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1 Graduate School of Biosphere Science, Hiroshima University, Kagamiyama, Higashi-Hiroshima 739-8528, Japan
2 Japan Agency for Marine-Earth Science and Technology, Natsushima-cho, Yokosuka 237-0061, Japan
3 Center for Advanced Marine Core Research, Kochi University, Monobe, Nankoku 783-8502, Japan
Correspondence
Takeshi Naganuma
takn{at}hiroshima-u.ac.jp
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ABSTRACT |
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7c alcohol and C18 : 17c and cyclopropane C19 : 0 cyc fatty acids were predominant in both strains. The DNA G+C contents of IS-Hb4T and IS-Hb7T were respectively 43.3 and 42.1 mol%. Physiological and biochemical analyses combined with DNA–DNA hybridization results allowed us to place strains IS-Hb4T (=JCM 14154T=DSM 18394T) and IS-Hb7T (=JCM 14155T=DSM 18393T) in the genus Halobacillus as the respective type strains of the novel species Halobacillus profundi sp. nov. and Halobacillus kuroshimensis sp. nov.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains IS-Hb4T and IS-Hb7T are AB189298 and AB195680.
Genetic relatedness of strains IS-Hb4T and IS-Hb7T to related Halobacillus type strains and differential carbon source utilization patterns are available with the online version of this paper.
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; Spring et al., 1996). So far, nine species of this genus have been identified (Amoozegar et al., 2003a, b; Yoon et al., 2003, 2004, 2005; Liu et al., 2005). The increasing number of publications on bio-applications and other aspects of Halobacillus and the large number of 16S rRNA gene sequences deposited in databases for unidentified species reflect the wide distribution of these bacteria and their considerable scientific interest (Burja et al., 1999; Pinar et al., 2001; Yang et al., 2002; Rivadeneyra et al., 2004). In our investigations of the diversity of halophilic bacteria in various habitats over the last few years, we obtained strains IS-Hb4T and IS-Hb7T in an endemic population from a carbonate rock collected at a deep-sea methane seep at Kuroshima Knoll, south-western Japan. Living in the special environment of low temperature, high pressure and low oxygen availability, these bacteria possess several features that are different from those of described species that would be considered evidence of interesting adaptation.
Samples from which the bacteria were isolated, carbonate rocks authentically formed in a methane seep of the Kuroshima Knoll, located at 642 m depth at 24° 07.8' N 124° 11.2' E (Fujikura et al., 2003; Inagaki et al., 2004), were collected with the remotely operated vehicle Dolphin 3K, operated by the Japan Agency for Marine Earth Science and Technology (JAMSTEC). The in situ water temperature, salinity (electric conductivity) and methane concentration were 7.6 °C, 35.5 mS cm–1 and 
1 µM. An enrichment medium containing 0.5 % (w/v) Bacto-peptone (Difco), 0.25 % yeast extract (Difco), 0.1 % D-glucose (Wako) and 15 % NaCl (Okamoto et al., 2001; Okamoto & Naganuma, 2003; Okamoto, 2004) in distilled water was used to culture and store the new isolates at 30 °C, except for certain changes in salinity and temperature in some tests. Distinct single colonies on 1.5 % agar plates of the generic medium were selected and isolated at least three times to obtain pure cultures. Type strains Halobacillus halophilus DSM 2266T, Halobacillus litoralis DSM 10405T, Halobacillus salinus JCM 11546T, Halobacillus trueperi DSM 10404T, Halobacillus karajensis DSM 14948T, Halobacillus locisalis DSM 16468T, Halobacillus yeomjeoni DSM 17110T, Halobacillus aidingensis DSM 18198T and Halobacillus dabanensis DSM 18199T were used as reference strains.
Gram reaction, acid-fast staining, motility and endospore observation, enzyme activities (catalase, urease, phenylalanine deaminase, oxidase) and hydrolysis of starch, aesculin, gelatin and casein were tested according to conventional protocols (Doetsch, 1981; Smibert & Krieg, 1981). For anaerobic growth and nitrate reduction examination, the bacteria were tested using the same medium in which they grew well in isolation step both on agar plates and in liquid broth in an anaerobic atmosphere of (v/v) 80 % N2, 10 % CO2 and 10 % H2 (Te-Her Anaero-Box ANX-1 system; Hirasawa). Media (in flasks for agar culture and in test tubes for liquid culture) were well gassed under nitrogen to remove oxygen before being autoclaved. Test tubes and agar plates were manipulated inside the anaerobic chamber. Any residual oxygen carried over or generated unexpectedly by the culture procedure inside the chamber was detected by an oxygen sensor and eliminated by the system until undetectable. Colonies and OD600 were observed to determine anaerobic growth. Liquid medium supplemented with 0.1 % KNO3 in test tubes containing Durham tubes was inoculated aerobically and anaerobically for nitrate reduction assay. Escherichia coli K-12 and Virgibacillus marismortui DSM 12325T were used as positive controls and H. litoralis DSM 10405T, H. trueperi DSM 10404T and H. salinus JCM 11546T were used as negative controls; uninoculated medium was also included. Sulfanilic acid and 
-naphthylamine solutions and zinc powder were used to detect formation of nitrite and denitrification as described in the conventional method (Smibert & Krieg, 1981). Ability to utilize single carbon sources was tested using Biolog microplates based on the instructions of the manufacturer and previous studies (Garland & Mills, 1991; Garland, 1996, 1999). Acid production from carbohydrates was assayed using API 50CH and API 20 CE kits (bioMérieux). Aerobic growth at hydrostatic pressures of 0.1, 10, 20 and 30 MPa was examined using stainless-steel pressure vessels (Rigosha) compressed with a high-pressure stainless steel hand pump model 11-100 equipped with a pressure gauge (Enerpac). Inoculated liquid medium with 10 % NaCl added was filled into sterile polyethylene transfer pipettes. The pipettes were then heat-sealed with complete exclusion of air bubbles and incubated in the pressure vessels under a certain pressure at room temperature for 1 week. Bacterial growth was observed as turbidity or formation of cell clumps.
Bacterial cells from cultures at stationary phase were harvested and genomic DNA was extracted according to protocol described by Wilson (1995). The PCR procedure of DeLong (1992) for amplifying the 16S rRNA gene was followed. Nearly full-length sequences (1500 bp) of amplified 16S rRNA genes were obtained using a Dual CyDye Terminator sequencing kit (Amersham Biosciences) and sequenced with a Long-Read Tower sequencer (Visible Genetics). The sequences obtained were used to search for similarity on public databases (DDBJ/GenBank/EMBL) using the FASTA program (Pearson & Lipman, 1988) and aligned with CLUSTAL X software version 1.83 (Thompson et al., 1997). Phylogenetic trees were then constructed based on neighbour-joining, minimum evolution and maximum-parsimony methods using MEGA 3.1 (Kumar et al., 2004) and compared with those inferred by using the SEQBOOT, DNADIST, DNAMLK and CONSENSE programs of the PHYLIP package version 3.6 (Felsenstein, 2004) through 100–1000 bootstrap replications. Rooted trees which showed only minor differences in topology and high frequency of bootstrapping were chosen for phylogenetic analysis.
Non-radioactive digoxigenin-labelling DNA hybridization and anti-digoxigenin chemiluminescent detection methods were applied to determine DNA–DNA relatedness of the novel strains to all type strains of the genus Halobacillus. DIG-11-dUTP-labelled ssDNAs were hybridized with reference ssDNAs immobilized on positively charged nylon filter membrane (Brown, 1995) using DIG-High Prime DNA Labelling, Detection Starter kit II and DIG Wash and Block buffer set (Roche Molecular Biochemicals) under the manufacturer's instructions. The chemiluminescent density of hybrids was detected using the VersaDoc Imaging System model 5000 and analysed with Quantity One software version 4.4 (Bio-Rad). Experiments were repeated three times. The G+C content of the strains was determined by capillary zone electrophoresis (CZE) (Fraga et al., 2002; Hua & Naganuma, 2007). Highly purified genomic DNAs were enzymically hydrolysed into nucleosides (Tamaoka & Komagata, 1984; Mesbah et al., 1989) and nucleosides were then eluted in an alkaline phosphate buffer system, separated and detected quantitatively by a CAPI-3300 multichannel CZE (Otsuka Electronics). Cellular fatty acids were extracted and analysed using conventional GC-MS methods (Sasser, 2001). Quinones were extracted from cells according to Nishijima et al. (1997) and analysed by HPLC. Bacterial cell walls were hydrolysed and peptidoglycans were extracted and purified using high-performance TLC. The amino acid composition of hydrolysed peptidoglycans was detected using HPLC (Komagata & Suzuki, 1987).
The 16S rRNA gene sequences of strains IS-Hb4T and IS-Hb7T showed high similarity to those of type strains of genus Halobacillus, H. halophilus NCIMB 9251T (97.3 and 96.4 %, respectively), H. trueperi DSM 10404T (98.9 and 97.9 %), H. litoralis SL-4T (98.8 and 97.8 %), H. karajensis DSM 14948T (99.2 and 98.1 %), H. salinus HSL-3T (97.8 and 97.0 %), H. locisalis SL-4T (98.3 and 97.6 %), H. yeomjeoni MSS-402T (98.2 and 97.7 %), H. aidingensis AD-6T (98.0 and 97.2 %) and H. dabanensis D-8T (99.4 and 98.5 %) (see Supplementary Table S1 in IJSEM Online), confirming their close relationship at the species level in this genus. Phylogenetic relationships of strains IS-Hb4T and IS-Hb7T and other type strains as well as other species of bacilli are shown in Fig. 1. The novel strains shared low levels of DNA–DNA relatedness with H. halophilus DSM 2266T (12.2 and 30.7 % relatedness, respectively, with IS-Hb4T and IS-Hb7T), H. trueperi DSM 10404T (33.0 and 20.1 %), H. litoralis DSM 10405T (24.6 and 14.7 %), H. karajensis DSM 14948T (10.4 and 27.4 %), H. salinus JCM 11546T (25.4 and 18.6 %), H. locisalis (8.5 and 23.5 %), H. yeomjeoni DSM 17110T (1.0 and 1.4 %), H. aidingensis DSM 18198T (17.1 and 23.4 %) and H. dabanensis DSM 18199T (6.0 and 5.3 %) (Supplementary Table S1). DNA–DNA relatedness between the two strains was 49.5 %. The results above indicated sufficient genotypic evidence for their assignment to separate novel species (Wayne et al., 1987).
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). MK-7 was detected as the main menaquinone of strains IS-Hb4T and IS-Hb7T. Unlike other Halobacillus species, which often produce the predominant fatty acids anteiso-C15 : 0, anteiso-C17 : 0, iso-C14 : 0, iso-C15 : 0 and iso-C16 : 0, the deep-sea isolates IS-Hb4T and IS-Hb7T showed high percentages of C16 : 0 (28.22 and 20.28 %, respectively), C16 : 17c alcohol (12.25 and 8.47 %), C18 : 17c (30.99 and 25.98 %) and C19 : 0 cyc (18.99 and 14.54 %) in their fatty acid profiles. Furthermore, some acids, such as C12 : 07 and C17 : 0 cyc, were found in these isolates for the first time within the halobacilli (Table 1). The DNA G+C contents of strains IS-Hb4T and IS-Hb7T were 43.3 and 42.1 mol%, respectively (Table 2).
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. Under increased hydrostatic pressure, growth was observed in all cases from 0.1 to 30.0 MPa. Weak growth of strain IS-Hb4T and IS-Hb7T (small colonies of about 0.5 mm in diameter after 48 h, with slow growth and little increase in OD600) was observed under anaerobic conditions and strain IS-Hb4T (but not strain IS-Hb7T) reduced nitrate to nitrite; these differences from other species of the genus Halobacillus show a tendency of adaptation of these strains to the deep-sea environment. If so, they are the first members of the genus Halobacillus to share anaerobic activity with Bacillus species (Marino et al., 2000, 2001; Ye et al., 2000).
Description of Halobacillus profundi sp. nov.
Halobacillus profundi (pro.fun'di. L. gen. n. profundi of the depths of the sea, of the deep-sea).
Rod-shaped, Gram-positive, non-motile cells, 0.5–1.0 by 1.0–2.9 µm, occur singly or in pairs or short chains (Fig. 2a). Endospores are spherical or ellipsoidal and are located in a central position. Colonies are circular, convex with entire margins, pale yellow in colour and 1.5–2.5 mm in diameter after 3 days. Temperature range for growth is 9–47 °C (optimum 25 °C). Growth occurs in medium containing 0.5–30 % (w/v) NaCl (optimum 10 %). The pH range for growth is 5.5–10.0 (optimum pH 7.5–8.0). Weak growth is observed under anaerobic conditions. Nitrate is variably reduced to nitrite. Catalase- and oxidase-positive. Acid-fastness, phenylalanine deaminase and urease tests are negative. Tweens 20, 40 and 80, starch, casein and aesculin are hydrolysed. Gelatin, dextrin, -cyclodextrin and glycogen are not hydrolysed. Acid is produced from D-fructose, maltose, D-glucose, D-xylose, D-mannitol, maltose, mannose, rhamnose, sucrose, trehalose, raffinose, mannitol, sorbitol and N-acetylglucosamine. Acid is not produced from D-tagatose, cellobiose, D-galactose, melibiose, cellobiose or inositol. The following substrates are utilized as single sources of carbon: N-acetyl-D-glucosamine, i-erythritol, -D-lactose, D-mannitol, pyruvic acid methyl ester, -cyclodextrin, Tweens 40 and 80, -ketoglutaric acid, -ketobutyric acid, -ketovaleric acid, D-saccharic acid, sebacic acid, L-glutamic acid, glycyl L-aspartic acid and D-serine (Supplementary Table S2). The cell wall contains peptidoglycan based on L-orn–D-Asp. The major menaquinone is MK-7. Major fatty acids are C16 : 0, C16 : 17c alcohol, C18 : 17c and C19 : 0 cyc. The DNA G+C content of the type strain is 43.3 mol% (determined by CZE).
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Description of Halobacillus kuroshimensis sp. nov.
Halobacillus kuroshimensis (ku.ro.shi.men'sis. N.L. masc. adj. kuroshimensis from Kuroshima, Japan, where the type strain was isolated).
Rod-shaped, Gram-positive, non-motile cells, 0.5–1.0 by 1.6–3.3 µm, occur singly or in pairs or short chains (Fig. 2b). Endospores are spherical or ellipsoidal and are located in a terminal position. Colonies are circular, convex with entire margins, yellow–orange in colour and 1.5–2.5 mm in diameter after 3 days. Temperature range for growth is 9–48 °C (optimum 25 °C). Growth occurs in medium containing 0.5–25 % (w/v) NaCl (optimum 6 %). pH range for growth is 5.5–10.0 (optimum pH 7.5–8.0). Growth occurs weakly under anaerobic conditions. Nitrate is not reduced to nitrite. Catalase- and oxidase-positive. Acid-fastness, phenylalanine deaminase and urease tests are negative. Tweens 20, 40 and 80, starch, gelatin, casein and aesculin are hydrolysed. Dextrin, -cyclodextrin and glycogen are not hydrolysed. Acid is produced from D-fructose, D-glucose, maltose, mannose, inositol, glycerol, N-acetylglucosamine, sucrose and cellobiose. Acid is not produced from D-tagatose, D-galactose, salicin, D-xylose, D-mannitol, D-trehalose or melibiose. D-Xylose, -D-glucose, myo-inositol, maltose, D-mannose and Tweens 40 and 80 are utilized as single carbon sources (Supplementary Table S2). The cell wall contains peptidoglycan based on L-orn–D-Asp. The major menaquinone is MK-7. Fatty acids C16 : 17c alcohol, C18 : 17c and C19 : 0 cyc are abundant. The DNA G+C content of the type strain is 42.1 mol% (determined by CZE).
The type strain, IS-Hb7T (=JCM 14155T=DSM 18393T), was isolated from the same sample as strain IS-Hb4T.
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ACKNOWLEDGEMENTS |
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