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1 Biotechnology Research Centre, University of Tokyo, Yayoi 1-1-1, Bunkyo-Ku, Tokyo 113-8657, Japan
2 National Agricultural Research Centre, Park Road, Islamabad 45500, Pakistan
3 Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi 1-1-1, Bunkyo-Ku, Tokyo 113-8657, Japan
4 SORST, JST, Chiyoda-ku, Tokyo, Japan
Correspondence
Iftikhar Ahmed
iftikharnarc{at}hotmail.com
Toru Fujiwara
atorufu{at}mail.ecc.u-tokyo.ac.jp
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ABSTRACT |
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SEMs of cells of strain T-16XT, details of boron tolerance for strain T-16XT and related strains, parsimony and maximum-likelihood trees based on 16S rRNA gene sequences and results of TLC of polar lipids of strain T-16XT are available as supplementary material in IJSEM Online.
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TOPABSTRACTMAIN TEXTREFERENCES |
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) and some animals (Rowe et al., 1998; Rowe & Eckhert, 1999). Its essentiality for bacteria has been reported recently (Ahmed et al., 2007). A boron-containing quorum-sensing signal molecule is produced in several species of bacteria (Chen et al., 2002). The antibiotics boromycin (Kohno et al., 1996) and tartrolon A and B (Irschik et al., 1995), which are synthesized by bacteria, also contain boron. Negrete-Raymond et al. (2003) described the catabolism of phenyl boronic acid in an Arthrobacter nicotinovorans strain, during which boron is predicted to be released as orthoboric acid [B(OH)3].
At elevated levels, boron is toxic to living cells. Because of its toxicity, boron has long been used in the treatment of recurrent vulvovaginal candidiasis caused by some species of Candida and Saccharomyces (Swate & Weed, 1974; Otero et al., 2002). Boron is used as a food preservative to sterilize against micro-organisms (Nielsen, 2004) and is also used as an insecticide against cockroaches (Cochran, 1995).
We screened and isolated several boron-tolerant species from a soil containing naturally high levels of boron from the Hisarcik area in the Kutahya Province of Turkey. This area has been reported to be naturally high in boron minerals (Çöl & Çöl, 2003). The recently reported species ‘Bacillus boroniphilus’, isolated from this soil, can tolerate more than 450 mM boron and requires boron for growth (Ahmed et al., 2007). From our samples, we characterized a novel bacterial strain, T-16XT, that is moderately halotolerant and highly boron-tolerant. Based upon the data, we propose that the strain belongs to the genus Gracilibacillus. The genus Gracilibacillus was described by Wainø et al. (1999) and its three currently characterized species were isolated from extreme hypersaline environments.
We used previously described isolation and enrichment procedures to obtain strain T-16XT (Ahmed et al., 2007). The purified culture of the isolate was maintained on agar medium and also stored as a glycerol (35 %, w/v) stock at –80 °C. Sporangia and the sizes of cells grown on Luria–Bertani agar (pH 7.0) for 16 days were observed under phase-contrast microscopy, whereas flagella were observed using a scanning electron microscope according to a previously described procedure (Ahmed et al., 2007). It was clearly evident that individuals of strain T-16XT use a monotrichous flagellum (see Supplementary Fig. S1 available in IJSEM Online) for movement and produce endospores in a non-bulging or slightly swollen sporangium. Gram staining, performed according to Hucker's modified method (Cowan, 1974), revealed that the cells of strain T-16XT are Gram-positive.
The toxic effects of high boric acid concentrations on living cells are well known (Nable et al., 1997). The boron tolerance of strain T-16XT was compared with that of Escherichia coli DH10B as a control, following the procedure described previously by Ahmed et al. (2007). Strain T-16XT showed boron tolerance (Supplementary Fig. S2) because it grew in TSB medium (pH 7.4±0.1) containing 450 mM boric acid (H3BO3, referred to simply as boron in this paper). In similar tests, we observed that the closely related strain Gracilibacillus halotolerans DSM 11805T tolerated up to 50 mM boron, Gracilibacillus dipsosauri DSM 11125T up to 150 mM boron and Paraliobacillus ryukyuensis IAM 15001T as much as 100 mM boron. Among recently reported boron-tolerant species (Ahmed et al., 2007), ‘B. boroniphilus’ strains are reported to withstand more than 450 mM boron and cannot survive in its absence. In contrast, strain T-16XT tolerated 450 mM boron, but did not require it as an essential component for growth. Boron salts have often been used in microbial growth media (Stanier et al., 1966); however, the biological functions that require boron in plants and microbes are not clear, despite the fact that boron is required for growth in some organisms.
The ranges of pH, NaCl concentration and temperature for growth of strain T-16XT were determined as described previously (Ahmed et al., 2007). Motility, catalase and oxidase tests, resistance to antibiotics and enzyme activities were also evaluated following procedures described previously (Ahmed et al., 2007). Various physiological and biochemical tests were carried out using API 50 CHB and API 20E galleries (bioMérieux) according to the manufacturer's instructions. Physiological experiments using the API system, the determination of antibiotic resistance using ATB-VET and catalase and oxidase tests were repeated several times. The Biolog GP2 and GN2 characterization systems were used to determine various metabolic features according to the manufacturer's instructions.
Strain T-16XT was moderately halotolerant (Table 1) and highly boron-tolerant (Supplementary Fig. S2). The strain withstood 11 % (w/v) NaCl and grew optimally in the presence of 1–3 % NaCl. Because it exhibited optimum growth at alkaline pH (range pH 7.5–8.5) and was able to grow at above pH 9.0, it was characterized as alkalitolerant, according to the definition of Jones et al. (1994). The best growth occurred on BUG medium containing 20 mM boron and 1 % (w/v) NaCl, but we also observed growth on marine agar 2216 (MA; Difco), tryptic soya agar (TSA) and nutrient agar (NA), although growth was slow and colonies were small. Strain T-16XT shares many characteristics with members of the genus Gracilibacillus. The characteristics that differentiated strain T-16XT from closely related type strains are shown in Table 1. Additional characteristics are included in the species description. In addition to its boron tolerance, the major characteristic that differentiated strain T-16XT from closely related type strains was a positive Voges–Proskauer test.
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. The purified PCR product was sequenced as described previously (Ahmed et al., 2007). The consensus sequence obtained using the DNASIS pro software package (hitachi software engineering) was compared with the sequences of closely related type strains retrieved from the ddbj/embl database using BLAST searches. An alignment was produced using CLUSTAL X 1.8 software (Thompson et al., 1997) and edited using the BioEdit software package (Hall, 1999) to exclude ambiguous positions and gaps from the calculations. Ultimately, 1302 bp were used to calculate evolutionary distances and Knuc values (Kimura, 1980) and to construct a phylogenetic tree using the neighbour-joining method (Saitou & Nei, 1987) in the PHYLIP software package (Felsenstein, 2005). The tree was plotted using NJplot software. To assess the stability of the phylogenetic tree, a bootstrap analysis (Felsenstein, 2005) was performed using 1000 resamplings of the neighbour-joining data. Phylogenetic trees were also generated using maximum-likelihood and maximum-parsimony algorithms, which generated relationships for the novel strain similar to those constructed using the neighbour-joining method (Supplementary Fig. S3). These analyses strongly support the affiliation of strain T-16XT with the genus Gracilibacillus.
Based on the comparison of 16S rRNA gene sequence data, the highest similarity of strain T-16XT was 96.7 % with Gracilibacillus orientalis XH-63T, followed by 95.5 % with G. halotolerans NNT, 95.4 % with G. dipsosauri DD1T and 95.7 % with Paraliobacillus ryukyuensis O15-7T. Strain T-16XT was associated with ‘Bacillus group 1’ in the subgroup of halophilic or halotolerant organisms as described by Ash et al. (1991) and formed a clade with G. orientalis XH-63T at a 64 % bootstrap value (Fig. 1). The phylogenetic position of strain T-16XT with G. orientalis was also supported by cellular fatty acid profiles (Table 2), in addition to other physiological and chemotaxonomic data.
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). Its phylogenetic position (Fig. 1) was also closely associated with G. orientalis. Halobacillus species possess the unsaturated fatty acids C16 : 1
7c alcohol and C17 : 110c, which were absent from the profiles of strain T-16XT and other members of Gracilibacillus.
MK-7 (90 %) was determined to be the predominant respiratory quinone system in the novel strain using the method described by Xie & Yokota (2003), although MK-6 (10 %) was also detected as a minor component. Cell-wall peptidoglycans were analysed for amino acid content using two-dimensional TLC and HPLC (Shimadzu) as described elsewhere (Schleifer & Kandler, 1972; Groth et al., 1996). The peptidoglycans of strain T-16XT contained glutamic acid, meso-diaminopimelic acid, alanine and muramic acid in the molar ratio of 1.0 : 1.1 : 2.0 : 0.4 as the diagnostic amino acids, representing peptidoglycan type A1
(directly cross-linked meso-diaminopimelic acid; Schleifer & Kandler, 1972). The polar lipids were extracted and purified from 100 mg dried cells by the procedure of Minnikin et al. (1984) and examined by two-dimensional TLC, using Kieselgel 60 F254 plates (Merck), as described by Kudo (2001). The polar lipid profile of strain T-16XT consisted predominantly of diphosphatidylglycerol and phosphatidylglycerol (Supplementary Fig. S4). An unknown aminolipid (AL1) and three unknown polar lipids (L1, L2, L3) were also detected, which could not be identified with any of the specific spray reagents employed. However, no reagent for detection of glycolipids was used. The type species of the genus, G. halotolerans, was also diagnosed with MK-7 as the predominant respiratory quinone system, meso-diaminopimelic acid in cell-wall peptidoglycans of type A1 and the major polar lipids diphosphatidylglycerol and phosphatidylglycerol (Wainø et al., 1999) and hence these characteristics of strain T-16XT are in accordance with the traits of the genus Gracilibacillus; however, the lack of phosphatidylethanolamine, an unknown phospholipid and two unknown aminophospholipids reported to be present in G. orientalis (Carrasco et al., 2006) distinguished strain T-16XT from its phylogenetic neighbour (Fig. 1). These characteristics also fit many other bacilli. Thus, they do not indicate that the strain is a member of Gracilibacillus.
The DNA G+C content of strain T-16XT was 35.8 mol% as determined using a procedure described previously (Ahmed et al., 2007). The other three species of the genus Gracilibacillus have G+C contents in the range 37–39 mol%, which is slightly higher than that of strain T-16XT. However, the highest 16S rRNA gene sequence similarity of strain T-16XT occurred with members of Gracilibacillus (Fig. 1), and critical analysis of other chemotaxonomic data (Table 1) also suggested that strain T-16XT belongs to the genus Gracilibacillus.
For DNA–DNA hybridization experiments, the genomic DNA of the novel strain and of the previously described closely related type strains was isolated using Qiagen Genomic-tip 500/G following the manufacturer's protocol, with a minor modification in which RNase T1 was used in addition to RNase A. DNA–DNA reassociation was carried out as described by Ezaki et al. (1989) at 39 °C with photobiotin-labelled DNA in Nunc 96-well microplates. The DNA–DNA relatedness values of strain T-16XT were 26.2 % with G. orientalis CCM 7326T, 13.1 % with G. halotolerans DSM 11805T, 15.2 % with G. dipsosauri DSM 11125T and 16.2 % with Paraliobacillus ryukyuensis IAM 15001T. These values were lower than the threshold of 70 % and thus indicate that strain T-16XT represents a novel species (Stackebrandt & Goebel, 1994). The morphological, chemotaxonomic, phylogenetic and genotypic features of strain T16XT suggest that it belongs to the genus Gracilibacillus; we propose the name Gracilibacillus boraciitolerans sp. nov.
Description of Gracilibacillus boraciitolerans sp. nov.
Gracilibacillus boraciitolerans (bo.ra'ci.i.to'le.rans. N.L. n. boracium boron; L. part. adj. tolerans tolerating; N.L. part. adj. boraciitolerans boron-tolerating).
Cells are motile using a long monotrichous flagellum. Cells are Gram-positive, short rods, 2.0–4.5 µm in length, 0.3–0.9 µm in diameter, occurring singly, occasionally in pairs; filamentous cells also occur. Spherical endospores are produced in a non-swollen or slightly swollen sporangium in a terminal or subterminal position. Colonies are circular with entire margins, spreading but slightly convex, translucent and viscous in texture, 2–3 mm in diameter after 4 days growth on BUG agar medium (pH 7.5) at 30 °C. Younger colonies are dirty white, but become pink and then red in a few to several days. The pink or red pigment may diffuse into the agar medium after several days. Colonies are mostly light pink at high salt concentrations. Grows optimally at 25–28 °C; the temperature range for growth is 16–37 °C; no growth occurs at 
45 °C and little growth at 16 °C after several days. The optimum pH for growth is 7.5–8.5, with a range of pH 6.0–10.0. The type strain can tolerate 0–450 mM boron, but grows optimally in the absence of boron. The NaCl tolerance range is 0–11 % (w/v), indicating that the type strain is moderately halotolerant; it can grow on MA, TSA and NA (with or without boron or NaCl). Oxidase, catalase, Voges–Proskauer and o-nitrophenyl 
-D-galactopyranoside (ONPG) tests are positive, whereas tests for production of indole and H2S, nitrate reduction, lysine and ornithine decarboxylases, arginine dihydrolase, tryptophan deaminase, utilization of citrate and hydrolysis of gelatin and urea are negative (API 20E). Can produce acid from L-arabinose, D-ribose, glucose, D-mannose, aesculin, D-cellobiose, D-maltose, D-lactose, D-melibiose and D-trehalose; weakly positive for acid production from D-xylose, methyl -D-xylopyranoside, D-fructose, D-mannitol and D-sorbitol (API 50CHB). Can oxidize 3-methyl glucose, amygdalin, arbutin, D-cellobiose, dextrin, D-fructose, D-galactose, D-mannitol, D-mannose, D-melezitose, D-melibiose, D-psicose, D-raffinose, D-ribose, D-sorbitol, D-trehalose, D-xylose, gentiobiose, glycerol, lactulose, L-arabinose, maltose, maltotriose, palatinose, salicin, sucrose, turanose, 
-D-glucose, -D-lactose, methyl -D-galactoside, methyl -D-galactoside, methyl -D-glucoside, methyl -D-glucoside, DL-lactic acid, D-glucuronic acid, gluconic acid, pyruvic acid and -ketobutyric acid (Biolog). The major cellular fatty acids are: anteiso-C15 : 0 (45.7 %), iso-C15 : 0 (18.2 %), anteiso-C17 : 0 (16.9 %), iso-C17 : 0 (3.2 %), C16 : 0 (5.3 %), C15 : 0 (1.9 %), iso-C16 : 0 (1.9 %), C18 : 19c (1.0 %) and traces (less than 1 %) of some other fatty acids. The cell wall contains peptidoglycan with meso-diaminopimelic acid as the diagnostic amino acid, representing cell-wall peptidoglycan type A1. The dominant respiratory lipoquinone system is MK-7. Major polar lipids are diphosphatidylglycerol and phosphatidylglycerol. In addition, moderate to minor amounts of an unknown aminolipid and three polar lipids are detected. Strong enzyme activity is observed for alkaline phosphatase, -galactosidase and - and -glucosidase, whereas weak enzyme activity is observed for -galactosidase, esterase (C8), esterase lipase (C8) and leucine arylamidase (API ZYM). Resistant to penicillin, amoxicillin and metronidazol (ATB-VET Strip). The G+C content of the type strain is 35.8 mol% (HPLC).
Strain T-16XT (=DSM 17256T=IAM 15263T=ATCC BAA-1190T), which was isolated from soil naturally containing boron minerals from the Hisarcik area in the Kutahya Province of Turkey, is the type strain.
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ACKNOWLEDGEMENTS |
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