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Extremobiosphere Research Center, Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan
Correspondence
Yuichi Nogi
nogiy{at}jamstec.go.jp
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Bacillus wakoensis JCM 9140T, Bacillus hemicellulosilyticus JCM 9152T, Bacillus cellulosilyticus JCM 9156T, Bacillus akibai JCM 9157T and Bacillus mannanilyticus JCM 10596T are AB043851, AB043846, AB043852, AB043858 and AB043864, respectively.
Tables detailing the growth characters, the utilization of carbohydrate substrates and fatty acid profiles of the five novel species are available as supplementary material in IJSEM Online.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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), cyclomaltodextrin glucanotransferase (CGTase) (Yamamoto et al., 1972) and cellulase (Horikoshi et al., 1971). These species produce extracellular enzymes that are resistant to high pH and/or high temperature conditions (Nielsen et al., 1995; Horikoshi, 1999). Since Vedder (1934) first isolated the aerobic, endospore-forming, obligate alkaliphilic bacterium Bacillus alcalophilus, many obligately or facultatively alkaliphilic Bacillus strains have been isolated for use in industry, biotechnology and physiology (Horikoshi, 1999). However, the majority of these strains have not been identified at the species level. The aim of this study was to classify a collection of 20 industrially important alkaliphilic Bacillus strains at the species level. |
METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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. The strains were stored as a working collection at 5 °C on Horikoshi II agar slopes (10 g glucose, 5 g polypeptone, 5 g yeast extract, 10 g NaCl, 1 g K2HPO4, 0·2 g MgSO4.7H2O, 15 g agar, 900 ml distilled water, pH 9, to which 100 ml 10 % NaHCO3 solution was added aseptically after autoclaving).
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Cellular fatty acids and respiratory lipoquinones.
Alkaliphilic Bacillus strains were cultured in Horikoshi II broth at pH 9 and 30 °C for 2 days, under which conditions all strains exhibited growth. Cells were washed twice with 0·7 % NaCl at 4 °C followed by centrifugation at 8000 g and freeze-drying. Dried cells (20 mg) were placed in Teflon-lined, screw-capped tubes containing 2 ml anhydrous methanolic HCl and heated to 100 °C for 3 h. After cooling, 1 ml water was added and the fatty acid methyl esters were extracted with n-hexane. Samples were analysed for cellular fatty acids using a gas-liquid chromatography/mass spectrometer (Komagata & Suzuki, 1987).
Isoprenoid quinones were extracted with chloroform/methanol (2 : 1) from dried cells (200 mg) and purified on TLC. The purified isoprenoid quinones were analysed using reverse-phase HPLC (Komagata & Suzuki, 1987).
Genotypic characterization.
Chromosomal DNA was purified using a standard method (Saito & Miura, 1963). The DNA G+C content was determined using reverse-phase HPLC (Tamaoka & Komagata, 1984). For analysis of relatedness, DNA–DNA hybridization was carried out at 40 °C for 4 h and measured fluorometrically using the method of Ezaki et al. (1989).
16S rRNA gene sequences were obtained by direct sequencing of PCR-amplified DNA as described previously (Kato et al., 1998). Nucleotide substitution rates (Knuc) (Kimura, 1980) were determined and a distance matrix tree was constructed with the neighbour-joining method (Saitou & Nei, 1987) using the CLUSTAL_X program (Thompson et al., 1997). Alignment gaps and unidentified base positions were not taken into consideration for the calculations. The topology of the phylogenetic tree was evaluated by performing a bootstrap analysis with 1000 replicates. The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of the isolates are shown in Fig. 1. Other reference sequences were obtained from the GenBank database.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTS AND DISCUSSIONREFERENCES |
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; Stackebrandt & Goebel, 1994; Stackebrandt et al., 2002). However, bacterial strains with a difference in 16S rRNA gene sequence of less than 3 % cannot be allocated to the same species without support from DNA–DNA relatedness studies. In the 16S rRNA gene sequence clustering, 12 groups of strains that showed a high degree of internal sequence similarity (98·3–99·7 %) could be delineated. In the neighbour-joining tree, the sequences form a distinct lineage, with alkaliphilic Bacillus species as the closest relatives (Fig. 1
). The DNA–DNA hybridization values between Bacillus clausii DSM 8716T and strains O-4, H-167 and IC were greater than 89 % and therefore these three strains were identified as B. clausii. DNA–DNA relatedness values between Bacillus pseudofirmus DSM 8715T and strains 8-1, 2b-2 and 27-1 were greater than 80 % and therefore these three strains were identified as B. pseudofirmus. For Bacillus halodurans DSM 497T and strains C-3 and 202-1, DNA–DNA relatedness was greater than 93 % and therefore these two strains were identified as B. halodurans. Between Bacillus cohnii DSM 6307T and strains D-6 and 199, DNA–DNA relatedness was greater than 78 % and therefore these two strains were identified as B. cohnii. The DNA–DNA hybridization value of 98 % indicated that Bacillus agaradhaerens DSM 8721T and strain S-2 represent the same species and a value of 70 % indicated that Bacillus horikoshii DSM 8719T and strain KX-6 also represent the same species.
The 16S rRNA gene sequence analysis showed that strains 13, 17-1, K-12-5 and DSM 8717 are closely related to each other (99·1–99·7 %). The DNA–DNA reassociation values among strains 13, 17-1, K-12-5 and DSM 8717 were greater than 80 % and therefore these four strains were identified as representatives of the same species. According to the sequence similarity values and results of the phylogenetic analysis based on these 16S rRNA gene sequences, these strains are most closely related to Bacillus oshimensis JCM 12663T (98·4–98·5 %). The DNA–DNA reassociation value between strain DSM 8717 and B. oshimensis JCM 12663T was 67·6 % (Yumoto et al., 2005). Yumoto et al. (2005) found seven characteristics that differentiated B. oshimensis JCM 12663T from DSM 8717. In this study, three of these characteristics, hydrolysis of Tweens 20, 40 and 60, were found to be the same for B. oshimensis JCM 12663T and DSM 8717 and another of these characteristics, lower temperature for growth, was found to be variable for each strain. On the basis of these observations, these strains were identified as representatives of the same species. However, according to the results of the 16S rRNA gene sequence analysis, strains N-1T and 1139T were closely related to Bacillus krulwichiae JCM 11691T (97·4 and 96·1 %, respectively, and between strain N-1T and 1139T the sequence similarity value was 97·1 %), but the DNA–DNA relatedness values between strains N-1T and 1139T and B. krulwichiae JCM 11691T were less than 30 %, and therefore these strains were identified as representing a novel species.
In the 16S rRNA gene sequence analysis, strain C-11T was closely related to Bacillus alcalophilus DSM 485T (96·3 %), B. halodurans ATCC 27557T (96·1 %), Bacillus okuhidensis JCM 10945T (96·1 %) and strain 1139T (96·3 %), but the respective DNA–DNA reassociation values between strain C-11T and these type strains were less than 25 %, and therefore this strain was identified as representing a novel species. The 16S rRNA gene sequence analysis showed that strain N-4T was closely related to Bacillus vedderi DSM 9768T (97·4 %), but the DNA–DNA reassociation value between strain N-4T and this type strain was less than 27 % and therefore this strain was identified as representing a novel species. In the 16S rRNA gene sequence analysis of strain AM-001T, the highest similarity was observed with Bacillus horti JCM 9943T (94·1 %). The DNA–DNA relatedness value between strain AM-001T and this type strain was less than 20 % and therefore this strain was identified as representing a novel species.
Physiological and biochemical characteristics
Phenotypic characteristics of the 20 alkaliphilic Bacillus strains and alkaliphilic Bacillus type strains are shown in Table 2 and in Supplementary Table S1 in IJSEM Online, respectively. The utilization of carbohydrate substrates for the novel species, as deduced from the Biolog tests, is shown in Supplementary Table S2 in IJSEM Online. A comparison of the physiological and biochemical characteristics of the five groups showed some differences when compared with the type strains and with each other. Strain N-1T and B. pseudoalcalophilus grew at similar temperatures (10–40 °C), pH (8–10) and NaCl concentration (0–10 %), but showed varying results for the hydrolysis of casein and gelatin and for the reduction of nitrate. Strains C-11T and N-1T grew at similar temperatures, pH and NaCl concentrations (C-11T: 10–40 °C, pH 8–11, 0–12 % NaCl; N-1T: 20–40 °C, pH 8–10, 0–12 % NaCl) as B. clarkii (20–45 °C, pH 8–11, 0–12 % NaCl) and B. krulwichiae (temperature range not determined, pH 8–10, 0–12 % NaCl), although their hydrolysis of casein and gelatin and their menaquinone content were different. Strain C-11T also showed characteristic utilization of the carbohydrate substrates D-melibiose, D-raffinose and stachyose. Strain 1139T and B. cohnii displayed growth at similar temperatures, pH and NaCl concentrations (20–45 °C, pH 8–11, 0–7 % NaCl), although they are phylogenetically separate and their hydrolysis of casein and gelatin is different. Strain 1139T utilized various carbohydrates. Strain AM-001T showed characteristics unlike those of any other strain and utilized a limited range of carbohydrates.
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On the basis of these chemotaxonomic and phylogenetic studies, five novel alkaliphilic Bacillus species are proposed.
Description of Bacillus wakoensis sp. nov.
Bacillus wakoensis (wa.ko.en'sis. N.L. masc. adj. wakoensis of Wako, a city in Japan).
Cells are rod-shaped, 1·5–2·0 µm in length and 0·5–0·8 µm in width, Gram-positive. Cells are motile by peritrichous flagella and produce spores that are ellipsoidal and located terminally in the sporangium, which is swollen. Colonies are circular and yellowish. Grows between 10 and 40 °C, with the optimum at around 37 °C. The range of pH for growth is from 8 to 10, with the optimum at pH 9–10. Tests positive for catalase, for hydrolysis of starch and cellulose and for nitrate reduction. It is negative for hydrolysis of Tweens 20, 40 and 60, casein, gelatin and oxidase and for the production of indole and H2S. Acid is produced from arbutin, cellobiose, D-fructose, glucose, D-maltose, D-mannitol, D-mannose, D-psicose, salicin, D-sorbitol, sucrose, D-trehalose, turanose and D-xylose; no gas evolution occurs from these carbohydrates. The organism can grow at an NaCl concentration of 10 % (w/v). The major isoprenoid quinone types are MK-6 and MK-7. Major fatty acids are iso-C15 : 0, anteiso-C15 : 0 and C16 : 0. The genomic DNA G+C content is 38·1 mol%, as determined by HPLC.
The type strain is N-1T (=JCM 9140T=DSM 2521T).
Description of Bacillus hemicellulosilyticus sp. nov.
Bacillus hemicellulosilyticus (hem.i.cell.u.lo.si.ly'ti.cus. N.L. neut. n. hemicellulosum hemicellulose; Gr. adj. lutikos able to loosen, able to dissolve; N.L. masc. adj. hemicellulosilyticus hemicellulose-dissolving).
Cells are rod-shaped, 2·0–6·0 µm in length and 0·3–0·5 µm in width, Gram-variable. Cells are motile by peritrichous flagella and produce spores that are ellipsoidal and located terminally in the sporangium, which is swollen. Colonies are circular and white. It grows at between 10 and 40 °C, with the optimum at around 37 °C. The range of pH for growth is from 8 to 11, with the optimum at around pH 10. Tests positive for catalase and for the hydrolysis of Tweens 20, 40 and 60 and hemicellulose. It is negative for oxidase, hydrolysis of soluble starch, gelatin and casein, for the production of indole and H2S and for nitrate reduction. Acid is produced from arbutin, cellobiose, D-fructose, D-glucose, D-lactose, D-maltose, maltotriose, D-mannose, D-mannitol, D-melibiose, palatinose, D-raffinose, salicin, D-sorbitol, stachyose, sucrose, D-trehalose and turanose; no gas evolution occurs from these carbohydrates. The organism can grow at an NaCl concentration of 12 % (w/v), but not at 15 %. The major isoprenoid quinone type is MK-7. Major fatty acids are iso-C15 : 0, anteiso-C15 : 0, C16 : 0 and anteiso-C17 : 0. The genomic DNA G+C content is 36·8 mol%, as determined by HPLC.
The type strain is C-11T (=JCM 9152T=DSM 16731T).
Description of Bacillus cellulosilyticus sp. nov.
Bacillus cellulosilyticus (cell.u.lo.si.ly'ti.cus. N.L. neut. n. cellulosum cellulose; Gr. adj. lutikos able to loosen, able to dissolve; N.L. masc. adj. cellulosilyticus cellulose-dissolving).
Cells are rod-shaped, 2·0–3·0 µm in length and 0·3–0·4 µm in width, Gram-positive. Cells are motile by peritrichous flagella and produce spores that are ellipsoidal and located subterminally in the sporangium, which is swollen. Colonies are circular to slightly irregular and cream-coloured. Grows at between 20 and 40 °C, with the optimum at around 37 °C. The range of pH for growth is from 8 to 10, with the optimum at around pH 9–10. Tests positive for catalase and nitrate reduction and for the hydrolysis of soluble starch, Tweens 20, 40 and 60 and cellulose. It is negative for oxidase, for hydrolysis of gelatin and casein and for the production of indole and H2S. Acid is produced from arbutin, cellobiose, D-fructose, D-glucose, D-lactose, D-maltose, maltotriose, D-mannose, salicin, sucrose, D-trehalose and turanose; no gas evolution occurs from these carbohydrates. The organism can grow at an NaCl concentration of 12 % (w/v) NaCl, but not at 15 %. The major isoprenoid quinone type is MK-7. Major fatty acids are iso-C15 : 0, anteiso-C15 : 0 and C16 : 0. The genomic DNA G+C content is 39·6 mol%, as determined by HPLC.
The type strain is N-4T (=JCM 9156T=DSM 2522T).
Description of Bacillus akibai sp. nov.
Bacillus akibai (a.ki.ba'i. N.L. gen. n. akibai of Akiba, named after the Japanese microbiologist Teruhiko Akiba, who made fundamental contributions to the study of alkaliphilic bacteria).
Cells are rod-shaped, 3·0–4·0 µm in length and 0·6–0·8 µm in width, Gram-positive. Cells are motile by peritrichous flagella and produce spores that are ellipsoidal and located subterminally in the sporangium, which is slightly swollen. Colonies are circular and yellowish. It grows at between 20 and 45 °C, with the optimum at around 37 °C. The range of pH for growth is from 8 to 10, with the optimum at around pH 9–10. Tests positive for catalase, for nitrate reduction and for the hydrolysis of soluble starch, Tweens 20, 40 and 60 and cellulose. It is negative for oxidase, for hydrolysis of gelatin and casein and for the production of indole and H2S. Acid is produced from L-arabinose, arbutin, cellobiose, D-fructose, D-galactose, D-glucose, D-maltose, maltotriose, D-mannose, D-mannitol, D-melezitose, palatinose, D-psicose, salicin, D-sorbitol, sucrose, D-trehalose and turanose; no gas evolution occurs from these carbohydrates. The organism can grow at an NaCl concentration of 7 % (w/v), but not at 10 %. The major isoprenoid quinone types are MK-6 and MK-7. Major fatty acids are iso-C14 : 0, iso-C15 : 0, anteiso-C15 : 0 and C16 : 0. The genomic DNA G+C content is 34·4 mol%, as determined by HPLC.
The type strain is 1139T (=JCM 9157T=ATCC 43226T).
Description of Bacillus mannanilyticus sp. nov.
Bacillus mannanilyticus (mann.an.i.ly'ti.cus. N.L. neut. n. mannanum mannan; Gr. adj. lutikos able to loosen, able to dissolve; N.L. masc. adj. mannanilyticus mannan-dissolving).
Cells are rod-shaped, 3·0–6·0 µm in length and 0·6–0·8 µm in width, Gram-variable. Cells are motile by peritrichous flagella and produce spores that are ellipsoidal and located terminally in the sporangium, which is swollen. Colonies are circular and yellow. It grows at between 20 and 45 °C, with the optimum at around 37 °C. The range of pH for growth is from 8 to 10, with the optimum at around pH 9. The bacterium tests positive for catalase and for the hydrolysis of Tweens 40 and 60, soluble starch, gelatin, casein and mannan and is negative for oxidase, for the production of indole and H2S and for nitrate reduction. Acid is produced from D-fructose, glucose, D-maltose, mannose, D-galactose, D-xylose, D-mannitol, sorbitol, D-trehalose, raffinose, sucrose, D-lactose, glycerol, inulin and starch; no gas evolution occurs from these carbohydrates. The organism can grow at an NaCl concentration of 3 % (w/v), but not at 5 %. The major isoprenoid quinone type is MK-7. Major fatty acids are C16 : 0 and C16 : 1. The genomic DNA G+C content is 37·4 mol%, as determined by HPLC.
The type strain is AM-001T (=JCM 10596T=DSM 16130T).
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REFERENCES |
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