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1 Department of Biology and Medicinal Science, Pai Chai University, 14 Yeonja-1-Gil, Seo-Gu, Daejeon 302-735, Republic of Korea
2 Department of Biological Sciences, Korea Advanced Institute of Science and Technology, 373-1, Guseong-dong, Yuseong-gu, Daejeon 305-701, Republic of Korea
3 Institute of Biochemical Physics, Kosigin st. 4, 119991 Moscow, Russia
4 Korean Collection for Type Cultures (KCTC), Korea Research Institute of Bioscience and Biotechnology, 52 Oeundong, Yusong-gu, Daejeon 305-333, Republic of Korea
Correspondence
Wan-Taek Im
wandra{at}kaist.ac.kr
Sung-Taik Lee
e_stlee{at}kaist.ac.kr
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These authors contributed equally to this work. 
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain Gsoil 420T is AB245377.
An expanded neighbour-joining phylogenetic tree and DNA–DNA relatedness results for strain Gsoil 420T and related Bacillus species are available as supplementary data with the online version of this paper.
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TOPABSTRACTMAIN TEXTREFERENCES |
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; Yoon et al., 2003; Yumoto et al., 2003; Vargas et al., 2005). During the course of a study on the culturable aerobic and facultative anaerobic bacterial community present in a soil sample from a ginseng field in Pocheon Province, South Korea, a large number of novel bacterial strains were isolated (Im et al., 2005). In this study, we have characterized one of those isolates, i.e. a halotolerant strain designated Gsoil 420T. Phenotypic, chemotaxonomic and phylogenetic analyses establish the affiliation of the isolate to the genus Bacillus. The data obtained also suggest that this isolate represents a novel species of the genus Bacillus. Strain Gsoil 420T was originally isolated from a soil sample from a ginseng field in Pocheon Province (South Korea). The soil sample was thoroughly suspended in 50 mM phosphate buffer (pH 7.0) and the suspension, following serial dilution, was then spread onto a modified version of R2A solid medium containing the following (l–1): 0.25 g tryptone, 0.25 g peptone, 0.25 g yeast extract, 0.125 g malt extract, 0.125 g beef extract, 0.25 g Casamino acids, 0.25 g soytone, 0.5 g glucose, 0.3 g soluble starch, 0.2 g xylan, 0.3 g sodium pyruvate, 0.3 g K2HPO4, 0.05 g MgSO4, 0.05 g CaCl2 and 15 g agar. The plates were incubated at 25 °C for 1 month. Single colonies on the plates were purified by subculturing. Strain Gsoil 420T was one of the isolates that appeared on the modified-R2A agar plates under aerobic conditions. Strain Gsoil 420T was routinely cultured on R2A agar at 25 °C and maintained as a glycerol suspension (20 %, w/v) at –70 °C.
The Gram reaction was determined using the non-staining method as described by Buck (1982). The cell morphology was observed under a Nikon light microscope at x1000, with cells grown for 3 days at 25 °C on R2A agar. Catalase activity was determined by assessing bubble production in 3 % (v/v) H2O2; oxidase activity was determined using 1 % (w/v) tetramethyl-p-phenylenediamine. To determine the assimilation of various substrates as sole carbon sources, a defined liquid medium containing the following (l–1) was used: 1.8 g K2HPO4, 1.08 g KH2PO4, 0.5 g NaNO3, 0.5 g NH4Cl, 0.1 g KCl, 0.1 g MgSO4 and 0.05 g CaCl2. A vitamin solution (Widdel & Bak, 1992), a trace element solution (SL-10; Widdel et al., 1983) and a selenite/tungstate solution (Tschech & Pfennig, 1984) were added to the medium and the pH adjusted to 6.8 by the addition of HCl. Aliquots of this liquid medium were added to 96-well trays and then filter-sterilized carbon sources were added to each well (individually, at 0.1 %, w/v). The trays were incubated at 25 °C for up to 7 days and then growth in the wells was examined visually. The negative-control well did not contain an added carbon source. The positive-control well contained R2A broth (l–1: 0.5 g peptone, 0.5 g yeast extract, 0.5 g Casamino acid, 0.5 g dextrose, 0.5 g soluble starch, 0.3 g sodium pyruvate, 0.3 g K2HPO4, 0.05 g MgSO4 and 0.05 g CaCl2). Some physiological characteristics were determined using API 20E and API ID 32GN galleries according to the instructions of the manufacturer (bioMérieux). Anaerobic growth was determined in serum bottles containing R2A broth supplemented with thioglycolate (1 g l–1) under a nitrogen atmosphere. Aerobic nitrate reduction was later confirmed by inoculating three 25 ml serum bottles each containing 12 ml R2A broth supplemented with 10 mM KNO3. The reduction of nitrate was determined using an ion chromatograph (model 790 personal IC; Metrohm) equipped with a conductivity detector and an anion exchange column (Metrosep Anion Supp 4; Metrohm). Tests for the degradation of DNA [in which DNase agar (Scharlau) plates were flooded with 1 M HCl], casein, chitin, starch (Atlas, 1993), lipid (Kouker & Jaeger, 1987), xylan, cellulose and collagen (Ten et al., 2004, 2005) were performed and evaluated after 7 days. Growth at different temperatures (4, 15, 25, 30, 37 and 42 °C) and various pH values (pH 5.0–10.0; at intervals of 0.5 pH units) was assessed after incubation for up to 5 days. The effect of pH on growth was determined on R2A broth media using three different buffers (final concentration, 50 mM): acetate buffer (for pH 5.0–5.5), phosphate buffer (for pH 6.0–8.0) and Tris buffer (for pH 8.5–10.0).
Salt tolerance was tested on R2A agar supplemented with 1–15 % (w/v) NaCl after incubation for up to 5 days. Growth on nutrient agar, trypticase soy agar (TSA) and MacConkey agar was also evaluated, at 25 °C.
An almost-complete 16S rRNA gene sequence of strain Gsoil 420T was determined as described below. DNA was extracted using a commercial genomic DNA-extraction kit (Core Biosystem); PCR-mediated amplification of the 16S rRNA gene and sequencing of the purified PCR product were carried out according to Kim et al. (2005). An almost-complete 16S rRNA gene sequence was compiled using SeqMan software (DNASTAR). The 16S rRNA gene sequences of related taxa were obtained from the GenBank database. Multiple alignments were performed using the CLUSTAL_X program (Thompson et al., 1997). Gaps were edited in the BioEdit program (Hall, 1999). Evolutionary distances were calculated using the Kimura two-parameter model (Kimura, 1983). A phylogenetic tree was constructed by using the neighbour-joining method (Saitou & Nei, 1987) and maximum parsimony (Fitch, 1971) in MEGA3 (Kumar et al., 2004); a bootstrap analysis (Felsenstein, 1985) based on 1000 resamplings was performed.
To measure the G+C content of the chromosomal DNA, the genomic DNA of Gsoil 420T was extracted and purified as described by Ausubel et al. (1995) before being determined as described by Mesbah et al. (1989), using reversed-phase HPLC. Isoprenoid quinones were extracted with chloroform/methanol (2 : 1, v/v), evaporated under vacuum conditions and re-extracted in n-hexane/water (1 : 1, v/v). The crude n-hexane–quinone solution was purified using Sep-Pak Vac silica cartridges (Waters) and subsequently analysed using HPLC, as described previously (Hiraishi et al., 1996). Cellular fatty acid profiles were determined for strains grown on R2A agar (Difco) for 2 days at 30 °C. The cellular fatty acids were saponified, methylated and extracted according to the protocol of the Sherlock Microbial Identification System (MIDI). The fatty acids were then analysed by gas chromatography (model 6890 apparatus; Hewlett Packard) using the Microbial Identification software package (Sasser, 1990). The value range was obtained by performing duplicate experiments.
Strain Gsoil 420T was found to consist of Gram-positive, strictly aerobic, non-motile, rod-shaped cells. Central and subterminal ellipsoidal endospores were observed in swollen sporangia. Colonies grown on R2A agar plates (Difco) for 2 days were smooth, glossy, circular, convex, light yellow and 1.5–3.0 mm in diameter. Oxidase and catalase reactions were positive. Despite the fact that strain Gsoil 420T was isolated from a non-saline environment, it was shown to tolerate NaCl concentrations of up to 12 % (w/v), though it did not require NaCl for growth. Other physiological characteristics of strain Gsoil 420T are summarized in the species description. Phenotypic and chemotaxonomic characteristics that serve to differentiate strain Gsoil 420T from related Bacillus species are listed in Table 1. In contrast to its closest relative, Bacillus niacini IFO 15566T, strain Gsoil 420T did not utilize L-rhamnose, L-fucose, D-sorbitol, itaconate or suberate as sole carbon sources, did not hydrolyse gelatin and did not produce acid from most of the carbohydrates tested. In comparison with the phylogenetically close relative Bacillus bataviensis LMG 21833T, Gsoil 420T did not grow under anaerobic conditions, did not grow on TSA or at 50 °C, was negative for 
-galactosidase production, utilization of L-rhamnose, L-fucose, malonate, propionate and L-serine, and was positive for the assimilation of L-arabinose, inositol and L-histidine. A number of phenotypic and chemotaxonomic characteristics can be used to distinguish strain Gsoil 420T from any other phylogenetically related Bacillus species.
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), strain Gsoil 420T fell within a coherent cluster comprising B. niacini IFO 15566T (16S rRNA gene sequence similarity, 98.6 %), B. bataviensis LMG 21833T (98.6 %), Bacillus soli LMG 21838T (98.3 %), Bacillus drentensis LMG 21831T (98.0 %), Bacillus novalis LMG 21837T (98.0 %), Bacillus vireti LMG 21834T (97.9 %), Bacillus foraminis LMG 23174T (97.6 %), Bacillus fumarioli LMG 17489T (97.4 %) and Bacillus jeotgali JCM 10885T (97.0 %) (Fig. 1). The 16S rRNA gene sequence similarities between Gsoil 420T and all other Bacillus species with validly published names were below 96.8 %. These data indicate that strain Gsoil 420T is separate from recognized Bacillus species other than the nine mentioned above (Stackebrandt & Goebel, 1994). To differentiate strain Gsoil 420T from these closely related species, DNA–DNA hybridization was performed.
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, with photobiotin-labelled DNA probes and micro-dilution wells. Hybridization was performed with five replications for each sample: the highest and lowest values obtained for each sample were excluded and the remaining three values were used to calculate similarity values. The DNA relatedness values quoted are the means of these three values. In comparisons between Gsoil 420T and the closely related species, the highest DNA–DNA reassociation value was 43.2 %, for B. niacini KCTC 3562T (see Supplementary Table S1 available IJSEM Online), indicating that the isolate is not related to them at species level (Wayne et al., 1987). The DNA G+C content of strain Gsoil 420T was 44.9 mol%, which lies within the range observed for members of the genus Bacillus (Shida et al., 1997).
The predominant isoprenoid quinone in strain Gsoil 420T was MK-7. The fatty acid profile of the isolate (shown in Table 2) was compared with those of the type strains of phylogenetically related Bacillus species grown under the same conditions. Strain Gsoil 420T contained large amounts of iso- and anteiso-branched fatty acids: the main components were 12-methyl tetradecanoic acid (anteiso-C15 : 0), 13-methyl tetradecanoic acid (iso-C15 : 0) and 12-methyl tridecanoic acid (iso-C14 : 0), being typical of members of the genus Bacillus (Kämpfer, 1994). However, some qualitative and quantitative differences in fatty acid content could be observed between strain Gsoil 420T and its phylogenetically closest relatives. In particular, in comparison with B. niacini KCTC 3562T, B. bataviensis DSM 15601T and B. drentensis DSM 15600T, strain Gsoil 420T contained larger amounts of anteiso-C15 : 0 and iso-C15 : 0. Additionally, strain Gsoil 420T could be differentiated from B. niacini KCTC 3562T by the significantly smaller amounts of C16 : 0 and C16 : 1
11c, by the absence of C18 : 0 and by the presence of C16 : 17c alcohol. In contrast to B. bataviensis DSM 15601T and B. novalis DSM 15603T, strain Gsoil 420T produced C14 : 0 and C16 : 111c but contained smaller amounts of iso-C16 : 0 and anteiso-C17 : 0.
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). Therefore, on the basis of the data presented, strain Gsoil 420T represents a novel species of the genus Bacillus, for which the name Bacillus pocheonensis sp. nov. is proposed.
Description of Bacillus pocheonensis sp. nov.
Bacillus pocheonensis (po.che.on.en'sis. N.L. masc. adj. pocheonensis pertaining to Pocheon Province in South Korea, the source of the soil sample from which the type strain was isolated).
Cells are strictly aerobic, rod-shaped, 0.7–1.3 µm in width and 3.5–6.5 µm in length and occur singly or in chains. Growth occurs at 20–30 °C, the optimum temperature being 25 °C. The pH range for growth is 5.0–8.5, with an optimum between pH 6.5 and 7.0. Nitrate is reduced to nitrite. Growth occurs on nutrient agar, but not on TSA or MacConkey agar. Hydrolyses aesculin, but not starch, chitin, xylan, CM-cellulose, casein or DNA. Negative for lipase activity. The following substrates are utilized for growth: D-glucose, D-fructose, D-galactose, D-mannose, L-xylose, D-xylose, L-arabinose, D-lyxose, D-cellobiose, maltose, D-melibiose, D-raffinose, N-acetyl-D-glucosamine, acetate (weak growth), pyruvate, lactate, 3-hydroxybutylate (weak growth), valerate (weak growth), fumarate, benzoate (weak growth), salicin, malate, succinate (weak growth), sucrose, trehalose, inositol (weak growth), D-mannitol, glycerol, inulin, L-alanine (weak growth), L-arginine (weak growth), L-asparagine, L-aspartate, L-phenylalanine (weak growth), L-glutamine, L-histidine and L-proline. The following substrates are not utilized for growth: D-fucose, ethanol, L-rhamnose, L-sorbose, D-arabinose, D-ribose, citrate, formate, propionate, tartrate, gluconate, caprate, maleic acid, phenyl acetate, 3-hydroxybenzoate, 4-hydroxybenzoate, malonate, glutarate, itaconate, adipate, suberate, oxalate, D-lactose, D-adonitol, dulcitol, xylitol, D-sorbitol, amygdalin, methanol, glycogen, dextran, L-cysteine, glycine, L-isoleucine, L-leucine, L-glutamate, L-threonine, L-lysine, L-methionine, L-serine, L-tryptophan, L-tyrosine and L-valine. In API 20E tests, the Voges–Proskauer reaction is weakly positive and the reactions for gelatin hydrolysis, -galactosidase, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase, urease, hydrogen sulphide production and indole production are all negative. Acid is weakly produced from L-arabinose but is not produced from D-mannitol, inositol, D-sorbitol, L-rhamnose, sucrose, D-melibiose, D-glucose or amygdalin. The major fatty acids are anteiso-C15 : 0, iso-C15 : 0 and iso-C14 : 0. The DNA G+C content is 44.9 mol%.
The type strain, Gsoil 420T (=KCTC 13943T=DSM 18135T), was isolated from soil from a ginseng field in Pocheon Province, South Korea.
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ACKNOWLEDGEMENTS |
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