, melezitose, methyl -D-glucoside, -D-melibiose, methanol, D-raffinose and D-sorbitol. The A2pm isomer is of the meso type and is accompanied by its 3-hydroxy derivative and arabinose, xylose, galactose, ribose, mannose and glucose in whole-cell hydrolysates. The muramic acid N-acyl type is glycolyl. Mycolic acids are absent. Contains phosphatidylethanolamine, diphosphatidylglycerol, phosphatidylglycerol phosphatidylinositol and phosphatidylinositol mannosides. Glucosamine-containing phospholipid and phosphatidylcholine are absent. The major menaquinone is MK-9(H4), with minor amounts of MK-9(H6) and MK-9(H2). The fatty acid profile is characterized by significant amounts of iso-C15 : 0 (37·6 %), C17 : 18c (9·3 %) and C17 : 0 (9·0 %). Smaller amounts of anteiso-C15 : 0 (7·5 %), iso-C16 : 0 (5·7 %), anteiso-C17 : 0 (5·0 %), iso-C17 : 0 (2·5 %), anteiso-C17 : 0 (2·3 %), anteiso-C17 : 0 (2·1 %), iso-C17 : 19c (1·8 %), C15 : 0 (1·7 %) and iso-C18 : 0 (1·2 %) fatty acids are also present. The DNA G+C content is 71 mol%.
The type strain, JCM 7543T (=DSM 44098T), was isolated from a soil sample collected in Yamanashi, Japan.
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ACKNOWLEDGEMENTS |
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