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Korea Research Institute of Bioscience and Biotechnology, 52 Oeundong, Yusong, Daejeon 305-333, Korea
Correspondence
Chang-Jin Kim
changjin{at}kribb.re.kr
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain BH30097T is AY616012.
A photomicrograph showing sporangia and vegetative cells of the type strain of Virgibacillus koreensis is available as supplementary material in IJSEM Online.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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), Gracilibacillus (Wainø et al., 1999), Virgibacillus (Heyndrickx et al., 1999), Filobacillus (Schlesner et al., 2001), Oceanobacillus (Lu et al., 2001), Lentibacillus (Yoon et al., 2002) and Pontibacillus (Lim et al., 2005) based on 16S rRNA gene sequence comparisons and chemotaxonomic characteristics.
The genus Virgibacillus was first proposed by Heyndrickx et al. (1998) based on polyphasic data from amplified rDNA restriction analysis (ARDRA), fatty acid profiles, SDS-PAGE patterns of whole-cell proteins and phenotypic characterization, and its description was later emended by Heyrman et al. (2003). Members of the genus Virgibacillus bear oval to ellipsoidal endospores, are motile, Gram-positive rods and have DNA G+C contents ranging from 36 to 43 mol% (Heyrman et al., 2003). The halotolerant bacterium Bacillus salexigens (Garabito et al., 1997) was transferred to the new genus Salibacillus as Salibacillus salexigens (Wainø et al., 1999). Arahal et al. (2000) later proposed the reclassification of Bacillus marismortui as Salibacillus marismortui. Subsequently, Heyrman et al. (2003) proposed on the basis of genotypic and phenotypic data that Virgibacillus and Salibacillus should be combined in a single genus. Following the Rules of the Bacteriological Code (Lapage et al., 1992), the species of Salibacillus were transferred to Virgibacillus as Virgibacillus salexigens and Virgibacillus marismortui. Recently, Bacillus halodenitrificans, first described by Denariaz et al. (1989), was transferred to the genus Virgibacillus as Virgibacillus halodenitrificans (Yoon et al., 2004). The genus Virgibacillus comprises eight species at the time of writing.
We isolated a novel bacterium, strain BH30097T, from a salt field. The morphological, biochemical and phylogenetic distinctiveness of the isolate is described, and we consider that it should be assigned to a novel species of the genus Virgibacillus. As part of our study of this novel isolate, it became apparent that Virgibacillus picturae is closer to the genus Oceanobacillus than to Virgibacillus based on a phylogenetic analysis of their 16S rRNA gene sequences. V. picturae was described by Heyrman et al. (2003); at that time, Heyrman et al. (2003) studied the polyphasic characteristics of Virgibacillus picturae, but did not describe its phylogenetic relationship to the genus Oceanobacillus. The genus Oceanobacillus, with the single species Oceanobacillus iheyensis, was first described by Lu et al. (2001), and Oceanobacillus oncorhynchi was subsequently proposed by Yumoto et al. (2005). Therefore, to clarify the taxonomic position of V. picturae, we examined its phenotypic and chemotaxonomic characteristics, 16S rRNA gene sequences and phylogenetic relationships.
Strain BH30097T was isolated from a salt field near Taean-Gun on the Yellow Sea in Korea on a nutrient agar containing artificial sea water (ASW) including 7 % NaCl. The isolate and reference strains, such as V. halodenitrificans KCTC 3790T and related Virgibacillus and Oceanobacillus species, were cultured on marine agar 2216 (Difco) for 48 h at 30 °C.
Cell morphology was examined by light microscopy and motility was determined with an optical microscope using the hanging drop technique (Skerman, 1967). The flagellum type was determined using transmission electron microscopy using cells from the exponential phase of growth, in which cells were negatively stained with 1 % (w/v) phosphotungstic acid and air-dried and the grids were examined using a transmission electron microscope (Philips). Anaerobic growth was recorded in an anaerobic chamber on marine agar. Growth experiments were performed using screw-capped tubes and growth was estimated by monitoring the OD600. The ability to grow with different added salt concentrations (0–25 % w/v NaCl) was tested with nutrient broth (Difco) as the basal medium. Growth at different temperatures was observed in trypticase soy broth at 10, 15, 20, 25, 30, 35, 40, 45 and 50 °C. Growth experiments at different pH values were performed using 10 ml trypticase soy broth adjusted to pH 6·0–10·0 (Sorokin, 2005); 100 mM Na2HPO4/NaH2PO4 buffer (pH 6·0–8·0) and 100 mM NaHCO3/Na2CO3 buffer (pH 9·0–10·0) were used. This experiment was performed based on the methods of Yumoto et al. (1998). API 20E and API 50CHB systems (bioMérieux) were used for physiological and biochemical characterization. All suspension media were supplemented with 7 % (w/v) NaCl. All API tests were performed in accordance with the manufacturer's recommendations (bioMérieux). Catalase activity was determined by bubble production from 3 % (v/v) H2O2, and oxidase activity was determined using 1 % (w/v) tetramethyl-p-phenylenediamine.
Cells of the isolate were Gram-positive rods, motile by means of peritrichous flagella, that formed chains and/or filaments (see Supplementary Fig. S1 in IJSEM Online); ellipsoidal endospores formed in terminal positions (Supplementary Fig. S1). Strain BH30097T formed circular, low-convex, smooth, semi-translucent and cream-coloured colonies. The isolate grew anaerobically and at an NaCl concentration of 0·5–20 %; optimum growth was at 5–10 % (w/v) NaCl. The isolate grew at between 10 and 45 °C, but not at 50 °C; optimum growth was observed at 25 °C. Strain BH30097T grew at pH 5·5–9·0, with an optimum at pH 7·0. The isolate tested positive for aesculin hydrolysis, 
-galactosidase, oxidase and catalase activities and acid production from amygdalin, L-arabinose, cellobiose, aesculin, D-fructose, maltose and D-xylose. It gave negative results for nitrate reduction, indole production, D-glucose acidification, arginine hydrolysis, urease, gelatin hydrolysis and acid production from N-acetylglucosamine, D-arabinose, galactose, L-fucose, glycerol, glycogen, myo-inositol, 5-keto-D-gluconate, mannitol, D-mannose, D-melibiose, L-rhamnose and D-turanose.
For total cellular fatty acid analysis, cells were cultured on trypticase soy agar for 48 h at 30 °C and the fatty acids were extracted following the procedures for the Microbial Identification System (MIDI, Inc.), as described previously (Lee et al., 1996; Yang et al., 1993). Isoprenoid quinones were extracted with chloroform/methanol (2 : 1, v/v), and purified by TLC on Merck Kieselgel 60 F254 plates (20x20 cm, 0·5 mm thickness) using petroleum ether/diethyl ether (9 : 1, v/v) as the solvent. The identity of the quinones was determined by HPLC, as described by Shin et al. (1996). Diaminopimelic acid (DAP) isomers were determined using the method of Komagata & Suzuki (1987). Extraction and analysis of polar lipids by two-dimensional TLC were performed according to the methods of Komagata & Suzuki (1987).
Whole-cell fatty acid profiles for strain BH30097T and related Virgibacillus and Oceanobacillus species are shown in Table 1. Major fatty acids (>1 %) in strain BH30097T were anteiso-C15 : 0 (43·42 %), iso-C16 : 0 (14·42 %), iso-C14 : 0 (8·32 %), anteiso-C17 : 0 (7 %), iso-C15 : 0 (6·13 %), C16 : 0 (5·91 %), C15 : 0 (5·08 %), C16 : 1
7c alcohol (3·35 %), C16 : 111c (2·24 %) and C14 : 0 (1·81 %). This profile was similar to those of members of the genus Virgibacillus. The major menaquinone and DAP isomer in the cell-wall peptidoglycan of strain BH30097T were MK-7 and meso-DAP, respectively. Cells of strain BH30097T and O. iheyensis KCTC 3954T contained diphosphatidylglycerol, phosphatidylglycerol and unidentified phospholipids. An unknown aminophospholipid that gave a positive reaction to ninhydrin spraying, reported for some Virgibacillus species by Heyrman et al. (2003), was not detected in strain BH30097T or O. iheyensis KCTC 3954T.
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. The DNA G+C content was determined using the reversed-phase HPLC method described by Tamaoka & Komagata (1984). The DNA G+C contents of BH30097T and V. halodenitrificans KCTC 3790T were 41 and 38 mol%, respectively.
Two universal primers (9F and 1492R) described by Stackebrandt & Liesack (1993) were used for PCR amplification of the 16S rRNA gene, and the amplified PCR product was purified using a QIAquick PCR purification kit (Qiagen). The purified 16S rRNA gene was then sequenced using an ABI Prism BigDye Terminator cycle sequencing ready reaction kit (Applied Biosystems), with an automatic DNA sequencer (model 377; Applied Biosystems). Nearly complete 16S rRNA gene sequences (1435 bp) were determined for BH30097T and aligned with those of representatives from the genus Virgibacillus and related taxa using CLUSTAL W software (Thompson et al., 1994). A phylogenetic tree was constructed using the neighbour-joining method (Saitou & Nei, 1987) based on distance matrix data. Evolutionary distances were calculated using the Jukes & Cantor (1969) model. The PHYLIP software package (Felsenstein, 1993) was used for all the analyses. The topology of the phylogenetic tree was evaluated using a bootstrap analysis (Felsenstein, 1985) of the neighbour-joining method based on 1000 replications.
The primary structures of the 16S rRNA gene sequence of strain BH30097T were compared with those of closely related reference strains. A phylogenetic tree, based on Knuc values (Fig. 1), indicated that strain BH30097T belonged to the genus Virgibacillus. Strain BH30097T was phylogenetically most closely related to V. halodenitrificans KCTC 3790T (96·7 % 16S rRNA gene sequence similarity). Levels of sequence similarity between strain BH30097T and other Virgibacillus species ranged from 93·8 to 96·0 %. These values fell within the range that generally can be used to define a novel species (Rossello-Mora & Amann, 2001; Stackebrandt et al., 2002).
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). We chose two reference strains, V. halodenitrificans KCTC 3790T and Virgibacillus carmonensis KCTC 3819T, for the DNA–DNA hybridization experiments, V. halodenitrificans KCTC 3790T because it was the strain most closely related to BH30097T and V. carmonensis KCTC 3819T as the type species of the genus. As shown in Table 2, DNA–DNA reassociation values between strain BH30097T and the two reference strains were less than 28 %, and that between the two reference strains was less than 33 %. As such, the 16S rRNA gene sequence data comparison and DNA–DNA hybridization results demonstrated that strain BH30097T was most closely related to the genus Virgibacillus but was not a member of any recognized Virgibacillus species.
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; Namwong et al., 2005) and Oceanobacillus (Lu et al., 2001). Oceanobacillus currently comprises two species, O. iheyensis (Lu et al., 2001) and O. oncorhynchi (Yumoto et al., 2005). In our study, we found that V. picturae was linked to the genus Oceanobacillus with a bootstrap resampling value of 68·9 % (Fig. 1
). In the phylogenetic tree constructed using the neighbour-joining algorithm, the genus Oceanobacillus (including V. picturae) formed a distinct clade with Virgibacillus and Lentibacillus (Fig. 1). A phylogenetic tree was also constructed using the maximum-likelihood method (Saitou & Nei, 1987) based on distance matrix data. Evolutionary distances were calculated using the Jukes & Cantor (1969) model. The topology of the phylogenetic tree constructed using the maximum-likelihood algorithm was similar to that of the tree constructed using the neighbour-joining algorithm (data not shown). There are currently not enough taxonomic data to distinguish Virgibacillus from Oceanobacillus (Tables 1 and 2). They have similar chemotaxonomic characteristics, such as their major menaquinone (MK-7), cellular fatty acids (anteiso-C15 : 0) and polar lipids (Table 3). In their fatty acid profiles, genera related to the genus Bacillus have anteiso-C15 : 0 as the major cellular fatty acid. V. picturae and the two Oceanobacillus species also had anteiso-C15 : 0 as the major fatty acid. Clear differences in the amounts of iso-C15 : 0, iso-C16 : 0, anteiso-C17 : 0 and C16 : 0 among V. picturae and O. iheyensis and O. oncorhynchi were observed. V. picturae grew at pH 7·0–10·0, and O. iheyensis and O. oncorhynchi respectively grew at pH 6·5–10·0 and pH 9·0–10·0. These results showed they are facultatively alkaliphilic bacteria, an important characteristic of the genus Oceanobacillus. On the basis of the morphological, physiological and chemotaxonomic characteristics presented and 16S rRNA gene sequence comparisons, it is proposed that Virgibacillus picturae be transferred to the genus Oceanobacillus as Oceanobacillus picturae comb. nov.
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, 2000; Denariaz et al., 1989; Heyndrickx et al., 1998, 1999; Heyrman et al., 2003; Lu et al., 2001; Wainø et al., 1999; Yoon et al., 2004; Yumoto et al., 2005), are given in Table 3.
Description of Virgibacillus koreensis sp. nov.
Virgibacillus koreensis (ko.re.en'sis. N.L. masc. adj. koreensis for Korea, where the type strain was isolated).
Cells are Gram-positive, rod-shaped (0·5–0·7x2·0–7·0 µm) and motile by means of peritrichous flagella. Ellipsoidal spores are formed in terminal positions. Colonies are circular, low-convex, smooth, semi-translucent and cream-coloured on marine agar. The type strain grows in an anaerobic chamber at 37 °C. The temperature range for growth is 10–45 °C (optimal at 25 °C). The pH range for growth is 5·5–9·0 (optimal at pH 7·0). No growth occurs with NaCl concentrations of more than 20 %, while optimal growth occurs with a NaCl concentration of 5–10 %. Positive for aesculin hydrolysis, -galactosidase, oxidase and catalase activities and acid production from amygdalin, L-arabinose, cellobiose, aesculin, D-fructose, maltose and D-xylose. Negative for nitrate reduction, indole production, glucose acidification, arginine hydrolysis, urease, gelatin hydrolysis and acid production from N-acetylglucosamine, D-arabinose, galactose, L-fucose, glycerol, glycogen, myo-inositol, 5-keto-D-gluconate, mannitol, D-mannose, D-melibiose, L-rhamnose and D-turanose. The DNA G+C content is 41 mol%, the major isoprenoid quinone is MK-7 and the major cellular fatty acids are anteiso-C15 : 0 and iso-C16 : 0. The cell-wall peptidoglycan contains meso-DAP.
The type strain, BH30097T (=KCTC 3823T=JCM 12387T), was isolated from a salt field near Taean-Gun on the Yellow Sea in Korea.
Emended description of genus Oceanobacillus Lu et al. 2002
Oceanobacillus (O.ce.a.no.ba.cil'lus. Gr. n. okeanos the ocean; L. dim. n. bacillus a small rod; N.L. masc. n. Oceanobacillus the ocean bacillus/rod).
Gram-positive, spore-forming rods, motile by means of peritrichous flagella. Ellipsoidal spores are subterminal or terminal within swollen sporangia. Obligately aerobic or facultatively anaerobic, obligately or facultatively alkaliphilic and grow at 0–22 % (w/v) NaCl. Catalase and oxidase reactions are positive. Growth occurs at 5–42 °C. The predominant cellular fatty acid is anteiso-C15 : 0. The major isoprenoid quinine is MK-7. The DNA G+C content is 35·8–40 mol%. The type species is Oceanobacillus iheyensis.
Description of Oceanobacillus picturae (Heyrman et al. 2003) comb. nov.
Oceanobacillus picturae (pic.tu'rae. L. gen. n. picturae pertaining or belonging to a painting).
Basonym: Virgibacillus picturae Heyrman et al. 2003.
The description matches that given by Heyrman et al. (2003). The type strain is strain LMG 19492T (=DSM 14867T=KCTC 3821T).
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ACKNOWLEDGEMENTS |
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