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Bacillus decisifrondis sp. nov., isolated from soil underlying decaying leaf foliage

¹ Microbial Gene Research and Resources Facility, School of Biomolecular and Biomedical Sciences, Faculty of Science, Griffith University, Brisbane, QLD 4111, Australia
² Center for Forestry and Horticultural Research and Australian School of Environmental Studies, Faculty of Environmental Sciences, Griffith University, Brisbane, QLD 4111, Australia

Correspondence
Bharat K. C. Patel
b.patel{at}griffith.edu.au

	ABSTRACT

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An aerobic bacterium, designated strain E5HC-32^T, was isolated from soil underlying the decaying leaf litter of a slash pine forest located in south east Queensland, Australia. The strictly aerobic, motile rod-shaped cells (0.8–1.6x2.6–4.8 µm) produced subterminal spherical spores which distended the cells. Strain E5HC-32^T grew optimally in 1 % trypticase soy broth (TSB) at 30 °C (temperature range for growth, 25–40 °C) and a pH of 8.4 (pH growth range, pH 7.1–9.1). Electron microscopic examination of negatively stained cells revealed the presence of peritrichous flagella and thin sections showed the presence of a typical Gram-positive type cell-wall ultrastructure. The strain was catalase-positive and oxidase-negative and metabolized pyruvic acid methyl ester, D-galactonic acid lactone, -ketobutyric acid, -ketovaleric acid, L-proline, L-alanine, urocanic acid, inosine, uridine, thymidine, glycerol, -cyclodextrin, -D-lactose, D-psicose, D-raffinose, L-rhamnose, D-sorbitol, turanose, cis-aconitic acid, -hydroxybutyric acid, L-alaninamide and 2-aminoethanol. The G+C content of DNA was 41±1 mol% as determined by the thermal denaturation method. 16S rRNA gene sequence analysis revealed that strain E5HC-32^T was placed equidistantly as a member of the class Bacilli, phylum Firmicutes, with Bacillus sphaericus DSM 28^T and Bacillus odysseyi ATCC PTA-4993^T (similarity of 93 %). In addition to its significant phylogenetic separation from its nearest relatives, strain E5HC-32^T possessed phenotypic traits that also suggested that it represented a novel species, for which the name Bacillus decisifrondis sp. nov. is proposed. The type strain is E5HC-32^T (=JCM 13601^T=DSM 17725^T).

Transmission electron micrographs of cells of strain E5HC-32^T are available as a supplementary figure in IJSEM Online.

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Soil is one of the most complex and heterogeneous environments and contains significant microbial diversity (Tiedje et al., 1999). Although the microbiology of soils has been investigated for over a hundred years and many novel strains have been isolated recently, many more strains have so far eluded cultivation (Sait et al., 2002). One of the dominant groups in soils is the spore-forming group of the class Bacilli, phylum Firmicutes. A wide variety of spore morphologies have so far been observed in this class, with the round-spore-formers being one of the least represented. Although the first round-spore-forming Bacillus was described in 1898 (Chester, 1898) and Bacillus sphaericus DSM 28T was isolated and characterized in 1904 (Neide, 1904), the taxonomic study of this group languished due to the lack of differentiating methods until the recent advent of molecular biological techniques. 16S rRNA gene sequence analysis has shown that most of the round-spore-formers cluster in Bacillus rRNA group 2 (Ash et al., 1991) and include Bacillus fusiformis ATCC 7055^T (Priest et al., 1988), Bacillus insolitus DSM 5^T (Nakamura, 2000), Bacillus neidei NRRL BD-101 (Nakamura et al., 2002), Bacillus pycnus NRRL NRS-1691^T (Nakamura et al., 2002), B. sphaericus DSM 28^T (Nakamura, 2000), Bacillus silvestris DSM 12223^T (Rheims et al., 1999), Ureibacillus thermosphaericus DSM 10633^T (formerly Bacillus thermosphaericus) (Nakamura, 2000; Fortina et al., 2001) and Bacillus odysseyi ATCC PTA-4993^T (La Duc et al., 2004) and Sporosarcina globispora DSM 4^T (formerly Bacillus globisporus), Sporosarcina psychrophila ATCC 23304^T (formerly Bacillus psychrophilus) and Sporosarcina pasteurii DSM 33^T (formerly Bacillus pasteurii) (Yoon et al., 2001). In this study, we report the isolation of a novel round-spore-forming bacterium, designated strain E5HC-32^T, which was isolated from soil underlying the decaying leaf litter of a slash pine forest located in south east Queensland, Australia.

For the isolation of strain E5HC-32^T, a 10 g moist soil sample was vortexed with 50 ml of sterile distilled water for 5 min. The suspension was then rocked horizontally for 5 min, serial ten-fold dilutions were prepared and 100 µl of the mixture was spread onto trypticase soy broth (TSB) Gelrite plates, pH 7.2 that contained (g l^–1); 3 g TSB, 2.033 g MgCl₂.6H₂O, 0.882 g CaCl₂.2H₂O and 20 g Gelrite. The plates were incubated at room temperature (25 °C) for up to 6 days. Morphologically distinct single colonies that developed were picked up and restreaked onto fresh TSB Gelrite plates at least twice before being considered pure. Several pure isolates with different colony morphologies were selected and stored in 0.3 % TSB containing 15 % glycerol at –80 °C. One of the isolates that produced cream, round, smooth colonies after 3–5 days of incubation at 30 °C was designated strain E5HC-32^T and characterized further.

Cell morphology was determined by phase-contrast microscopy and by electron microscopy (Kanso & Patel, 2003). Cells of strain E5HC-32^T were motile, rod-shaped (0.8–1.6x2.6–4.8 µm) and produced subterminal spherical spores which distended the cells. Electron microscopy of negatively stained cells showed the presence of peritrichous flagella and examination of thin sections revealed the presence of a typical single, thick Gram-positive cell-wall ultrastructure (see Supplementary Fig. S1 in IJSEM Online).

The conditions for growth of strain E5HC-32^T were tested in different concentrations of TSB (up to 3 %) with temperatures ranging from 25 to 50 °C and pH ranging from 5.1 to 9.5. Growth was measured at 660 nm in a spectrophotometer (Novaspec LKB; Pharmacia-Biotech Pty Ltd) and generation time was calculated using standard microbiological practice. Strain E5HC-32^T grew optimally at 30 °C (growth temperature range of between 25 and 40 °C) with a pH of 8.4 (pH range for growth of between 7.1 and 9.1). The generation time under these optimal conditions (1 % TSB, pH 8.4 and incubation temperature of 30 °C) was determined to be 4 h. All subsequent growth experiments were conducted using these conditions.

The metabolic profile of strain E5HC-32^T was examined with GN2 Biolog plates (Hayward). For this analysis, the strain was grown on Biolog Universal Growth (BUG) medium agar plates. An inoculum was prepared from the colonies that developed on these plates and was subsequently used to inoculate the wells of the GN2 Biolog plates as recommended by the manufacturer. After 24 h incubation at 30 °C, the absorbances in the wells of the microtitre plates were read and the results transformed into positive, borderline and negative scores by the Biolog MicroStation System software program. Strain E5HC-32^T metabolized pyruvic acid methyl ester, D-galactonic acid lactone, -ketobutyric acid, -ketovaleric acid, L-proline, L-alanine, urocanic acid, inosine, uridine, thymidine, glycerol, -cyclodextrin, -D-lactose, D-psicose, D-raffinose, L-rhamnose, D-sorbitol, turanose, cis-aconitic acid, -hydroxybutyric acid, L-alaninamide and 2-aminoethanol, but not dextrin, glycogen, Tween 40, Tween 80, N-acetyl-D-galactosamine, N-acetyl-D-glucosamine, adonitol, L-arabinose, D-arabitol, D-cellobiose, i-erythritol, D-fructose, L-fucose, D-galactose, gentiobiose, -D-glucose, myo-inositol, lactulose, maltose, D-mannitol, D-mannose, D-melibiose, methyl -D-glucoside, sucrose, D-trehalose, xylitol, succinic acid monomethyl ester, acetic acid, citric acid, formic acid, D-galacturonic acid, D-gluconic acid, D-glucosaminic acid, D-glucuronic acid, -hydroxybutyric acid, -hydroxybutyric acid, p-hydroxyphenylacetic acid, itaconic acid, -ketoglutaric acid, DL-lactic acid, malonic acid, propionic acid, quinic acid, D-saccharic acid, sebacic acid, succinic acid, bromosuccinic acid, succinamic acid, glucuronamide, D-alanine, L-alanyl glycine, L-asparagine, L-aspartic acid, L-glutamic acid, glycyl L-aspartic acid, glycyl L-glutamic acid, L-histidine, hydroxy-L-proline, L-leucine, L-ornithine, L-phenylalanine, L-pyroglutamic acid, D-serine, L-serine, L-threonine, DL-carnitine, -aminobutyric acid, phenyethylamine, putrescine, 2,3-butanediol, DL--glycerol phosphate, -D-glucose 1-phosphate or D-glucose 6-phosphate. The strain hydrolysed casein, but not starch, as determined by the method of Kanso & Patel (2003). Catalase but not oxidase was produced as determined by the H₂O₂ and oxidase detection strips (MedVet Science Ltd), respectively. Strain E5HC-32^T was a strict aerobe and could not grow in anaerobic 1 % TSB medium that had been prepared using the method of Andrews & Patel (1996).

For genomic DNA purification, a 50 ml actively growing culture was centrifuged at 5400 r.p.m. for 20 min at 4 °C (4K15; Sigma) and the pellet was resuspended in 4 ml buffer A (5 mM Tris HCl pH 8.0, 100 mM NaCl and 5 mg lysozyme). After incubation on ice for 5 min, 0.85 ml buffer [300 mM EDTA pH 7.5 and 5 % (w/v) SDS] and 100 µl of 20 mg proteinase K ml^–1 were added and the mixture was incubated at 55 °C overnight. An equal volume of phenol : chloroform : isoamyl alcohol (25 : 24 : 1) was added, the mixture was gently agitated for 30 min, after which 3 volumes of cold 100 % ethanol were carefully overlaid and the flocculent DNA at the interface was spooled onto a sterile disposable loop. The spooled DNA was resuspended in 5 ml TE buffer (10 mM Tris HCl pH 7.4, 1 mM EDTA pH 8) and the quality was assessed by agarose gel electrophoresis, ethidium bromide staining and visualization under a UVP GDAS 1200 gel documentation analysis system (UVP Inc). The mol% G+C content of the genomic DNA was determined by the thermal denaturation method (Marmur & Doty, 1961) using a spectrophotometer (Cintra20; GBC Scientific Equipment) as previously described (Spanevello et al., 2002). The G+C content of the DNA of strain E5HC-32^T was determined to be 41±1 mol%.

For studies on the 16S rRNA gene, 10 ml of an overnight culture of strain E5HC-32^T was centrifuged at 5400 r.p.m. for 20 min at 4 °C (4K15; Sigma), the pellet was resuspended in 100 µl TE buffer and the cells were lysed by boiling for 15 min. The lysate was centrifuged at 14 000 r.p.m. for 15 min in a microcentrifuge (model 1-15; Sigma) and 2 µl aliquots of the supernatant were used as a template for the amplification of the 16S rRNA gene (Andrews & Patel, 1996). Sequencing of the gene was performed essentially as described previously (Andrews & Patel, 1996). The partial sequences that were generated were assembled using BioEdit v5.0.1 (Hall, 1999) and the consensus sequence of 1305 nucleotides was manually corrected for errors. The most closely related sequences in GenBank (version 152) and the Ribosomal Database Project II (release 9.37) databases identified using BLAST (Altschul et al., 1997) and the Sequence Match program (Cole et al., 2005) were extracted, aligned and manually adjusted according to the 16S rRNA secondary structure using BioEdit. Sequence uncertainties were omitted and phylogenetic reconstruction was achieved using TREECON (Van de Peer et al., 1997) in which pairwise evolutionary distances were computed from percentage similarities (Jukes & Cantor, 1969) and phylogenetic trees were constructed from evolutionary distances using the neighbour-joining method (Saitou & Nei, 1987). Tree topology was re-examined by the bootstrap method of resampling (Felsenstein, 1985) using 1000 bootstraps. Phylogeny was also re-evaluated using ARB phylogenetic software which had been compiled on a Linux platform (Ludwig et al., 2004). For analysis, the 16S rRNA gene sequence of strain E5HC-32^T was first aligned against the Hugenholz 16S rRNA dataset using the NAST aligner tool (http://greengenes.lbl.gov/cgi-bin/nph-index.cgi) and the aligned sequence was imported into the ARB program for further phylogenetic analysis. Both phylogenetic analyses concurred and indicated that strain E5HC-32^T shared a close phylogenetic relationship with the round-spore-forming Bacillus rRNA group 2 (Ash et al., 1991) which included B. fusiformis ATCC 7055^T (Priest et al., 1988), B. insolitus DSM 5^T (Nakamura, 2000), B. neidei NRRL BD-101 (Nakamura et al., 2002), B. pycnus NRRL NRS-1691^T (Nakamura et al., 2002), B. sphaericus DSM 28^T (Nakamura, 2000), B. silvestris DSM 12223^T (Rheims et al., 1999), U. thermosphaericus DSM 10633^T (formerly B. thermosphaericus) (Nakamura, 2000; Fortina et al., 2001), B. odysseyi ATCC PTA-4993^T (La Duc et al., 2004), S. globispora DSM 4^T, S. psychrophila ATCC 23304^T and S. pasteurii DSM 33^T (Yoon et al., 2001) with a mean gene sequence similarity of 91 %.

Strain E5HC-32^T shares a number of phenotypic characteristics with its neighbours that include the ability to metabolize pyruvate, amino acids, purines and pyrimidines, but not hexoses, pentoses or disaccharides. The closest phylogenetic relatives of strain E5HC-32^T were B. sphaericus DSM 28^T (Nakamura, 2000) and B. odysseyi ATCC PTA-4993^T (La Duc et al., 2004) which were equidistantly placed from strain E5HC-32^T (gene sequence similarity of 93 %) (Fig. 1). This large distance separating strain E5HC-32^T from its two nearest neighbours and a number of phenotypic differences that are set out in Table 1 suggest that strain E5HC-32^T represents a novel species. We propose that strain E5HC-32^T represents a novel species, Bacillus decisifrondis sp. nov., in the Bacillus rRNA group 2.

View larger version (30K): [in this window] [in a new window]   Fig. 1. The phylogenetic position of Bacillus decisifrondis strain E5HC-32T within the radiation of members of the round-spore-forming, family Planococcaceae, order Bacillales, phylum Firmicutes, sometimes referred to as the Bacillus rRNA group 2. GenBank accession numbers are given in parentheses. Ureibacillus thermosphaericus DSM 10633T (AJ292316) and Ureibacillus terrenus DSM 12654T (AJ276403) represent the Ureibacillus cluster, Kurthia sibirica DSM 4747T (AJ605774) and Kurthia gibsonii ATCC 43195T (AY123716) represent the Kurthia cluster; Planococcus kocurii DSM 20747T (AF145718), Planococcus citreus DSM 20549T (AF500008) represent the Planococcus cluster and Planomicrobium alkanoclasticum NCIMB 13489T (AF029364) and Planomicrobium okeanokoites NBRC 12536T (AF145719) represent the Planomicrobium clusters. Bootstrap values above 95 % from 1000 replicates are shown. Bar, 10 nucleotide changes.

Description of Bacillus decisifrondis sp. nov.
Bacillus decisifrondis (de.ci.si.fron'dis. L. part. adj. decisus thrown off, dead, died; L. n. frons frondis of/from foliage; N.L. gen. n. decisifrondis from thrown off decayed foliage).

Cell size is 0.8–1.6 µmx2.6–4.8 µm. Electron microscopy of the type strain reveals the presence of peritrichous flagella, round spores, inclusion bodies and a rough outer wall surface. Growth is strictly aerobic and occurs at temperatures between 25 and 40 °C (optimum temperature, 30 °C) and at pH values of 7.1 to 9.1 (optimum pH, 8.4). Able to metabolize the following in GN2 Biolog plates: pyruvic acid methyl ester, D-galactonic acid lactone, -ketobutyric acid, -ketovaleric acid, L-proline, urocanic acid, inosine, uridine, thymidine, glycerol, -cyclodextrin, -D-lactose, D-psicose, D-raffinose, L-rhamnose, D-sorbitol, turanose, cis-aconitic acid, -hydroxybutyric acid, L-alaninamide, L-alanine and 2-aminoethanol. Does not metabolize the following in GN2 Biolog plates: dextrin, glycogen, Tween 40, Tween 80, N-acetyl-D-galactosamine, N-acetyl-D-glucosamine, adonitol, L-arabinose, D-arabitol, D-cellobiose, i-erythritol, D-fructose, L-fucose, D-galactose, gentiobiose, -D-glucose, myo-inositol, lactulose, maltose, D-mannitol, D-mannose, D-melibiose, methyl -D-glucoside, sucrose, D-trehalose, xylitol, succinic acid monomethyl ester, acetic acid, citric acid, formic acid, D-galacturonic acid, D-gluconic acid, D-glucosaminic acid, D-glucuronic acid, -hydroxybutyric acid, -hydroxybutyric acid, p-hydroxyphenylacetic acid, itaconic acid, -ketoglutaric acid, DL-lactic acid, malonic acid, propionic acid, quinic acid, D-saccharic acid, sebacic acid, succinic acid, bromosuccinic acid, succinamic acid, glucuronamide, D-alanine, L-alanyl glycine, L-asparagine, L-aspartic acid, L-glutamic acid, glycyl-L-aspartic acid, glycyl L-glutamic acid, L-histidine, hydroxy-L-proline, L-leucine, L-ornithine, L-phenylalanine, L-pyroglutamic acid, D-serine, L-serine, L-threonine, DL-carnitine, -aminobutyric acid, phenylethylamine, putrescine, 2,3-butanediol, DL--glycerol phosphate, -D-glucose 1-phosphate and D-glucose 6-phosphate. Hydrolyses casein but not starch and produces catalase but not oxidase. The DNA G+C content is 41±1 mol%.

The type strain, E5HC-32^T (=JCM 13601^T=DSM 17725^T), was isolated from soil underlying the decaying leaf litter of slash pine forest in south east Queensland, Australia.

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