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1 Korea Research Institute of Bioscience and Biotechnology (KRIBB), PO Box 115, Yusong, Taejon, Korea
2 Department of Food and Life Science, Sungkyunkwan University, Chunchun-dong 300, Jangan-gu, Suwon, Korea
3 National Research Laboratory of Molecular Ecosystematics, Institute of Probionic, Probionic Corporation, Bio-venture Center, KRIBB, Yusong, Taejon, Korea
Correspondence
Yong-Ha Park
yhpark{at}kribb.re.kr
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based on L-orn–D-Asp. The predominant menaquinone found in strain HSL-3T was menaquinone-7 (MK-7). Strain HSL-3T had a cellular fatty acid profile containing large amounts of branched fatty acids; the major fatty acids were anteiso-C15 : 0, iso-C15 : 0 and iso-C16 : 0. The DNA G+C content of strain HSL-3T was 45 mol%. Phylogenetic analysis based on 16S rDNA sequences showed that strain HSL-3T falls within the radiation of the cluster comprising Halobacillus species. Strain HSL-3T exhibited levels of 16S rDNA similarity of 97·4–98·4 % to the type strains of Halobacillus species. Levels of DNA–DNA relatedness between strain HSL-3T and the type strains of all validly named Halobacillus species were in the range 7·3–9·2 %. On the basis of phenotypic and phylogenetic data and the genomic distinctiveness, strain HSL-3T (=KCCM 41590T=JCM 11546T) should be placed in the genus Halobacillus as the type strain of a novel species, for which the name Halobacillus salinus sp. nov. is proposed.
The GenBank accession number for the 16S rDNA sequence of strain HSL-3T is AF500003.
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). Developments in molecular biological methods and chemical analysis revealed the taxonomic heterogeneity of the genus Bacillus (Ash et al., 1991; Priest, 1981; Slepecky & Hemphill, 1991; Stackebrandt & Liesack, 1993). In particular, 16S rRNA sequence analyses revealed the presence of several phylogenetically distinct lineages within the genus Bacillus (Ash et al., 1991; Nielsen et al., 1994). Subsequently, some phylogenetic groups have been proposed as the new genera Alicyclobacillus (Wisotzkey et al., 1992), Aneurinibacillus, Brevibacillus (Shida et al., 1996), Marinibacillus (Yoon et al., 2001), Paenibacillus (Ash et al., 1993), Salibacillus (Wainø et al., 1999) and Virgibacillus (Heyndrickx et al., 1998). In addition, some aerobic or facultatively anaerobic, endospore-forming rods have been described as the new genera Amphibacillus (Niimura et al., 1990), Halobacillus (Spring et al., 1996), Gracilibacillus (Wainø et al., 1999) and Jeotgalibacillus (Yoon et al., 2001). Nevertheless, there are few clear-cut differences in phenotypic, and particularly chemotaxonomic, properties among these genera, with some exceptions, including the genera belonging to Bacillus rRNA group 2 (Niimura et al., 1990; Shida et al., 1997; Wainø et al., 1999; Yoon et al., 2001). Most of them are characterized chemotaxonomically by having MK-7 as the predominant menaquinone, meso-diaminopimelic acid or L-lysine at position 3 of the peptide subunit of the peptidoglycan and one or more of anteiso-C15 : 0, iso-C15 : 0, C16 : 0 and iso-C16 : 0 as the major fatty acids.
The genus Halobacillus is clearly differentiated from other related genera in the cell-wall peptidoglycan type; members of the genus have peptidoglycan based on L-orn–D-Asp (Spring et al., 1996), whereas other related genera contain meso-diaminopimelic acid or L-lysine at position 3 of the cell-wall peptidoglycan (Shida et al., 1997; Wainø et al., 1999; Yoon et al., 2001). The genus Filobacillus, which has been described recently, contains L-ornithine at position 3 of the cell-wall peptidoglycan but has peptidoglycan based on L-orn–D-Glu (Schlesner et al., 2001). The genus Halobacillus was proposed with two novel species, Halobacillus litoralis and Halobacillus trueperi, as well as Sporosarcina halophila, which was transferred to the genus as Halobacillus halophilus (Spring et al., 1996). Since then, no further Halobacillus species have been proposed. Recently, a halophilic bacterial strain, HSL-3T, was isolated from a salt lake on the coast of the East Sea in Korea. This organism was considered to be a member of the genus Halobacillus from the results of preliminary study based on partial 16S rDNA sequence comparison. Accordingly, the aim of the present study was to determine the exact taxonomic position of strain HSL-3T with a combination of phenotypic properties, detailed phylogenetic analysis based on nearly complete 16S rDNA sequence and genomic relatedness. On the basis of the data presented below, strain HSL-3T should be placed in the genus Halobacillus as a novel species, for which we propose the name Halobacillus salinus sp. nov.
Strain HSL-3T was isolated from a salt lake near Hwajinpo beach on the East Sea in Korea by the dilution-plating technique on marine agar 2216 (MA) (Difco). For investigation of morphological and physiological characteristics, strain HSL-3T was generally cultivated on MA and in marine broth 2216 (MB) (Difco) at 30 °C. Cell biomass of strain HSL-3T for analysis of the cell wall and menaquinones and for DNA extraction was obtained from MB cultures at 30 °C. Strain HSL-3T was cultivated on a horizontal shaker at 150 r.p.m. and broth cultures were checked microscopically for purity before being harvested by centrifugation. For fatty acid methyl ester (FAME) analysis, cell mass of strain HSL-3T and reference strains was obtained from agar plates after 4 days cultivation at 30 °C on MA and MA supplemented with approximately 8·1 % (w/v) NaCl. The reference strains were H. halophilus KCTC 3685T, H. litoralis KCTC 3687T and H. trueperi KCTC 3686T. Cell morphology was examined by light microscopy and transmission electron microscopy (TEM). Flagellation type was examined by TEM using cells from exponentially growing culture. The cells were negatively stained with 1 % (w/v) phosphotungstic acid and after air drying, the grids were examined by using a model CM-20 transmission electron microscope (Philips). Gram reaction was determined using the bioMérieux Gram Stain kit according to the manufacturer's instructions. Catalase activity was determined by bubble production in a 3 % (v/v) hydrogen peroxide solution. Oxidase activity was determined by oxidation of 1 % p-aminodimethylaniline oxalate. Urease activity was determined as described by Cowan & Steel (1965) with the modification that 3 % (w/v) NaCl was added. Hydrolysis of casein, starch and Tween 80 was determined as described by Cowan & Steel (1965). Hydrolysis of aesculin and gelatin and nitrate reduction were determined as described by Lanyi (1987) with the modification that 3 % (w/v) NaCl was added. Hydrolysis of hypoxanthine, tyrosine and xanthine was examined on MA with concentrations of substrates described previously (Cowan & Steel, 1965). Acid production from carbohydrates was determined as described by Leifson (1963). Growth under anaerobic conditions was determined after incubation in an anaerobic chamber with MA that had been prepared anaerobically. Growth at various NaCl concentrations was investigated on MA and in MB. Growth at various temperatures was measured on MA at 4–55 °C.
Preparation of cell wall and determination of peptidoglycan structure were carried out by the methods described by Schleifer & Kandler (1972) with the modification that TLC on cellulose sheets was used instead of paper chromatography. Menaquinones were analysed as described previously (Komagata & Suzuki, 1987) using reverse-phase HPLC. For quantitative analysis of cellular fatty acid compositions, a loop of cell mass was harvested and FAMEs were prepared and identified following the instructions of the Microbial Identification System (MIDI). Chromosomal DNA was isolated and purified according to the method described previously (Yoon et al., 1996), with the exception that RNase T1 was used together with RNase A. The G+C content was determined by the method of Tamaoka & Komagata (1984). DNA was hydrolysed and the resultant nucleotides were analysed by reverse-phase HPLC.
16S rDNA was amplified by PCR using two universal primers as described previously (Yoon et al., 1998). The PCR product was purified with a QIAquick PCR purification kit (Qiagen). Sequencing of the purified 16S rDNA was performed using an ABI PRISM BigDye Terminator cycle sequencing ready reaction kit (Applied Biosystems) as recommended by the manufacturer. The purified sequencing reaction mixtures were electrophoresed automatically using an Applied Biosystems model 377 automatic DNA sequencer. Alignment of sequences was carried out with CLUSTAL W software (Thompson et al., 1994). Gaps at the 5' and 3' ends of the alignment were omitted from further analysis. Phylogenetic trees were inferred by using three tree-making algorithms, the neighbour-joining (Saitou & Nei, 1987), maximum-likelihood (Felsenstein, 1981) and maximum-parsimony (Kluge & Farris, 1969) methods in the PHYLIP package (Felsenstein, 1993). Evolutionary distance matrices for the neighbour-joining method were calculated with the algorithm of Jukes & Cantor (1969) with the DNADIST program. The stability of relationships was assessed by a bootstrap analysis based on 1000 resampling of the neighbour-joining dataset by using the programs SEQBOOT and CONSENSE of the PHYLIP package. DNA–DNA hybridization was performed fluorometrically by the method of Ezaki et al. (1989) using photobiotin-labelled DNA probes and microdilution wells. Hybridization was performed with five replications for each sample. Of the values obtained, the highest and lowest values in each sample were excluded and the remaining three values were used for calculation of similarity values. DNA relatedness values are the means of three values.
Strain HSL-3T was Gram-positive but changed to Gram-variable as cultures aged. Cells of strain HSL-3T were rods, measuring approximately 0·7–1·1 µm wide by 1·5–4·0 µm long in 3 day cultures at 30 °C on MA (Fig. 1). The cells showed no difference in their morphology on MA or MA containing approximately 10 % NaCl. Cells of strain HSL-3T were motile by means of peritrichous flagella. Ellipsoidal endospores were observed at central or subterminal positions in swollen sporangia. Colonies of strain HSL-3T were smooth, circular to slightly irregular, slightly raised, pale orange-yellow in colour and 2–3 mm in diameter after 3 days on MA. Strain HSL-3T grew optimally at 30–37 °C; it grew at 10 and 45 °C but not at 4 °C or temperatures above 46 °C. Strain HSL-3T grew well in the pH range 6·0–8·0, with an optimum of approximately 7·0, and growth was observed at pH 5·0 but not at pH 4·5. Strain HSL-3T grew optimally in the presence of 2–10 % (w/v) NaCl, and showed poor growth in the absence of NaCl. It grew in the presence of 23 % NaCl but not in the presence of more than 24 % NaCl. Strain HSL-3T did not grow under anaerobic conditions on MA. Strain HSL-3T showed catalase and oxidase activities but no urease activity. Aesculin, casein and Tween 80 were hydrolysed and no hydrolysis of hypoxanthine, starch, tyrosine or xanthine was observed. Nitrate was not reduced to nitrite. Acid was produced from D-cellobiose, D-fructose, D-glucose, maltose, D-mannitol, D-mannose, sucrose and D-trehalose and produced weakly from D-galactose, D-melezitose and melibiose. Phenotypic properties of strain HSL-3T and Halobacillus species are summarized in Table 1.
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, based on L-orn–D-Asp, as described by Schleifer & Kandler (1972). The predominant menaquinone found in strain HSL-3T was unsaturated menaquinone with seven isoprene units (MK-7). The cellular fatty acid profile of strain HSL-3T is represented in Table 2, together with those of the type strains of the three Halobacillus species. Strain HSL-3T and the type strains of the three Halobacillus species were found to have similar fatty acid profiles when they were cultivated on either MA or MA containing approximately 10 % NaCl (Table 2). Strain HSL-3T had a cellular fatty acid profile containing large amounts of branched fatty acids, with anteiso-C15 : 0, iso-C15 : 0 and iso-C16 : 0 as the major fatty acids (Table 2). The DNA G+C content of the strain was 45 mol%.
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). In the tree based on the neighbour-joining algorithm, strain HSL-3T clustered with the clade comprising H. litoralis and H. trueperi, and the relationship between this cluster and H. halophilus was supported by bootstrap analysis at a confidence level of 99·0 % (Fig. 2). Strain HSL-3T exhibited levels of 16S rDNA similarity of 97·4, 98·4 and 98·2 %, respectively, to the type strains of H. halophilus, H. litoralis and H. trueperi. Levels of 16S rDNA similarity between strain HSL-3T and other species used in the phylogenetic analysis were less than 94·6 % (Fig. 2). DNA–DNA hybridization was performed to determine the genomic relatedness between strain HSL-3T and the type strains of the three Halobacillus species. Strain HSL-3T exhibited mean levels of DNA–DNA relatedness of 7·3, 8·5 and 9·2 %, respectively, with H. halophilus KCTC 3685T, H. litoralis KCTC 3687T and H. trueperi KCTC 3686T when the DNAs of the four strains were used separately as labelled DNA probes for cross-hybridization.
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), although there are a few differences in their cellular fatty acid compositions (Table 2
). In particular, the cell-wall peptidoglycan type, based on L-orn–D-Asp, is a key marker that differentiates strain HSL-3T and the genus Halobacillus from other genera of aerobic or facultative anaerobic, endospore-forming rods. Therefore, in view of the combined morphological, chemotaxonomic and phylogenetic data, it is evident that strain HSL-3T belongs to the genus Halobacillus.
Strain HSL-3T is similar to Halobacillus species in its morphological and most of its physiological characteristics (Table 1). However, there are some minor differences between strain HSL-3T and Halobacillus species, including tolerance of NaCl, temperature and pH for growth, the ability to hydrolyse some substrates and acid production from carbohydrates (Table 1). Strain HSL-3T shows growth in the presence of NaCl up to 23 %, whereas H. halophilus, H. litoralis and H. trueperi respectively show growth in the presence of NaCl up to 15, 25 and 30 % (Claus et al., 1983; Spring et al., 1996). While strain HSL-3T can grow at temperatures up to 45 °C, the other Halobacillus species cannot grow at 45 °C (Claus et al., 1983; Spring et al., 1996). Strain HSL-3T and the other Halobacillus species show differences in growth at pH 5·5 and 5·0. It is noteworthy that the fatty acid profile of strain HSL-3T also differs from those of the type strains of the other Halobacillus species in the proportions of some fatty acids (Table 2). These fatty acid profiles did not show conspicuous differences on MA containing 2 or 10 % NaCl. Levels of DNA–DNA relatedness are low enough to categorize strain HSL-3T as a distinct species within the genus Halobacillus (Wayne et al., 1987). Therefore, differences in some phenotypic characteristics and genetic distinctiveness together indicate that strain HSL-3T is a member of a species separate from previously described Halobacillus species.
On the basis of the data presented above, strain HSL-3T should be placed in the genus Halobacillus as a novel species, for which we propose the name Halobacillus salinus sp. nov.
Description of Halobacillus salinus sp. nov.
Halobacillus salinus (sa'li.nus. N.L. adj. salinus salted, salty).
Cells are rods, 0·7–1·1 µm wide by 1·5–4·0 µm long in 3 day cultures at 30 °C on MA. Gram-positive but Gram-variable in old cultures. Motile by means of peritrichous flagella. Central or subterminal ellipsoidal endospores are observed in swollen sporangia. Colonies are smooth, circular to slightly irregular, slightly raised, pale orange-yellow in colour and 2–3 mm in diameter after 3 days on MA. The optimal temperature for growth is 30–37 °C. Growth occurs at 10 and 45 °C but not at 4 °C or temperatures above 46 °C. The optimal pH for growth is around pH 7·0 and no growth is observed at pH 4·5. Grows optimally in the presence of 2–10 % (w/v) NaCl and growth is poor in the absence of NaCl. Growth occurs in the presence of 23 % NaCl but not 24 % NaCl. Growth does not occur under anaerobic conditions on MA. Catalase- and oxidase-positive. Urease-negative. Aesculin, casein, gelatin and Tween 80 are hydrolysed. Hypoxanthine, starch, tyrosine and xanthine are not hydrolysed. Nitrate is not reduced to nitrite. Acid is produced from D-cellobiose, D-fructose, D-glucose, maltose, D-mannitol, D-mannose, sucrose and D-trehalose and produced weakly from D-galactose, D-melezitose and melibiose. Acid is not produced from adonitol, L-arabinose, lactose, myo-inositol, D-raffinose, L-rhamnose, D-ribose, D-sorbitol, stachyose or D-xylose. The cell wall contains peptidoglycan based on L-orn–D-Asp. The predominant menaquinone is MK-7. The major fatty acids are anteiso-C15 : 0, iso-C15 : 0 and iso-C16 : 0. The G+C content is 45 mol% (determined by HPLC).
The type strain, strain HSL-3T (=KCCM 41590T=JCM 11546T), was isolated from a salt lake near Hwajinpo beach on the East Sea in Korea.
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ACKNOWLEDGEMENTS |
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I. J. Carrasco, M. C. Marquez, X. Yanfen, Y. Ma, D. A. Cowan, B. E. Jones, W. D. Grant, and A. Ventosa Gracilibacillus orientalis sp. nov., a novel moderately halophilic bacterium isolated from a salt lake in Inner Mongolia, China. Int J Syst Evol Microbiol, March 1, 2006; 56(Pt 3): 599 - 604. [Abstract] [Full Text] [PDF]
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J.-H. Yoon, S.-J. Kang, C.-H. Lee, H. W. Oh, and T.-K. Oh Halobacillus yeomjeoni sp. nov., isolated from a marine solar saltern in Korea Int J Syst Evol Microbiol, November 1, 2005; 55(6): 2413 - 2417. [Abstract] [Full Text] [PDF]
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M. T. Garcia, V. Gallego, A. Ventosa, and E. Mellado Thalassobacillus devorans gen. nov., sp. nov., a moderately halophilic, phenol-degrading, Gram-positive bacterium Int J Syst Evol Microbiol, September 1, 2005; 55(5): 1789 - 1795. [Abstract] [Full Text] [PDF]
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W. Y. Liu, J. Zeng, L. Wang, Y. T. Dou, and S. S. Yang Halobacillus dabanensis sp. nov. and Halobacillus aidingensis sp. nov., isolated from salt lakes in Xinjiang, China Int J Syst Evol Microbiol, September 1, 2005; 55(5): 1991 - 1996. [Abstract] [Full Text] [PDF]
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J.-M. Lim, C. O. Jeon, D.-J. Park, H.-R. Kim, B.-J. Yoon, and C.-J. Kim Pontibacillus marinus sp. nov., a moderately halophilic bacterium from a solar saltern, and emended description of the genus Pontibacillus Int J Syst Evol Microbiol, May 1, 2005; 55(3): 1027 - 1031. [Abstract] [Full Text] [PDF]
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C. O. Jeon, J.-M. Lim, J.-C. Lee, G. S. Lee, J.-M. Lee, L.-H. Xu, C.-L. Jiang, and C.-J. Kim Lentibacillus salarius sp. nov., isolated from saline sediment in China, and emended description of the genus Lentibacillus Int J Syst Evol Microbiol, May 1, 2005; 55(3): 1339 - 1343. [Abstract] [Full Text] [PDF]
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P.-G. Ren and P.-J. Zhou Salinibacillus aidingensis gen. nov., sp. nov. and Salinibacillus kushneri sp. nov., moderately halophilic bacteria isolated from a neutral saline lake in Xin-Jiang, China Int J Syst Evol Microbiol, March 1, 2005; 55(2): 949 - 953. [Abstract] [Full Text] [PDF]
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P.-G. Ren and P.-J. Zhou Tenuibacillus multivorans gen. nov., sp. nov., a moderately halophilic bacterium isolated from saline soil in Xin-Jiang, China Int J Syst Evol Microbiol, January 1, 2005; 55(1): 95 - 99. [Abstract] [Full Text] [PDF]
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J.-M. Lim, C. O. Jeon, S. M. Song, and C.-J. Kim Pontibacillus chungwhensis gen. nov., sp. nov., a moderately halophilic Gram-positive bacterium from a solar saltern in Korea Int J Syst Evol Microbiol, January 1, 2005; 55(1): 165 - 170. [Abstract] [Full Text] [PDF]
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