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1 Microbiological and Analytical Group, Food Research Laboratories, Mitsui Norin Co. Ltd, 223-1, Miyahara, Fujieda, Shizuoka 426-0133, Japan
2 Institute of Molecular and Cellular Biosciences, University of Tokyo, 1-1, Yayoi 1-chome, Bunkyo-ku, Tokyo 113-0032, Japan
Correspondence
Keiichi Goto
kgoto{at}mnk.co.jp
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Published online ahead of print on 12 September 2003 as DOI 10.1099/ijs.0.02906-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rDNA sequences obtained in this study are AB112712–AB112731, as detailed in Fig. 2
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Tables showing differential characteristics between strain NCIMB 13288T and related Aneurinibacillus strains and between strain DSM 6472T and related Brevibacillus strains, and a figure showing consensus nucleotide sequences, are available as supplementary material in IJSEM Online.
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. Subsequently, many strains, including some that were not in accordance with the criteria of Bacillus brevis sensu stricto, were classified as Bacillus brevis, according mainly to phenotype; as a result, Bacillus brevis has become a heterogeneous species, similar to Bacillus circulans (Nakamura & Swezey, 1983a, b). In the 1990s, based on polyphasic taxonomic studies of Bacillus brevis and its relatives, many species or strains were reclassified as novel species of the genera Brevibacillus and Aneurinibacillus (Nakamura, 1991, 1993; Takagi et al., 1993; Shida et al., 1994a, b, 1995, 1996; Meier-Stauffer et al., 1996; Heyndrickx et al., 1997). Recently, Brevibacillus invocatus was proposed as a novel species, according to the polyphasic identification of Bacillus and Brevibacillus strains from clinical, dairy and industrial specimens (Logan et al., 2002). Thus, at the time of writing, 11 species are recognized to belong to the genus Brevibacillus and three species are recognized to belong to the genus Aneurinibacillus. However, with the exception of the thermophilic species Brevibacillus thermoruber and Aneurinibacillus thermoaerophilus, distinguishing between these species is extremely difficult, as most strains are unreactive or weak in many biochemical tests and few have useful differential phenotypic characteristics (Heyndrickx et al., 1997; Logan et al., 2002). Even with molecular analyses, such as amplified rDNA restriction analysis (ARDRA), identification of these species is not always simple (Logan et al., 2002). In our previous studies, we demonstrated that a hypervariable (HV) region that corresponds to the 5' end of 16S rDNA (nucleotide positions 70–344; Bacillus subtilis numbering) is a useful marker for rapid identification and grouping of Alicyclobacillus species (Goto et al., 2002a, b), Bacillus species (Goto et al., 2000) and Paenibacillus species (Goto et al., 2002c). In this study, to ascertain how well the region is conserved within Brevibacillus species, we investigated sequence similarities among 29 strains that were supplied as Brevibacillus brevis. Fifty-two strains were obtained from DSMZ (Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH, Braunschweig, Germany), IAM (Institute of Molecular and Cellular Biosciences, University of Tokyo, Tokyo, Japan), NBRC/IFO (NITE Biological Resource Center/Institute for Fermentation, Osaka, Japan) and NCIMB (National Collection of Industrial and Marine Bacteria, Aberdeen, UK). All strains were grown in nutrient broth and agar, or brain heart infusion broth and agar (Difco), at the optimum growth temperature (35 or 50 °C).
During phenotypic characterization of organisms, unless indicated otherwise, the methods described by Gordon et al. (1973) were used. Acidification was examined with API 50 CH test strips (bioMérieux) at the optimum growth temperature. Hydrolysis of DNA was determined by using DNase test agar (Difco). Oxidase activity was determined by using the bioMérieux oxidase test. Each test was repeated three times.
For quinone analysis, cells were grown in 100 ml nutrient broth at the optimum growth temperature in a reciprocal shaker for 24 h. Quinones were extracted from freeze-dried cells according to Sano et al. (1996) and analysed by using an Alliance HPLC system that was equipped with a Waters 996 Photodiode Array detector. A Mightysil RP-18 column (4·6x250 mm; Kanto Chemical) was used for separation and methanol/propan-2-ol (3 : 1, v/v) was used as the eluent. Quinones were identified by their UV spectra. For fatty acid analysis, cells were grown on trypticase soy agar (Difco) at the optimum growth temperature for 24 h, as recommended by the manufacturers of the Microbial Identification system (MIS; Microbial ID). Fatty acid methyl esters were extracted from fresh wet biomass by saponification and methylation, according to Bligh & Dyer (1959) and Metcalfe et al. (1996), and analysed by using MIS software (version 4.02).
Genomic DNA was extracted and purified by using a High Pure PCR Template Preparation kit (Roche). For DNA–DNA hybridization, genomic DNA was extracted by using a Qiagen Blood and Cell Culture DNA Maxi kit and purified by equilibrium centrifugation in CsCl/ethidium bromide gradients (Treisman, 1989) by using an OptimaTM MAX Ultracentrifuge (Beckman Coulter). Samples were desalted by using an Ultrafree-4 Centrifugal Filter unit (Millipore). Genetic relatedness was determined fluorometrically with photobiotin-labelled DNA probes and microplates, as described by Ezaki et al. (1989), by using a CytoFluor Series 4000 multiwell plate reader (PerSeptive Biosystems). Hybridization was carried out under stringent conditions (optimal renaturation temperature+15 °C) for 3 h. Renaturation temperatures were based on the DNA G+C contents of the type strains of Aneurinibacillus aneurinilyticus (43·3 %), Bacillus methanolicus (38·6 %), Bacillus oleronius (34·9 %) and Brevibacillus brevis (47·3 %) (Ezaki et al., 1989). Each hybridization experiment was repeated at least three times. DNA G+C contents were determined by HPLC using purified genomic DNA solution, as described previously (Tamaoka & Komagata, 1984), with genomic DNA of Bacillus subtilis IAM 12118T as a control.
Almost-complete sequences were determined by using a 16S rRNA Gene kit (Applied Biosystems). Universal primers for amplification and sequencing of the HV region were: forward primer (F-1), 5'-GCYTAAYACATGCAAGTCGARCG-3' (corresponding to nucleotides 47–69 of Bacillus subtilis 16S rDNA; Y=C/T, R=A/G) and reverse primer (R-1), 5'-ACTGCTGCCTCCCGTAGGAGT-3' (corresponding to nucleotides 345–365 of Bacillus subtilis 16S rDNA). HV region DNA was amplified according to Sadaie et al. (1997) and sequenced by using a BigDye Terminator Cycle Sequencing kit (Applied Biosystems). An ABI Prism model 3100 genetic analyser (Applied Biosystems) was used for electrophoresis and data collection. Sequence analysis was performed by using GeneWorks (version 2.0; IntelliGenetics) and GenBank/EMBL/DDBJ. Multiple sequence alignment was performed with CLUSTAL W version 1.7 (Thompson et al., 1994). Phylogenetic trees were constructed from evolutionary data, which were calculated with Kimura's two-parameter model (Kimura, 1980), by using the neighbour-joining method of Saitou & Nei (1987). Robustness of individual branches was estimated by bootstrapping with 1000 replicates (Felsenstein, 1985).
To ascertain the conservation of the HV region within Brevibacillus brevis and its variation among different Brevibacillus species, we sequenced the HV regions of 29 strains that were identified previously as Brevibacillus brevis, as well as Aneurinibacillus migulanus DSM 8373, A. thermoaerophilus DSM 10155, Brevibacillus agri DSM 6366, Brevibacillus borstelensis DSM 6453, three strains of Brevibacillus sp. (DSM 4410, DSM 4411 and DSM 4412) and all type strains of Aneurinibacillus and Brevibacillus species. The results are summarized in Fig. 1 as a phylogenetic dendrogram, based on a comparison of 239 common nucleotide positions. Of the 29 Brevibacillus brevis strains, 13 clustered with Aneurinibacillus species, eight clustered with Bacillus species and eight clustered with Brevibacillus species. Of the eight that clustered with Brevibacillus species, two clustered with the type strain (DSM 30T), along with Brevibacillus choshinensis DSM 8552T and Brevibacillus formosus DSM 9885T, all showing 100 % sequence similarity. DSM 6472 and NCIMB 13288 did not cluster with any species of the genera Aneurinibacillus or Brevibacillus. Sequence similarity values within the clusters that contained A. migulanus, A. thermoaerophilus, Bacillus oleronius, Brevibacillus agri and Brevibacillus parabrevis were 100 %. In the Bacillus methanolicus cluster, NCIMB 12522, NCIMB 12525, NCIMB 12526, NCIMB 12527 and NCIMB 12528 all showed 100 % sequence similarity to Bacillus methanolicus NCIMB 13113T. However, NCIMB 12523 and NCIMB 12524 differed at five nucleotide positions, including two polymorphic positions, with the closest relative being Bacillus methanolicus NCIMB 13113T. NCIMB 12523 differed from NCIMB 12524 at the two polymorphic sites. On the other hand, A. migulanus DSM 8373, A. thermoaerophilus DSM 10155, Brevibacillus agri DSM 6366 and Brevibacillus borstelensis DSM 6453 clustered with their individual type strains with 100 % sequence similarity. Three strains of Brevibacillus sp. (DSM 4410, DSM 4411 and DSM 4412) also clustered with A. thermoaerophilus DSM 10154T, with 100 % sequence similarity.
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shows informative nucleotide positions among strains of the Brevibacillus brevis–Brevibacillus choshinensis–Brevibacillus formosus cluster. When polymorphic nucleotide positions were removed, the 16S rDNA sequences of Brevibacillus brevis DSM 30T, [Brevibacillus brevis] DSM 5619 and Brevibacillus formosus DSM 9885T were identical, but that of [Brevibacillus brevis] DSM 5760 differed from these three strains at nucleotide positions 612 and 620. By direct sequence comparison, Brevibacillus choshinensis DSM 8552T differed from these four strains at six or seven reliable nucleotide positions (99·5–99·6 % similarity). Thus, Brevibacillus choshinensis DSM 8552T was an outlier of this cluster. However, nine informative nucleotide positions were removed as an alignment gap, making it difficult to describe the phylogeny of these five strains. Fig. 2 shows the phylogenetic tree of type strains of Aneurinibacillus and Brevibacillus species, [Brevibacillus brevis] DSM 6472 and [Brevibacillus brevis] NCIMB 13288, based on a comparison of 1430 common nucleotide positions. DSM 6472 and NCIMB 13288 were members of the genera Brevibacillus and Aneurinibacillus, respectively (these clusters were supported by high bootstrap values of 100 %) but they differed clearly from species with validly published names. 16S rDNA sequence similarity of DSM 6472 to the type strains of Brevibacillus species ranged between 95·4 and 98·8 % and sequence similarity of NCIMB 13288 to type strains of Aneurinibacillus species ranged between 96·8 and 97·9 %. These results indicate that DSM 6472 and NCIMB 13288 are novel species of the genera Brevibacillus and Aneurinibacillus, respectively.
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. The DNA G+C contents of strains in the Aneurinibacillus cluster ranged from 42·9 to 46·7 mol%. The highest value, for [Brevibacillus brevis] NCIMB 13288, was 46·7 mol%. DNA G+C contents of strains in the Bacillus methanolicus cluster ranged from 38·4 to 38·9 mol%, but these values were about 10 mol% lower than values that were estimated by the renaturation rate method (De Ley et al., 1970; Arfman et al., 1992). The DNA G+C content of Bacillus methanolicus NCIMB 13113T, which was determined by the HPLC method at the TORAY Research Center (Tokyo, Japan), was 38·0 mol% (our data, 38·6 mol%); thus, we considered that the discrepancy was due to differences in the methods being used. The DNA G+C content of [Brevibacillus brevis] NCIMB 8774 (34·8 mol%) was in good accordance with the value from Bacillus oleronius DSM 9356T. DNA G+C contents of strains in the Brevibacillus cluster ranged from 40·4 to 57·3 mol% and grouped well within each species cluster, respectively. The DNA G+C content of [Brevibacillus brevis] DSM 6472 was in the middle of the range, at 51·9 mol%.
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. In the clusters of A. migulanus, A. thermoaerophilus, Bacillus oleronius, Brevibacillus agri, Brevibacillus borstelensis and Brevibacillus parabrevis, there was at least 83 % DNA–DNA relatedness between the type strain and other strains; thus, strains belonged to a single species within each cluster.
In the Bacillus methanolicus cluster, six strains with identical HV region sequences showed >95 % DNA–DNA relatedness to the type strain of Bacillus methanolicus and were thus considered to belong to this species. On the other hand, strains NCIMB 12523 and NCIMB 12524 showed intermediate DNA–DNA relatedness values (52–63 %) to other strains in the cluster, indicating some internal heterogeneity within Bacillus methanolicus (Arfman et al., 1992). Although strains NCIMB 12523 and NCIMB 12524 could be subspecies of Bacillus methanolicus, we regarded strains NCIMB 12522–NCIMB 12528 as provisional members of Bacillus methanolicus, in agreement with Arfman et al. (1992).
Brevibacillus brevis DSM 30T, DSM 5619, DSM 5760 and Brevibacillus formosus DSM 9885T showed intermediate DNA–DNA relatedness (46–61 %). A previous study (Shida et al., 1995) reported that DNA–DNA relatedness between the type strains of Brevibacillus brevis and Brevibacillus formosus was 6 %. In our study, DNA–DNA relatedness values were intermediate (46–61 %), which is consistent with their highly similar 16S rDNA sequences (Amann et al., 1992; Hiraishi & Ueda, 1994; Stackebrandt & Goebel, 1994) and almost-identical DNA G+C contents (47·0–47·3 mol%). Thus, Brevibacillus brevis and Brevibacillus formosus are closely related genetically and, furthermore, there are strains that are intermediate between the species. These observations are also supported by a previous polyphasic taxonomic study (Logan et al., 2002). Although we tentatively regarded DSM 5619 and DSM 5760 as members of Brevibacillus brevis, further taxonomic studies are necessary to certify Brevibacillus brevis and Brevibacillus formosus as independent species. On the other hand, Brevibacillus choshinensis DSM 8552T, an outlier of the cluster based on 16S rDNA sequence analysis, had an HV region sequence that was almost identical to those of these strains (Table 1) and showed low DNA–DNA relatedness (10–19 %) to the other strains in the cluster. In API and other phenotypic analyses, Brevibacillus choshinensis could be distinguished from strains of Brevibacillus brevis and Brevibacillus formosus, whereas strains of Brevibacillus brevis and Brevibacillus formosus were indistinguishable (Logan et al., 2002); thus, Brevibacillus choshinensis could be regarded as an independent species.
NCIMB 13288 had 8–38 % DNA–DNA relatedness to strains within the Aneurinibacillus cluster. On the other hand, DSM 6472 had 8–12 % DNA–DNA relatedness to strains within the Brevibacillus cluster. DNA–DNA hybridization data and 16S rDNA sequence analysis suggested that these strains were novel species of the genera Aneurinibacillus and Brevibacillus, respectively, and further taxonomic studies were carried out.
Differential phenotypic characteristics between DSM 6472 and closely related Brevibacillus reference strains, and between NCIMB 13288 and Aneurinibacillus type strains, are shown as Supplementary Tables A and B in IJSEM Online. Many biochemical characteristics of DSM 6472 were unreactive, but the strain could be distinguished from phylogenetically related species by a combination of characteristics. However, distinguishing between strains remained difficult as currently available phenotypic tests produced either no results or unreliable results from replicates (Logan et al., 2002).
NCIMB 13288 grew aerobically at 35 and 55 °C, but not at 30 or 60 °C; its optimal growth temperature was 45–50 °C. This thermophilic property clearly distinguished NCIMB 13288 from the mesophilic species A. aneurinilyticus and A. migulanus. Whilst NCIMB 13288 and A. thermoaerophilus are both thermophilic species, several characteristics distinguish them from each other (see Supplementary Table A, available in IJSEM Online).
The major respiratory quinone of DSM 6472 and NCIMB 13288 was menaquinone 7 (MK-7). The fatty acid profiles of DSM 6472, NCIMB 13288 and type strains of Aneurinibacillus species were investigated (Table 3). In DSM 6472, major fatty acids were iso-C15 : 0 (21·29 %), anteiso-C15 : 0 (41·74 %) and iso-C16 : 0 (12·40 %). The profile of DSM 6472 was similar to those of other Brevibacillus species, but could be distinguished from them by a larger amount of iso-C16 : 0 (12·40 %). In NCIMB 13288, major fatty acids were iso-C15 : 0 (57·67 %), C16 : 0 (6·34 %) and iso-C17 : 0 (7·99 %); thus, this strain can be discriminated from other Aneurinibacillus species by lower amounts of anteiso-C15 : 0, iso-C16 : 0 and C16 : 1
11cis. Whilst fatty acid analysis may play a part in a polyphasic approach, we considered that it was not reliable on its own for identification of most taxa in the Bacillus group sensu lato, including Aneurinibacillus and Brevibacillus, as some other researchers have also suggested (Kämpfer, 1994; Logan et al., 2002).
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). Whilst some strains show extremely close relationships between or within species, large-scale taxonomic studies that use many isolates and authentic strains are needed. Moreover, polyphasic taxonomic analyses clearly demonstrate that strains NCIMB 13288 and DSM 6472 are novel species of the genera Aneurinibacillus and Brevibacillus, respectively; therefore, the names Aneurinibacillus danicus sp. nov. and Brevibacillus limnophilus sp. nov. are proposed. The revived name Brevibacillus limnophilus is used for strain DSM 6472T, which was originally deposited in the ARS Culture Collection as ‘Bacillus limnophilus’ by Porter in 1940 and was later identified as Bacillus brevis. In members of the genera Aneurinibacillus and Brevibacillus, the HV region sequence is conserved within species and has diverged between species, enabling identification and grouping, as we have already shown for Alicyclobacillus, Bacillus and Paenibacillus. Whilst there are still a few genera that have not yet been investigated, the HV region sequence is a powerful index for rapid and convenient identification and grouping of aerobic spore-formers. This method is of particular significance to the food industry and is gradually being used more widely. Consensual nucleotide sequences among species of the genera Aneurinibacillus and Brevibacillus are shown as a Supplementary Figure in IJSEM Online.
Description of Aneurinibacillus danicus sp. nov.
Aneurinibacillus danicus (da'ni.cus. N.L. adj. danicus Danish, pertaining to Denmark).
Gram-variable, strictly aerobic, motile, ellipsoidal spore-forming, straight rods (4·0–6·0 µm long and 0·8–1·0 µm wide). Ellipsoidal spores are oval and subterminal with swollen sporangia. Colonies on nutrient agar are circular, entire, smooth, flat, translucent and white (5–10 mm in diameter after 48 h). Temperature range for growth is 35–55 °C; optimum growth temperature is 45–50 °C. Optimum pH is 6·5–7·0; growth does not occur at pH 5·5 or 8·0. NCIMB 13288T fails to grow in nutrient broth that contains >5 % (w/v) NaCl and under anaerobic conditions. Positive for oxidase and catalase (weak), but negative for urease, utilization of citrate and nitrate reductase. Aesculin, casein, tyrosine (weak), gelatin and DNA are hydrolysed, but arbutin and starch are not. Acid is produced from glycerol, erythritol (weak), D-arabinose, L-arabinose (weak), D-xylose, L-xylose, ribose, adonitol, D-fructose, D-mannose, L-sorbose, dulcitol, sorbitol, xylitol, D-lyxose, D-tagatose and D-arabitol. Major fatty acids are iso-C15 : 0, C16 : 0 and iso-C17 : 0. Main quinone is MK-7. DNA G+C content is 46·7 mol%.
The type strain is NCIMB 13288T (=IAM 15048T).
Description of Brevibacillus limnophilus sp. nov.
Brevibacillus limnophilus (lim.no'phi.lus. Gr. n. limnos lake; L. adj. philus from Gr. adj. philos loving, friendly to; N.L. masc. adj. limnophilus lake-loving).
Gram-variable, strictly aerobic, motile, ellipsoidal spore-forming, straight rods (2·2–4·0 µm long and 0·5–0·6 µm wide). Ellipsoidal spores are oval and subterminal with swollen sporangia. Colonies on nutrient agar are circular, entire, smooth, convex, translucent and whitish-beige (3–4 mm in diameter after 48 h). Temperature range for growth is 20–45 °C; optimum growth temperature is 30–35 °C. Optimum pH is 7·0–7·5; growth does not occur at pH 6·0 or 8·5. DSM 6472T fails to grow in nutrient broth that contains >2 % (w/v) NaCl and under anaerobic conditions. Positive for catalase, but negative for oxidase and urease activities, utilization of citrate and nitrate reductase. Aesculin and DNA (weak) are hydrolysed, but arbutin, casein, gelatin, starch and tyrosine are not. Acid is produced from glycerol, L-arabinose, rhamnose, ribose and D-fructose. Major fatty acids are iso-C15 : 0, anteiso-C15 : 0 and iso-C16 : 0. Main quinone is MK-7. DNA G+C content is 51·9 mol%.
The type strain is DSM 6472T (=NRRL NRS-887T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
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P. Scheldeman, A. Pil, L. Herman, P. De Vos, and M. Heyndrickx Incidence and Diversity of Potentially Highly Heat-Resistant Spores Isolated at Dairy Farms Appl. Envir. Microbiol., March 1, 2005; 71(3): 1480 - 1494. [Abstract] [Full Text] [PDF]
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