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1 Korea Research Institute of Bioscience and Biotechnology, 52 Oeundong, Yusong, Daejeon 305-333, Republic of Korea
2 Department of Food Science and Technology, Chungnam University, Daejeon 305-764, Republic of Korea
Correspondence
Chang-Jin Kim
changjin{at}kribb.re.kr
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7c, C19 : 08c cyclo and C16 : 0. The DNA G+C content was 70 mol% and the predominant ubiquinone was Q-9. Phylogenetic analysis based on 16S rRNA gene sequences showed that strain SS20T belonged to the genus Halomonas. The levels of 16S rRNA gene sequence similarity to the type strains of Halomonas species were in the range 93·0–97·5 %. The levels of DNA–DNA relatedness between strain SS20T and the type strains of phylogenetically closely related Halomonas species were in the range 5·3–12·3 %. On the basis of physiological and molecular properties, strain SS20T represents a novel species of the genus Halomonas, for which the name Halomonas koreensis sp. nov. is proposed. The type strain is SS20T (=KCTC 12127T=JCM 12237T).
Jee-Min Lim and Jung-Hoon Yoon contributed equally to this work. 
Published online ahead of print on 7 May 2004 as DOI 10.1099/ijs.0.63194-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain SS20T is AY382579.
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-Proteobacteria includes four genera of halophilic bacteria, Halomonas, Chromohalobacter, Alcanivorax and Cobetia, and two genera of non-halophilic bacteria, Zymobacter and Carnimonas (Arahal et al., 2001
, 2002a; Dobson & Franzmann, 1996; Yakimov et al., 1998). Halomonas was described as comprising Gram-negative, halotolerant, aerobic bacteria capable of growing over a wide range of salt concentrations. Moderately halophilic bacteria are abundant in saline habitats, and a number of Halomonas species have been isolated from different terrestrial and aquatic saline environments, mainly salterns, estuarine water, salt lakes, salty foods, sea ice and deep-sea hydrothermal vent environments, in the last few years (Baumann et al., 1983; Mellado et al., 1995; Romanenko et al., 2002; Vreeland et al., 1980; Yoon et al., 2002; Reddy et al., 2003; Kaye et al., 2004). Furthermore, this group of bacteria has great biotechnological potential for the production of compatible solutes or hydrolytic enzymes (Margesin & Schinner, 2001; García et al., 2004).
The features of these moderately halophilic bacteria are too heterogeneous to justify their placement in the single genus Halomonas, and the descriptions of some of the species do not match the emended genus description (Romanenko et al., 2002). In addition, the genus Halomonas has an unusually wide range of G+C contents (about 52–68 mol%; Arahal et al., 2002b). Therefore some researchers have suggested that it might become possible to split the genus Halomonas into two or more groups (Arahal et al., 2002b; Romanenko et al., 2002).
During screening of halophilic micro-organisms, a Gram-negative, moderately halophilic, rod-shaped bacterium (SS20T) with a DNA G+C content of 70 mol% was isolated from a solar saltern in Korea. The aim of this study was to determine the taxonomic status of this organism: we describe this bacterium, strain SS20T, as the type strain of a novel species designated Halomonas koreensis sp. nov.
Strain SS20T was isolated from a solar saltern in the Dangjin area of the Yellow Sea in Korea. For isolation, soil samples were diluted serially, spread on marine agar 2216 (MA) (Difco) with the addition of 10 % (w/v) NaCl (final concentration, 11·94 % NaCl, w/v) and incubated for 3 days at 35 °C. Isolate SS20T was routinely grown aerobically on MA for 3 days at 35 °C except where indicated otherwise. Requirement for, and tolerance of, NaCl were determined in nutrient broth (3·0 g beef extract l–1, 5·0 g peptone l–1; Difco) supplemented with modified artificial sea water [ASW: 0–30 % (w/v) NaCl, 5·94 g MgSO4.7H2O l–, 4·53 g MgCl2.6H2O l–, 0·64 g KCl l– and 1·3 g CaCl2 l–]. Growth was tested at different temperatures (4–55 °C) and pH values (5·0–10·0) in nutrient broth with the addition of ASW containing 7 % (w/v) NaCl. Growth was monitored by measuring the optical density at 600 nm.
Cell morphology was studied using phase-contrast microscopy and transmission electron microscopy. The flagellum type was examined by transmission electron microscopy using cells from the exponential growth phase. Cells were mounted on Formvar-coated copper grids and negatively stained with 1 % potassium phosphotungstate (pH 7·0). Grids were examined in a Phillips 201 transmission electron microscope operated at 80 kV.
For quantitative analysis of whole-cell fatty acids, strain SS20T was cultivated on either MA or MA with the addition of 5 % (w/v) NaCl for 3 days at 35 °C. Fatty acid methyl esters were analysed by GC/MS according to the instructions of the Microbial Identification System (MIDI; Microbial ID).
Catalase activity was determined by bubble production in 3 % (v/v) aqueous hydrogen peroxide solution. Oxidase activity, nitrate reduction and hydrolysis of aesculin, casein, starch, Tween 80, urea, hypoxanthine, tyrosine, gelatin and xanthine were determined according to methods described previously (Cowan & Steel, 1965; Lanyi, 1987). Other physiological tests were carried out using the API 20 test kits (bioMérieux) according to the manufacturer's instructions, except that the cultured cells were suspended in ASW with 3 % (w/v) NaCl.
Isoprenoid quinones were analysed as described by Komagata & Suzuki (1987) using HPLC apparatus fitted with a reversed-phase column (GROM-SIL 100 ODS-2FE; Chromalytic Technology). Methanol/2-propanol (2 : 1, v/v) was used as the mobile phase and quinones were detected at 270 nm. The G+C content (mol%) was determined by reverse-phase HPLC using the method of Tamaoka & Komagata (1984).
DNA–DNA hybridization was carried out fluorometrically according to the method of Ezaki et al. (1989), using photobiotin-labelled DNA probes and microdilution wells. Chromosomal DNA was isolated and purified according to the method described by Yoon et al. (1996), except that ribonuclease T1 was used together with ribonuclease A. Halomonas alimentaria JCM 10888T, Halomonas elongata DSM 2581T, Halomonas maura DSM 13445T, Halomonas pacifica KCTC 2683T and Halomonas salina DSM 5928T were used as reference strains for DNA–DNA hybridization. Reference strains were grown in marine broth (Difco) at appropriate temperatures.
The 16S rRNA gene was amplified by PCR using the Eubac 27F and 1492R primers (DeLong, 1992) and PCR products were purified using the QIAquick PCR purification kit (Qiagen). The purified PCR product was sequenced using the ABI PRISM BigDye Terminator cycle sequencing kit and an Applied Biosystems model 310 automatic DNA sequencer. The sequence data were assembled using SeqMan (DNASTAR) and were compared with available 16S rRNA gene sequences from GenBank using the BLAST program (NCBI) to determine the approximate phylogenetic affiliation. The 16S rRNA gene sequence of strain SS20T was aligned with those of Halomonas species and some other related taxa by using the CLUSTAL W software (Thompson et al., 1994). Sequence similarity values were computed using SIMILARITY MATRIX version 1.1 (Ribosomal Database Project II; http://rdp.cme.msu.edu/html/analyses.html). Evolutionary distance matrices were calculated using the algorithm of the Kimura two-parameter model (Kimura, 1980) with the DNADIST program within the PHYLIP software package, version 3.6 (Felsenstein, 2002). Phylogenetic trees were constructed using two different methods, the maximum-likelihood method (Felsenstein, 1981) and the neighbour-joining method (Saitou & Nei, 1987) available in the PHYLIP software package. To evaluate the stability of the phylogenetic tree, a bootstrap analysis (1000 replications) was performed with the SEQBOOT, DNADIST, NEIGHBOR and CONSENSE programs in the PHYLIP package.
Strain SS20T grew on nutrient agar supplemented with ASW, but not on nutrient agar (Difco) with just NaCl. Strain SS20T on MA medium formed creamy, smooth, glistening and circular/slightly irregular colonies. Strain SS20T grew at salt concentrations in the range 1–20 % (w/v) NaCl. Growth of the strain was consistent at various salinities ranging from 1 to 12 % (w/v) NaCl. Growth occurred from pH 5·5 to 10 (optimum, pH 7·0–8·0) in nutrient broth containing 7 % (w/v) salts. Growth was observed at temperatures between 10 and 47 °C, having an optimum growth temperature of 35 °C. Strain SS20T was a Gram-negative, non-spore-forming, short rod 0·8–1·0 µm wide and 1·8–2·2 µm long. Cells were motile, each cell having several flagella (Fig. 1). Strain SS20T showed oxidase- and catalase-positive reactions. It hydrolysed hypoxanthine, urea and L-tyrosine, but hydrolysis of aesculin, casein, gelatin, starch, Tween 80 and xanthine was not observed. The strain reduced nitrate to nitrite. It produced acids from D-glucose and glycerol, but not from L-arabinose, D-fructose, D-mannose, arbutin, D-salicin, maltose, 
-D-lactose, D-melibiose, sucrose, D-trehalose, adonitol, D-xylose, D-galactose, D-mannitol or D-ribose. The phenotypic characteristics of strain SS20T are summarized and compared with those of the type strains of closely related Halomonas species in Table 1.
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7c, C 19 : 08c cyclo and C16 : 0 (Table 2). The fatty acid composition on MA was slightly different from that on MA supplemented with 5 % NaCl (w/v), as reported previously (Arahal et al., 2001; Bouchotroch et al., 2001; Franzmann & Tindall, 1990; Valderrama et al., 1998; Yoon et al., 2001, 2002). However, the major fatty acid profile of strain SS20T was similar to those of other members of the genus Halomonas, but was distinguishable from that of the genus Zymobacter, the closest phylogenetic neighbour (Arahal et al., 2001; Bouchotroch et al., 2001; Franzmann & Tindall, 1990; Okamoto et al., 1993; Yoon et al., 2002).
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). However, in agreement with the fatty acid profiles, phylogenetic analysis based on the nearly complete 16S rRNA gene sequence (1399 nt) showed that strain SS20T was positioned within the radiation of Halomonas species and formed a distinct phyletic line within a diffuse subclade of the genus in the neighbour-joining analysis (Fig. 2) as well as according to the maximum-likelihood method (data not shown). In addition, strain SS20T displayed some phenotypic properties that were different from those of related Halomonas species (Table 1
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). The levels of 16S rRNA gene sequence similarity between strain SS20T and H. pacifica DSM 4742T, H. salina ATCC 49509T, H. alimentaria KCCM 41042T, H. maura CECT 5298T, H. elongata ATCC 33173T, H. halophila DSM 4770T, H. eurihalina ATCC 49336T and H. halmophila ATCC 19717T were 97·5, 97·2, 97·2, 97·1, 96·8, 96·5, 96·0 and 95·9 %, respectively. DNA–DNA relatedness between strain SS20T and the type strains of closely related Halomonas species with high 16S rRNA gene sequence similarities was assessed. The values obtained were 10·8, 8·5, 11·2, 12·3, 5·5, 5·3, 7·5 and 7·8 % with H. pacifica, H. salina, H. alimentaria, H. maura, H. elongata, H. eurihalina, H. halmophila and H. halophila, respectively; these values are too low to allocate strain SS20T to any species within the genus Halomonas (Wayne, 1994). Because some researchers have suggested that the genus Halomonas could be split into several genera, strain SS20T may require reclassification in the future. On the basis of the phenotypic and molecular properties that have been reported to date, we propose that strain SS20T should be assigned to a novel species of the genus Halomonas, Halomonas koreensis sp. nov.
Description of Halomonas koreensis sp. nov.
Halomonas koreensis (ko.re.en'sis. N.L. fem. adj. koreensis pertaining to Korea).
Cells are Gram-negative, non-spore-forming, short rods measuring 0·8–1·0 µm in width and 1·8–2·2 µm in length. Oxidase- and catalase-positive. Cells are motile, each cell having several flagella. Colonies are creamy, smooth, glistening and circular/slightly irregular. Grows at salinities in the range 1–20 % (w/v) NaCl. Good growth at 1–12 % (w/v) NaCl. No growth occurs in the absence of salts. Grows between 10 and 47 °C (optimum, 35 °C) and from pH 5·5 to 10 (optimum, pH 7·0–8·0). Hypoxanthine, urea and L-tyrosine are hydrolysed. Aesculin, casein, gelatin, starch, Tween 80 and xanthine are not hydrolysed. Nitrate is reduced to nitrite. Acid is produced from D-glucose and glycerol, but not from L-arabinose, D-fructose, D-mannose, arbutin, D-salicin, maltose, -D-lactose, D-melibiose, sucrose, D-trehalose, adonitol, D-xylose, D-galactose, D-mannitol or D-ribose. The predominant isoprenoid quinone is Q-9. The major fatty acids are C18 : 17c, C19 : 08c cyclo and C16 : 0. The DNA G+C content is 70 mol%.
The type strain is SS20T (=KCTC 12127T=JCM 12237T), isolated from a solar saltern at Sungumi in Korea.
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ACKNOWLEDGEMENTS |
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