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1 Biotechnology Research Center, 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 Research Center for Water Environmental Technology, University of Tokyo, Hongo 7-3-1, Bunkyo-ku, Tokyo 113-8657, Japan
5 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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Results of growth experiments in the presence of boron, photomicrographs of cells of strain 10aT and results of separation of polar lipids of strain 10aT and related type strains are available as supplementary material in IJSEM Online.
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) and possibly also for animals (Rowe et al., 1998; Rowe & Eckhert, 1999). In bacteria, Chen et al. (2002) presented evidence for the biological role of boron in quorum sensing. On the other hand, boron is toxic to living cells when present above a certain threshold. Because of its toxic effects at high concentrations for micro-organisms, boron has been used as a food preservative (Nielsen, 2004), and it has also been used as an insecticide against cockroaches (Cochran, 1995). However, only recently, Bacillus boroniphilus, Chimaereicella boritolerans and Gracilibacillus boraciitolerans have been reported to tolerate more than 450, 300 and 450 mM boron, respectively, and/or require boron for growth (Ahmed et al., 2007a, b, c).
Over the last decade, the genus Bacillus has been dissected taxonomically into several new genera based on comprehensive analyses of 16S rRNA gene sequences and other chemotaxonomic data (Wisotzkey et al., 1992; Ash et al., 1993; Shida et al., 1996; Heyndrickx et al., 1998; Wainø et al., 1999; Yoon et al., 2001, 2002). rRNA group 2 of the genus Bacillus (Ash et al., 1991) containing L-lysine or D-ornithine in the peptide subunit also includes non-Bacillus-type organisms such as members of Caryophanon, Kurthia, Sporosarcina, Planococcus and Filibacter (Clausen et al., 1985; Keddie & Shaw, 1986; Stackebrandt et al., 1987; Pechman et al., 1976; Farrow et al., 1994). There is a need to re-evaluate the taxonomic status of this group. Although it has been discussed previously (Farrow et al., 1994; Rheims et al., 1999), no proposal has yet been put forward to transfer these organisms into one or more new or existing genera. In this paper, we characterize three round-spore-forming strains belonging to a new genus in Bacillus RNA group 2. This genus is distinguished from other members of this group by the presence of lysine and aspartate in the peptidoglycan of the cell wall.
The three strains were isolated from soil sampled randomly from the experimental field of the University of Tokyo (Yayoi campus), Japan. We used previously described isolation and enrichment procedures (Ahmed et al., 2007a). The purified isolates (strains 10aT, 11c and 12B) were maintained on agar medium, and also stored as glycerol (35 %, w/v) stocks at –80 °C, and subjected to characterization.
To demonstrate boron tolerance, strain 10aT and Escherichia coli DH10B (control) were grown up to upper mid-exponential phase (OD600 1.2) at 37 °C, with vigorous shaking. The cultures were serially diluted and 7 µl aliquots were spotted onto nutrient agar medium (NA; Difco) (pH 7.0) containing different levels of boron. The plates were incubated at 37 °C for 2 days before being photographed. Strain 10aT manifested tolerance of boron up to 100 mM on NA, whereas weak growth was observed at 150 mM boron (Supplementary Fig. S1 in IJSEM Online). The strain was also cultured in 150 ml Luria–Bertani (LB) medium (pH 7.0) with different levels of boron ranging from 0 (control) to 300 mM, while being shaken vigorously at 30 °C. After every 60 min, samples were taken aseptically to measure OD600 using a spectrophotometer (Hitachi U-1800). The data for OD600 against time plotted at different boron concentrations demonstrated that strain 10aT could grow with 0–100 mM boron in liquid culture (LB medium) and that growth was equivalent to that without addition of boron (Supplementary Fig. S2), indicating that boron was not required for growth. However, there was no growth at 200 mM boron and weak growth was observed at 150 mM boron.
Sporangia and the sizes of cells grown on NA with MgSO4.7H2O (1.01 mM), KCl (13.4 mM), FeSO4 (0.001 mM), Ca(NO3)2 (1.0 mM) and MnCl2 (0.01 mM) at pH 7.0 for 6 days at 30 °C were examined under phase-contrast microscopy. Cells of the strains produced oval or spherical endospores in a terminal position in a swollen sporangium (Supplementary Fig. S3). Cells of the strains were Gram-positive as determined according to Hucker's modified method (Cowan, 1974). Colonial morphology was observed on isolated colonies grown on nutrient agar (pH 7.0, Difco) for 2 days at 30 °C. The pH range for growth was determined in tryptic soya broth (TSB; Difco) with a pH range of 4.0 to 10.0 at 30 °C by monitoring OD600 using a mini-photometer (model 518R; TAITEC) and the temperature range for growth was determined on tryptic soya agar (TSA; Difco) (pH 7.0) by incubating at different temperatures from 4 to 50 °C. The isolated strains grew at pH 5.5–9.5 with optimum growth at pH 7.5 and no growth at pH 5.0. We observed growth of the strains at 16–45 °C with optimum growth at 37 °C; there was no growth at 
50 °C and only slight growth after several days at 16 °C. These findings distinguished the strains from the closely related species Bacillus fusiformis and Bacillus sphaericus, which can only grow up to 40 °C. Growth at various NaCl concentrations was investigated on TSA (pH 7.0) at 30 °C. The novel strains tolerated 0–5 % (w/v) NaCl in the agar medium. This differed from B. fusiformis, which can tolerate up to 7 % (w/v) NaCl (Priest et al., 1988). We also observed growth of the novel strains on marine agar 2216 (Difco), TSA and NA with and without addition of boron or NaCl.
Physiological and biochemical characteristics were determined using API 20E and API 50CH galleries (bioMérieux). The strains were positive for oxidase and catalase activities as assessed by previously described procedures (Ahmed et al., 2007a). Motility was also confirmed with M medium (bioMérieux) in addition to microscopy. Since mainly negative reactions were obtained with API 50CH and API 20E for utilization of various carbon sources, we analysed an extended array of metabolic features of the strains using the Biolog GP2 and GN2 characterization system. Resistance to antibiotics was assessed with an ATB-VET strip (bioMérieux) and enzyme activities were determined with an API ZYM strip (bioMérieux). All commercial kits were used according to the manufacturers' protocols. The isolated strains exhibited many features that were similar to those of B. fusiformis and B. sphaericus; however, they differed from these species in certain physiological and biochemical characteristics (Table 1). All three novel strains gave identical results in these tests.
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. The purified PCR product was sequenced as described previously (Ahmed et al., 2007a). The DNASIS Pro (Hitachi Software Engineering) software package was used to obtain the consensus sequence. Sequences of closely related type strains used for constructing the phylogenetic tree were selected and retrieved from the DDBJ/EMBL databases by BLAST searches for bacteria. Alignment was performed with CLUSTAL X (version 1.8w; Thompson et al., 1997) and evolutionary distances and Knuc values (Kimura, 1980) were generated. BioEdit software (Hall, 1999) was used to remove gaps and ambiguous bases in the alignments. A phylogenetic tree was constructed from 1294 unambiguously aligned nucleotides using the neighbour-joining method (Saitou & Nei, 1987) contained in the PHYLIP software package (Felsenstein, 2005) and plotted with NJPlot software. The stability of the relationship was assessed by bootstrap analysis (Felsenstein, 2005) by performing 1000 resamplings for the tree topology of the neighbour-joining data.
An almost-complete 16S rRNA gene sequence (1484 nucleotides) of strain 10aT was compared with sequences of closely related type strains retrieved from the public DDBJ database. Based on 16S rRNA gene sequence data, the similarity of the novel strain 10aT was 97.2 % to B. fusiformis DSM 2898T (GenBank accession no. AJ310083), 96.9 % to B. sphaericus DSM 28T (AJ310084), 96.1 % to Bacillus odysseyi 34hs-1T, 95.0 % to Bacillus massiliensis 4400831T and 94.5 % to Bacillus silvestris HR3-23T; the similarity was 99.3 % with strain 11c and 99.2 % with strain 12B after alignment, whereas strains 11c and 12B had 99.8 % similarity. The 16S rRNA gene sequence of strain 11c was omitted during construction of the phylogenetic tree because the sequence was incomplete. The novel strains occupied a separate lineage in the phylogenetic tree with high bootstrap support (Fig. 1). Strain 10aT is closely related to B. fusiformis and B. sphaericus in many other characteristics, although the data presented here also exhibited differences from these and other type strains of the genus Bacillus (Table 1
) and among closely related genera (Table 2). On the basis of morphological, physiological, phylogenetic, chemotaxonomic and genomic characteristics which we determined, strains 10aT, 11c and 12B are considered to be members of the same species.
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). DNA–DNA hybridization was performed at 42 °C with photobiotin-labelled DNA and microplates as described by Ezaki et al. (1989), using an HTS7000 Bio Assay Reader (Applied Biosystems) for fluorescence measurements. The DNA–DNA hybridization values among strains 10aT, 11c and 12B were more than 97.8 %, confirming that these strains belong to the same species. However, DNA–DNA relatedness of strain 10aT was 61.1 % with B. fusiformis DSM 2898T, 43.2 % with B. sphaericus IAM 13420T and 26.4 % with B. silvestris DSM 12223T. These values are less than the 70 % threshold needed to assign the strains to a novel species (Stackebrandt & Goebel, 1994). The DNA G+C content of the novel strains was 36.5–37.9 mol% as determined by HPLC using a procedure described previously (Ahmed et al., 2007a).
Respiratory quinones were analysed as described by Xie & Yokota (2003) and MK-7 (87 %) was determined as the predominant quinone system in the novel strains, although MK-6 (13 %) was also detected as a minor component. The purified cell wall was analysed for amino acids using two-dimensional TLC and then HPLC (Shimadzu) as described previously (Schleifer & Kandler, 1972; Groth et al., 1996). Strain 10aT contained peptidoglycan with alanine, glutamic acid, lysine and aspartic acid in a molar ratio of 1.83 : 1.0 : 0.69 : 0.63 as the diagnostic amino acids, in contrast to the type species of the genus Bacillus, Bacillus subtilis, which was diagnosed with meso-diaminopimelic acid in the cell-wall peptidoglycan (Schleifer & Kandler, 1972). During this study, B. fusiformis DSM 2898T produced similar results in cell-wall peptidoglycan analysis, with lysine, alanine, glutamic acid and aspartic acid in a similar molar ratio to strain 10aT. This represents peptidoglycan type A4
(Lys–Asp) as described by Schleifer & Kandler (1972). The close relative B. sphaericus was reported to contain L-lys–D-Asp in the peptidoglycan as the diagnostic amino acids by Stackebrandt et al. (1987). So far, peptidoglycan consisting of Lys–Asp has not been reported for any other endospore-forming species of Bacillus group 2 (Ash et al., 1991; Stackebrandt et al., 1987; Nakamura et al., 2002; Ranftl & Kandler, 1970; Rheims et al., 1999; Claus & Fritze, 1989), but the closely related species of Kurthia (Fig. 1) share this characteristic (Shaw & Keddie, 1983).
For whole-cell fatty acid analysis, the cells were grown on TSA for 24 h at 28 °C and the cellular fatty acid profile was determined using the GC-based Microbial Identification system (MIDI) according to the manufacturer's instructions. The cellular fatty acid profile for the novel strains consisted predominantly of iso- and anteiso-branched fatty acids (Table 3), which is similar to other members of the B. sphaericus-like group. A MIDI database search of profiles also supported the novel species status of the strains, as there was no match to any known species. Polar lipids were extracted and purified from 100 mg dried cells of strain 10aT, B. fusiformis DSM 2898T and B. sphaericus IAM 13420T 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). Strain 10aT shared a similar polar lipid profile with B. fusiformis DSM 2898T and B. sphaericus IAM 13420T, which consisted predominantly of diphosphatidylglycerol, phosphatidylglycerol and ninhydrin-positive phosphoglycolipid (Supplementary Fig. S4). The chemotaxonomic data showed some significant differences when compared with members of closely related genera, particularly the type species of the genus Bacillus in terms of polar lipid analysis (Kämpfer et al., 2006).
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) also demonstrated that Bacillus fusiformis and Bacillus sphaericus should be transferred to the genus Lysinibacillus as Lysinibacillus fusiformis comb. nov. and Lysinibacillus sphaericus comb. nov. Data on peptidoglycan composition and polar lipids of the next-closest phylogenetically related species, B. massiliensis and B. odysseyi, are not available; therefore, inclusion of these species in the genus Lysinibacillus is not recognized here. B. silvestris contains peptidoglycans with L-lysine and D-glutamate and its major polar lipids are phosphatidylglycerol, diphosphatidylglycerol and phosphatidylethanolamine together with minor amounts of phosphatidylserine and an unknown phospholipid. This chemical composition differentiates B. silvestris from members of the novel genus Lysinibacillus.
Description of Lysinibacillus gen. nov
Lysinibacillus (Ly.si'ni.ba.cil'lus. N.L. n. lysinum lysine; L. masc. n. bacillus a small staff or rod; N.L. masc. n. Lysinibacillus lysine bacillus, referring to the presence of the Lys–Asp type of peptidoglycan in the cell wall).
Motile, rod-shaped cells that produce ellipsoidal or spherical endospores which lie terminally in a swollen sporangium. Oxidase and catalase tests are positive, whereas the production of indole and H2S, nitrate reduction and 
-galactosidase (ONPG) tests are negative. Major cellular fatty acid is iso-C15 : 0. Cell-wall peptidoglycan contains lysine and aspartic acid as the diagnostic amino acids, representing the cell wall peptidoglycan type A4 (Lys–Asp). The dominant respiratory lipoquinone system is MK-7. Major polar lipids are diphosphatidylglycerol, phosphatidylglycerol and ninhydrin-positive phosphoglycolipid. The G+C content is 35–38 mol%. The type species is Lysinibacillus boronitolerans.
Description of Lysinibacillus boronitolerans sp. nov.
Lysinibacillus boronitolerans (bo.ro'ni.to'le.rans. N.L. n. boron -onis boron; L. part. adj. tolerans tolerating; N.L. part. adj. boronitolerans boron-tolerating).
In addition to the characteristics described for the genus, the species has the following features. Cells are 3.0–5.0 µm long and 0.8–1.5 µm in diameter. Colonies are circular with entire margins, flat/umbonate elevation, opaque and butyrous in texture and 2–3 mm in diameter after 2 days on NA (pH 7.0) plates at 37 °C. Temperature for growth is 16–45 °C, with optimum growth at 37 °C; there is no growth at 50 °C and little growth at 16 °C after several days. Growth is observed at pH 5.5–9.5, with optimum growth at pH 7.0–8.0 (most rapid initial growth at pH 7.5) but no growth at pH 5.0. Tolerates 0–100 mM boron in agar media, with optimum growth in the absence of boron and some growth at 150 mM boron after 2 days. NaCl is tolerated up to 5 % (w/v), indicating that it is moderately halotolerant. Growth is seen on marine agar 2216, TSA and NA with or without addition of boron or NaCl. Acid is produced from N-acetyl-D-glucosamine, D-xylose (weak) and aesculin (weak) (API 50CH); acid is not produced from carbohydrates (API 20E). Positive for Voges–Proskauer test, urease, L-arginine dihydrolase, tryptophan deaminase and citrate utilization and negative for hydrolysis of gelatin and L-lysine and L-ornithine decarboxylases. Oxidizes the following substrates: D-alanine, glycogen, D-ribose, D-tagatose, inosine, L-alanine, L-alanyl glycine, -cyclodextrin, 2-aminoethanol, L-histidine, L-leucine, L-ornithine, L-proline, L-threonine, acetic acid, glycyl L-glutamic acid, L-lactic acid, L-malic acid, L-glutamic acid, 2'-deoxyadenosine, L-serine, pyruvic acid, methyl pyruvic acid, TMP, monomethyl succinate, UMP, propionic acid, alaninamide, adenosine, AMP, lactamide, L-asparagine, thymidine, uridine, -hydroxybutyric acid, -ketovaleric acid, bromosuccinic acid, cis-aconitic acid, citric acid, DL-lactic acid, formic acid, gluconic acid, glycyl L-aspartic acid, i-erythritol, L-aspartic acid and -ketobutyric acid. Major cellular fatty acids are iso-C15 : 0 (32 %), anteiso-C15 : 0 (21 %), iso-C16 : 0 (11 %), anteiso-C17 : 0 (11 %), C16 : 1
7c alcohol (8 %), iso-C17 : 0 (6 %) and iso-C14 : 0 (2 %). Cell-wall peptidoglycan contains lysine, alanine, glutamic acid and aspartic acid as the diagnostic amino acids. In addition to the polar lipids given in the genus description, it also contains phosphatidylethanolamine. Strong enzyme activity is observed for -chymotrypsin and esterase (C8), whereas weak activity is observed for alkaline phosphatase, esterase lipase (C8), leucine arylamidase, acid phosphatase, valine arylamidase and naphthol-AS-BI-phosphohydrolase (API ZYM). The type strain is resistant to linomycin, colistin, sulfamethizol, oxolinic acid, fusidic acid and metronidazol (ATB-VET). The G+C content of the type strain is 36.5 mol% (determined by HPLC).
Strain 10aT (=DSM 17140T=IAM 15262T=ATCC BAA-1146T) is the type strain, isolated from soil collected in the experimental area of the University of Tokyo (Yayoi campus), Japan.
Description of Lysinibacillus fusiformis comb. nov.
Lysinibacillus fusiformis (fu.si.for'mis. L. n. fusus spindle; L. n. forma shape, form; N.L. adj. fusiformis spindle-shaped).
Basonym: Bacillus fusiformis (ex Meyer and Gottheil 1901) Priest et al. 1988.
The description of the species as given by Priest et al. (1988) is unchanged. Cell-wall peptidoglycan contains lysine, alanine, glutamic acid and aspartic acid in the molar ratio of 1.81 : 1.0 : 0.69 : 0.64 as diagnostic amino acids. Cellular fatty acid profile is listed in Table 3. Major polar lipids are diphosphatidylglycerol, phosphatidylglycerol and ninhydrin-positive phosphoglycolipid. The type strain is DSM 2898T (=JCM 12229T=LMG 9816T=ATCC 7055T).
Description of Lysinibacillus sphaericus comb. nov.
Lysinibacillus sphaericus (sphae'ri.cus. L. masc. adj. sphaericus spherical).
Basonym: Bacillus sphaericus Meyer and Neide 1904.
In addition to the characteristics summarized by Claus & Berkeley (1986), the cellular fatty acid composition is added to the description of the species (Table 3). Major polar lipids are diphosphatidylglycerol, phosphatidylglycerol, ninhydrin-positive phosphoglycolipid and an unknown polar lipid. The type strain is DSM 28T (=LMG 7134T=JCM 2502T=ATCC 14577T=CCM 2120T=NCIMB 9370T=NCTC 10338T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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