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1 Korea Research Institute of Bioscience and Biotechnology, 52 Oeundong, Yusong, Daejeon 305-333, Republic of Korea
2 Environmental Biotechnology National Core Research Center, Division of Environmental Biotechnology, Gyeongsang National University, 660-701, Korea
3 Yunnan Institute of Microbiology, Yunnan University, Kunming, Yunnan, 650091, P. R. China
Correspondence
Chang-Jin Kim
changjin{at}kribb.re.kr
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ABSTRACT |
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peptidoglycan with meso-diaminopimelic acid as the diagnostic diamino acid. The isolate showed Gram- and catalase-positive reactions and formed a terminal endospore with a swollen sporangium. The major cellular fatty acids were anteiso-C15 : 0, iso-C15 : 0, anteiso-C17 : 0 and iso-C16 : 0. The genomic DNA G+C content of the strain was 41·0 mol%. Comparative analysis of 16S rRNA gene sequences showed that strain BH163T formed a distinct line within the phyletic group classically defined as the genus Bacillus and was most closely related to the taxa [Bacillus] haloalkaliphilus DSM 5271T and Filobacillus milosensis DSM 13259T, with 16S rRNA gene sequence similarities of 95·9 and 94·5 %, respectively. On the basis of physiological and molecular properties, it is proposed that [Bacillus] haloalkaliphilus DSM 5271T is reclassified in the new genus Alkalibacillus as Alkalibacillus haloalkaliphilus gen. nov., comb. nov. Strain BH163T (=KCTC 3916T=DSM 16460T) was assigned as the type strain of the novel species Alkalibacillus salilacus.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain BH163T is AY671976.
An electron micrograph of strain BH163T and a table detailing cellular fatty acid compositions for strain BH163T and related type strains are available as supplementary material in IJSEM Online.
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). They are also metabolically diverse. Aerobic, spore-forming, moderately halophilic, Gram-positive rods are also taxonomically diverse and have been isolated from marine environments and related habitats. They were originally assigned to the genus Bacillus, but they have been reclassified as new genera by the application of molecular methods and improved phenotypic approaches (Heyndrickx et al., 1999; Spring et al., 1996; Wainø et al., 1999; Yoon et al., 2001, 2004).
In the course of screening halophilic bacteria, an aerobic Gram-positive, obligately halophilic bacterium, designated strain BH163T, was isolated from soil sediment of a salt lake. Comparative analysis of 16S rRNA gene sequences indicated that the closest relative of the strain was [Bacillus] haloalkaliphilus WN13T (95·9 % 16S rRNA gene sequence similarity), which was classified as a novel species within the genus Bacillus (Fritze, 1996). However, we found that strain WN13 should be reclassified in a new genus on the basis of phylogenetic and phenotypic characteristics. Therefore, we propose the reclassification of [Bacillus] haloalkaliphilus in the new genus Alkalibacillus as Alkalibacillus haloalkaliphilus gen. nov., comb. nov., with WN13T as the type strain. A novel species, Alkalibacillus salilacus sp. nov., type strain BH163T, is also described.
Strain BH163T was isolated from soil sediment of Ai-Ding Lake in Xin-jiang province in China. Ai-Ding Lake is a typical chloride-sulphate saline lake with a neutral pH and a 20–26 % (w/v) salt concentration. Surface soil sediment was sampled from a shallow area of the lakeside. To isolate halophilic bacteria, soil sediment was serially diluted, spread on marine agar 2216 (MA; Difco) supplemented with 15 % (w/v) NaCl [final concentration 16·94 % NaCl (w/v)] and incubated for 5 days at 28 °C. Requirement for and tolerance of NaCl were determined in tryptic soy broth (TSB) supplemented with modified artificial sea water [ASW; 0–30 % (w/v) NaCl, 5·94 g MgSO4.7H2O, 4·53 g MgCl2.6H2O, 0·64 g KCl and 1·3 g CaCl2 per litre]. The strain was routinely grown aerobically on MA containing 10 % (w/v) NaCl for 3 days at 30 °C except where indicated otherwise. Anaerobic growth was determined by incubation in an anaerobic chamber at 30 °C for 5 days on MA containing 10 % (w/v) NaCl. Optimum growth was tested at different temperatures (4–55 °C) on MA containing 10 % (w/v) NaCl and at different pH values (5·0–10·0) in TSB supplemented with ASW containing 10 % (w/v) NaCl.
Cell morphology was studied using light and transmission electron microscopy (TEM). Motility was observed at 24 and 48 h in agar-coated wet mounts using a light microscope (Nikon E600). Each agar-coated wet mount was prepared by placing 10 µl culture under a cover glass on a glass slide that had previously been coated with a film of 0·5 % (w/v) agarose (Cambrex) in distilled water and air-dried. For visualization of flagella, cells were mounted on Formvar-coated copper grids (Electron Microscopy Science) and negatively stained with 2 % (w/v) uranyl acetate for 15 s and then subjected to TEM (JEM-1010; JEOL). Endospores were stained according to the method of Schaeffer-Fulton (Smibert & Krieg, 1981).
Catalase activity was determined by the production of oxygen bubbles in 3 % (v/v) aqueous hydrogen peroxide solution. Oxidase activity was tested by the oxidation of 1 % (w/v) tetramethyl-p-phenylenediamine (Merck). Hydrolysis of aesculin, casein, starch, Tween 80, urea, hypoxanthine, tyrosine, gelatin and xanthine was determined on MA according to previously described methods (Cowan & Steel, 1965; Lanyi, 1987; Smibert & Krieg, 1994). Nitrate reduction was performed according to Lanyi (1987). Acid production from carbohydrates was tested as described by Leifson (1963); all suspension media were supplemented with ASW containing 10 % (w/v) NaCl.
GC analysis of fatty acid methyl esters was performed with cells grown on MA containing 5 or 10 % (w/v) NaCl for 3 days at 30 °C according to the manufacturer's instructions for the Microbial Identification System (MIDI; Microbial ID). Preparation of cell walls from the test strain and analyses of peptidoglycan structures were carried out using the methods described by Schleifer (1985) with the modification that TLC was performed on cellulose sheets instead of using paper chromatography. Isoprenoid quinones were analysed as described by Komagata & Suzuki (1987) using an HPLC fitted with a reverse-phase column (GROM-SIL 100 ODS-2FE; GROM). The DNA G+C content of strain BH163T was determined by reverse-phase HPLC according to Tamaoka & Komagata (1984).
The 16S rRNA gene was amplified by PCR using Eubac 27F and 1492R primers (DeLong, 1992) and sequenced. The resulting sequences were compared with available 16S rRNA gene sequences from GenBank using the BLAST program (http://www.ncbi.nlm.nih.gov/blast/) to determine the approximate phylogenetic affiliation and then aligned with closely related members by using CLUSTAL W software (Thompson et al., 1994). Sequence similarity values were computed using the Similarity Matrix tool, version 1.1 (Ribosomal Database Project II; http://35.8.164.52/html/; Cole et al., 2003). Gaps at the 5'- and 3'-ends of the alignment were omitted from further analyses. The phylogenetic trees were constructed using three different methods, neighbour-joining (Saitou & Nei, 1987), maximum-likelihood (Felsenstein, 1981) and maximum-parsimony (Fitch, 1971), using algorithms available in PHYLIP software, version 3.6 (Felsenstein, 2002). For the neighbour-joining method, evolutionary distance matrices were calculated according to the Kimura two-parameter model (Kimura, 1980). 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 software package.
Strain BH163T showed moderate halophilic properties, growing in media containing 5–20 % (w/v) NaCl; optimum growth occurred in media with 10–12 % (w/v) NaCl. Colonies of the strain were cream, smooth, low-convex and circular/slightly irregular on MA containing 10 % (w/v) NaCl. Growth was observed at temperatures between 15 and 40 °C, with an optimum growth temperature of 30 °C. Cells of the isolate were slender, strictly aerobic and motile rods (width of 0·4–0·5 µm and length 1·6–3·0 µm) with peritrichous flagella (see Supplementary Fig. S1 in IJSEM Online).
Strain BH163T grew well in the slightly alkaline conditions of pH 7·0–9·0 in TSB containing 10 % (w/v) NaCl; optimal growth was observed at pH 8·0. [Bacillus] haloalkaliphilus DSM 5271T, the previously determined closest relative based on 16S rRNA gene sequence similarities, also grows at concentrations of up to 25 % NaCl and shows good growth at relatively high pH (pH 9·7) (Fritze, 1996). The isolate produced a spherical terminal endospore with a swollen sporangium, as found in the phylogenetically close species [Bacillus] haloalkaliphilus and Filobacillus milosensis. Growth was not observed after 5 days of incubation under anaerobic conditions at 30 °C on MA with 10 % (w/v) NaCl.
Strain BH163T was catalase-positive, oxidase-negative and reduced nitrate to nitrite. Gram reaction and KOH tests of cells from early and late growth phases were positive and negative, respectively. However, it has been reported that [Bacillus] haloalkaliphilus and F. milosensis show Gram-negative reactions despite having been described as Gram-positive bacteria by Fritze (1996) and Schlesner et al. (2001) and confirmed by our tests. The analysis of cell-wall peptidoglycan showed that strain BH163T possessed A1-type peptidoglycan with meso-diaminopimelic acid (m-DAP) as the diagnostic diamino acid, which was identical to that of [Bacillus] haloalkaliphilus. However, F. milosensis possesses the A4
-type peptidoglycan, L-orn–D-Glu, which clearly distinguishes strain BH163T from F. milosensis (Fritze, 1996; Schlesner et al., 2001).
The predominant isoprenoid quinone of strain BH163T was menaquinone-7 (MK-7) and the G+C content of genomic DNA was about 41 mol%. The cellular fatty acid profile of strain BH163T was characterized as containing saturated branched fatty acids such as anteiso-C15 : 0 (
39·7 %), iso-C15 : 0 (30·9 %), anteiso-C17 : 0 (11·8 %) and iso-C16 : 0 (8·9 %) on MA containing 10 % (w/v) NaCl, which was similar to that of [B.] haloalkaliphilus (Fritze, 1996). The fatty acid profiles on MA with 5 or 10 % (w/v) NaCl were similar (see Supplementary Table S1 in IJSEM Online). The cell-wall peptidoglycan, fatty acid profiles, major lipoquinone and DNA G+C content of strain BH163T were similar to those of [Bacillus] haloalkaliphilus and clearly distinguishable from those of F. milosensis within the group classically defined as the genus Bacillus (Fritze, 1996; Schlesner et al., 2001). The typical phenotypic and chemotaxonomic properties of strain BH163T are summarized and compared with those of phylogenetically related type relatives in Table 1.
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; Nielsen et al., 1994; Schlesner et al., 2001; Stackebrandt & Liesack, 1993). The phylogenetic analysis showed that the isolate formed a phyletic group with [Bacillus] haloalkaliphilus DSM 5271T in the neighbour-joining analysis (Fig. 1). The topologies of the phylogenetic trees built using the maximum-likelihood and maximum-parsimony algorithms were similar to that of the tree constructed by the neighbour-joining analysis (data not shown). The closest relative of strain BH163T was [Bacillus] haloalkaliphilus DSM 5271T with 95·9 % 16S rRNA gene sequence similarity, a level at which they can be considered to be in the same genus. However, strain BH163T shared low 16S rRNA gene sequence similarity of 94·5 and 94·2 % with two other close relatives, F. milosensis DSM 13259T and Tenuibacillus multivorans NBRC 100370T, respectively.
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Description of Alkalibacillus gen. nov.
Alkalibacillus (Al.ka.li.ba.cil'lus. N.L. n. alkali alkali; L. n. bacillus rod; N.L. masc. n. Alkalibacillus bacillus living under alkaline conditions).
Cells are Gram-variable, spore-forming rods. Catalase-positive. Urease-negative. Spherical endospores are formed terminally in swollen sporangia. Strictly aerobic and moderately halophilic. Cells are motile by means of peritrichous flagella. Cell-wall peptidoglycan is of the A1 type with meso-DAP as the diagnostic diamino acid. Major isoprenoid quinone is MK-7. DNA G+C content is 38–41 mol% (HPLC). Predominant cellular fatty acids are iso-C15 : 0, anteiso-C15 : 0 and anteiso-C17 : 0. Phylogenetically, the genus belongs to the family Bacillaceae. The type species of the genus is Alkalibacillus haloalkaliphilus (=DSM 5271T).
Description of Alkalibacillus haloalkaliphilus (Fritze 1996) comb. nov.
Alkalibacillus haloalkaliphilus (hal.o.al.ka.li'phi.lus. Gr. n. hals salt; N.L. n. alkali alkali; Gr. adj. philos loving; N.L. masc. adj. haloalkaliphilus loving briny and alkaline media).
Basonym: Bacillus haloalkaliphilus Fritze 1996.
Gram reaction is negative. Catalase- and oxidase-positive. Nitrate not reduced to nitrite. Cells are 0·3–0·5 µm wide and 3–8 µm long. On alkaline nutrient agar supplemented with 5–10 % (w/v) NaCl, colonies are cream white. In the presence of 20 % (w/v) NaCl, colonies are slightly yellowish. The major cellular fatty acids are the saturated branched chain fatty acids iso-C15 : 0 (48 %), anteiso-C15 : 0 (11 %), anteiso-C17 : 0 (11 %) and iso-C17 : 0 (6 %). A small amount (19 %) of unsaturated fatty acids is also present. Chemo-organotrophic. Does not grow (or grows only very poorly) in nutrient broth or on nutrient agar without NaCl. Mesophilic. Obligately alkaliphilic. No growth occurs at pH 7 and good growth occurs at pH 9·7. Hydrolysis of starch is weak and no, or only weak, hydrolysis of casein occurs. Gelatin and hippurate are hydrolysed. Pullulan, Tween 20, Tween 80 and 4-methylumbelliferone glucuronide are not hydrolysed. Egg yolk lecithinase and urease tests are negative. The DNA G+C content is 38·0 mol% (HPLC).
The type strain, WN13T (=DSM 5271T=ATCC 700606T=CIP 106702T=JCM 12303T=LMG 17943T), was isolated from alkaline, highly saline mud from Wadi Natrun, Egypt.
Description of Alkalibacillus salilacus sp. nov.
Alkalibacillus salilacus (sa.li.lac'us. L. n. sal salt; L. n. lacus lake; N.L. gen. masc. n. salilacus of a salt lake).
Colonies are cream, smooth, low-convex and circular/slightly irregular. Cells are approximately 0·4–0·5 µm wide and 1·6–3·0 µm long. Strictly aerobic, spore-forming, motile rod. Gram-positive. KOH test negative. Catalase-positive and oxidase-negative. Nitrate is reduced to nitrite. Growth occurs at 15–40 °C (optimum 30 °C), pH 7·0–9·0 (optimum pH 8·0) and 5–20 % (w/v) NaCl (optimum 10–12 %). Aesculin is hydrolysed. Hydrolysis of casein, starch, Tween 80, L-tyrosine, hypoxanthine, xanthine, gelatin and urea is not observed. Acids are produced from L-arabinose, D-ribose, 
-D-lactose and D-fructose, but not from D-glucose, maltose, glycerol, D-trehalose, D-xylose, L-rhamnose, adonitol, D-raffinose, D-mannitol, arbutin, D-salicin, D-melibiose or D-mannose. DNA G+C content is 41·0 mol% (HPLC). Predominant cellular fatty acids are anteiso-C15 : 0, iso-C15 : 0, anteiso-C17 : 0 and iso-C16 : 0.
The type strain, BH163T (=KCTC 3916T=DSM 16460T), was isolated from a salt lake in the Xin-jiang province of China.
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ACKNOWLEDGEMENTS |
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B. S. Chung, S. H. Ryu, M. Park, Y. Jeon, Y. R. Chung, and C. O. Jeon Hydrogenophaga caeni sp. nov., isolated from activated sludge Int J Syst Evol Microbiol, May 1, 2007; 57(5): 1126 - 1130. [Abstract] [Full Text] [PDF]
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R. Usami, A. Echigo, T. Fukushima, T. Mizuki, Y. Yoshida, and M. Kamekura Alkalibacillus silvisoli sp. nov., an alkaliphilic moderate halophile isolated from non-saline forest soil in Japan Int J Syst Evol Microbiol, April 1, 2007; 57(4): 770 - 774. [Abstract] [Full Text] [PDF]
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M. Park, S. H. Ryu, T.-H. T. Vu, H.-S. Ro, P.-Y. Yun, and C. O. Jeon Flavobacterium defluvii sp. nov., isolated from activated sludge Int J Syst Evol Microbiol, February 1, 2007; 57(2): 233 - 237. [Abstract] [Full Text] [PDF]
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A. Pakdeeto, S. Tanasupawat, C. Thawai, S. Moonmangmee, T. Kudo, and T. Itoh Lentibacillus kapialis sp. nov., from fermented shrimp paste in Thailand Int J Syst Evol Microbiol, February 1, 2007; 57(2): 364 - 369. [Abstract] [Full Text] [PDF]
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S. Lu, S. H. Ryu, B. S. Chung, Y. R. Chung, W. Park, and C. O. Jeon Simplicispira limi sp. nov., isolated from activated sludge Int J Syst Evol Microbiol, January 1, 2007; 57(1): 31 - 34. [Abstract] [Full Text] [PDF]
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J.-M. Lim, C. O. Jeon, D.-J. Park, L.-H. Xu, C.-L. Jiang, and C.-J. Kim Paenibacillus xinjiangensis sp. nov., isolated from Xinjiang province in China. Int J Syst Evol Microbiol, November 1, 2006; 56(Pt 11): 2579 - 2582. [Abstract] [Full Text] [PDF]
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J.-C. Lee, J.-M. Lim, D.-J. Park, C. O. Jeon, W.-J. Li, and C.-J. Kim Bacillus seohaeanensis sp. nov., a halotolerant bacterium that contains L-lysine in its cell wall. Int J Syst Evol Microbiol, August 1, 2006; 56(Pt 8): 1893 - 1898. [Abstract] [Full Text] [PDF]
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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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I. Romano, L. Lama, B. Nicolaus, A. Gambacorta, and A. Giordano Alkalibacillus filiformis sp. nov., isolated from a mineral pool in Campania, Italy Int J Syst Evol Microbiol, November 1, 2005; 55(6): 2395 - 2399. [Abstract] [Full Text] [PDF]
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