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Int J Syst Evol Microbiol 57 (2007), 1060-1064; DOI  10.1099/ijs.0.64667-0
© 2007 International Union of Microbiological Societies

Bacillus selenatarsenatis sp. nov., a selenate- and arsenate-reducing bacterium isolated from the effluent drain of a glass-manufacturing plant

Shigeki Yamamura1, Mitsuo Yamashita2, Noriyuki Fujimoto2, Masashi Kuroda2, Masami Kashiwa3,{dagger}, Kazunari Sei3, Masanori Fujita3 and Michihiko Ike3

1 Water and Soil Environment Division, National Institute for Environmental Studies, 16-2 Onogawa, Tsukuba, Ibaraki 305-8506, Japan
2 Department of Biotechnology, Graduate School of Engineering, Osaka University, 2-1 Yamada-oka, Suita, Osaka 565-0871, Japan
3 Division of Sustainable Energy and Environmental Engineering, Graduate School of Engineering, Osaka University, 2-1 Yamada-oka, Suita, Osaka 565-0871, Japan

Correspondence
Shigeki Yamamura
yshige{at}nies.go.jp


   ABSTRACT
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A facultatively anaerobic, selenate- and arsenate-reducing bacterium, designated strain SF-1T, was isolated from a selenium-contaminated sediment obtained from an effluent drain of a glass-manufacturing plant in Japan. The bacterium stained Gram-positive and was a motile, spore-forming rod capable of respiring with selenate, arsenate and nitrate as terminal electron acceptors. The major cellular fatty acids of the strain were iso-C15 : 0, iso-C17 : 1{omega}10c and C16 : 1{omega}7c alcohol. The G+C content of the genomic DNA was 42.8 mol%. Though the nearest phylogenetic neighbour was Bacillus jeotgali JCM 10885T, with a 16S rRNA gene sequence similarity of 99.6 %, DNA–DNA hybridization studies showed only 14 % relatedness between these strains, a level that is clearly below the value recommended to delimit different species. This, together with the phenotypic differences (utilization of electron acceptors, NaCl tolerance), suggests that strain SF-1T represents a novel species of the genus Bacillus, for which the name Bacillus selenatarsenatis sp. nov. is proposed. The type strain is SF-1T (=JCM 14380T=DSM 18680T).

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain SF-1T is AB262082.

A figure showing a maximum-parsimony tree is available as supplementary material in IJSEM Online.

{dagger}Present address: Japan Agency for Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061, Japan. Back


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Selenium and arsenic, trace elements distributed widely in the Earth's crust, are required in trace amounts for growth and metabolism but are toxic at micromolar concentrations. In oxic environments, they occur primarily as the soluble oxyanions selenate [Se(VI)] and arsenate [As(V)]. In anoxic environments, these oxyanions can be utilized by prokaryotes as terminal electron acceptors for anaerobic respiration. The selenate- and/or arsenate-respiring prokaryotes isolated to date are diverse both physiologically and phylogenetically and are not confined to one particular phylum (Oremland & Stolz, 2000Go, 2003Go; Stolz et al., 2002Go). In general, oxyanions, including selenate and arsenate, are actively cycled and play an important role in carbon mineralization processes in certain environments.

A Gram-positive, selenate-reducing bacterium was isolated from a selenium-contaminated sediment collected from an effluent drain that had been receiving selenium-containing discharge from a glass-manufacturing plant. The bacterium, designated strain SF-1T (Fujita et al., 1997Go), is capable of respiring with selenate as a terminal electron acceptor and lactate as an electron donor. Selenate is reduced to elemental selenium via the intermediate selenite (Fujita et al., 1997Go; Kashiwa et al., 2000Go). A laboratory-scale continuous reactor using strain SF-1T had been constructed to remove selenate and selenite from wastewater (Fujita et al., 2002Go). Our studies revealed that strain SF-1T also grew anaerobically when arsenate was present as an electron acceptor (Yamamura et al., 2003Go), and this ability for dissimilatory reduction of arsenate to arsenite could be utilized to extract arsenic from contaminated soil for the purpose of bioremediation (Yamamura et al., 2005Go). Based on physiological, phylogenetic and molecular evidence presented here, the strain represents a novel species of the genus Bacillus.

Strain SF-1T was grown on a basal salt medium supplemented with 0.1 % yeast extract (pH 8.0) as described by Yamamura et al. (2003)Go. For aerobic growth, 10 g glucose l–1 was used as the electron donor, whereas sodium lactate (20 mM) was used instead of glucose for anaerobic growth with one of selenate, arsenate or nitrate (1 mM) as the electron acceptor. Bacillus jeotgali JCM 10885T, obtained from the RIKEN BRC-JCM, was cultivated on an appropriate medium (Yoon et al., 2001Go) or under the same condition as strain SF-1T, except that the pH was adjusted to 7.5, for phenotypic comparison. Biochemical tests were carried out using API 20E and API 50CHB kits according to the instructions of the manufacturer (bioMérieux). To determine sensitivity to antibiotics, a culture of strain SF-1T was inoculated onto LB agar plates (pH 8.0) containing kanamycin, tetracycline, chloramphenicol, ampicillin or erythromycin at 1–30 µg ml–1 and incubated at 37 °C for 4 days. Fatty acid methyl esters were extracted and analysed following the standard protocol of the Sherlock Microbial Identification System (MIDI).

For genomic DNA isolation, strain SF-1T and B. jeotgali JCM 10885T were grown aerobically in 1 litre batches to mid-exponential phase and cells were harvested by centrifugation at 8000 g (10 min, 4 °C). Genomic DNA was prepared using the DNeasy Tissue kit or DNeasy Plant kit (Qiagen) according to the manufacturer's instructions.

The G+C content of the DNA was determined by HPLC as described previously (Katayama-Fujimura et al., 1984Go). DNA–DNA hybridization of strain SF-1T and B. jeotgali JCM 10885T was carried out by the method of Ezaki et al. (1989)Go.

Gene fragments specific to the 16S rRNA-encoding regions were amplified by PCR using primers 20F (5'-GAGTTTGATCCTGGCTCAG-3'; positions 9–27) and 1500R (5'-GTTACCTTGTTACGACTT-3'; positions 1509–1492) (Kawasaki et al., 1993Go). Positions in the 16S rRNA gene fragment are based on the Escherichia coli numbering system (GenBank accession no. V00348) of Brosius et al. (1981)Go. Amplified 16S rRNA genes were sequenced directly using the ABI PRISM BigDye Terminator cycle sequencing ready reaction kit and an ABI PRISM model 310 Genetic Analyzer (Applied Biosystems). The following primers were used for sequencing: 20F, 1500R, 520F (5'-CAGCAGCCGCGGTAATAC-3'; positions 519–536), 520R (5'-GTATTACCGCGGCTGCTG-3'; positions 536–519), 920F (5'-AAACTCAAATGAATTGACGG-3'; positions 907–926) and 920R (5'-CCGTCAATTCATTTGAGTTT-3'; positions 926–907).

The 16S rRNA gene sequence of strain SF-1T determined was compared with reference sequences using BLAST similarity searches (Altschul et al., 1997Go) and the closely related sequences were obtained from GenBank. Multiple alignments were generated and the calculation of distance matrices for the aligned sequences (Kimura, 1980Go) was carried out using CLUSTAL X (Thompson et al., 1997Go) and MEGA version 3.1 (Kumar et al., 2004Go). Phylogenetic trees were inferred using the neighbour-joining (Saitou & Nei, 1987Go) and maximum-parsimony (Kluge & Farris, 1969Go) methods. The phylogenetic tree topology was evaluated by bootstrap analysis with 1000 replicates (Felsenstein, 1985Go). Sequence similarity values were calculated using GENETYX version 8 (Genetyx Corporation).

Strain SF-1T is a Gram-positive, oxidase-negative, catalase-positive, motile, spore-forming, facultatively anaerobic and rod-shaped bacterium (Fujita et al., 1997Go). Phylogenetic analysis based on the 16S rRNA gene sequence (1413 bp) of strain SF-1T indicated that it fell within the low-G+C-content, Gram-positive, aerobic, spore-forming bacilli (Fig. 1Go and Supplementary Fig. S1 available in IJSEM Online). The closest phylogenetic relative of strain SF-1T was B. jeotgali JCM 10885T, with a sequence similarity of 99.6 %; lower similarity was observed with some phylogenetically related Bacillus type strains, including Bacillus vireti LMG 21834T (96.7 %), Bacillus novalis LMG 21837T (96.6 %), Bacillus drentensis LMG 21831T (96.5 %), Bacillus niacini NBRC 15566T (96.1 %), Bacillus soli LMG 21838T (95.9 %), Bacillus bataviensis LMG 21833T (95.9 %) and Bacillus fumarioli LMG 17489T (95.5 %).


Figure 1
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  		Fig. 1. Neighbour-joining tree derived from 16S rRNA gene sequences showing the relationships between strain SF-1T and related Bacillus species. Bootstrap percentages (based on 1000 replications) greater than 50 % are given at branching points. Bar, 0.01 substitutions per nucleotide position. Paenibacillus polymyxa DSM 36T was used as the outgroup to root the tree. Accession numbers are given in parentheses. A maximum-parsimony tree is available as Supplementary Fig. S1 in IJSEM Online.

 
The optimal pH for aerobic growth of strain SF-1T is 8.0 and the optimal temperature is 40 °C. Strain SF-1T was able to grow on LB agar plates containing kanamycin (3 µg ml–1), tetracycline (3 µg ml–1) and chloramphenicol (5 µg ml–1), whereas it was highly sensitive to ampicillin and erythromycin. Several other biochemical and physiological characteristics of strain SF-1T were compared with those of its nearest phylogenetic relative on the basis of 16S rRNA gene sequence analysis, B. jeotgali JCM 10885T (Table 1Go). Strain SF-1T can grow not only aerobically but also anaerobically using selenate, arsenate and nitrate as terminal electron acceptors; the selenate is reduced to elemental selenium via selenite, arsenate to arsenite and nitrate to ammonia via nitrite (Fujita et al., 1997Go; Kashiwa et al., 2000Go; Yamamura et al., 2003Go, 2004Go). B. jeotgali JCM 10885T, however, was able to grow with neither selenate nor arsenate as terminal electron acceptors, although nitrate supported weak growth. B. jeotgali JCM 10885T can grow in the presence of 13 % (w/v) NaCl, whereas strain SF-1T did not grow in the presence of more than 7 % (w/v) NaCl. Additionally, strain SF-1T was positive for acid production from D-xylose, arbutin, salicin and amygdalin, whereas B. jeotgali JCM 10885T could not produce acid from these carbon compounds. Production of H2S was also observed only in strain SF-1T. These phenotypic differences seemed to distinguish SF-1T from its phylogenetic relative. The cellular fatty acid profile of strain SF-1T, in comparison with that of B. jeotgali JCM 10885T, is shown in Table 2Go. The major cellular fatty acid of strain SF-1T was found to be iso-C15 : 0 (47.3 mol%), as is the case for B. jeotgali JCM 10885T.


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  		Table 1. Comparison of phenotypic characteristics between strain SF-1T and B. jeotgali JCM 10885T

Unless otherwise specified, data for strain SF-1T were obtained from Fujita et al. (1997)Go and Yamamura et al. (2003)Go and data for B. jeotgali JCM 10885T were obtained from Yoon et al. (2001)Go and Imada et al. (2005)Go. +, Positive; –, negative; W, weakly positive. Both strain SF-1T and B. jeotgali JCM 10885T are positive for growth in the presence of 2 and 5 % NaCl, use of oxygen as an electron acceptor, catalase, beta-galactosidase, nitrate reduction, decomposition of starch and acid production from glucose, fructose, aesculin, cellobiose, maltose, sucrose, trehalose, starch, glycogen, gentiobiose and 5-ketogluconate. Both strains are negative for oxidase, formation of indole and acid production from glycerol, erythritol, D-arabinose, L-arabinose, ribose, L-xylose, adonitol, methyl beta-D-xyloside, galactose, mannose, sorbose, rhamnose, dulcitol, inositol, mannitol, sorbitol, methyl {alpha}-D-mannoside, methyl {alpha}-D-glucoside, N-acetylglucosamine, lactose, melibiose, inulin, melezitose, raffinose, xylitol, D-turanose, D-lyxose, D-tagatose, D-fucose, L-fucose, D-arabitol, L-arabitol, gluconate and 2-ketogluconate.

 

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  		Table 2. Cellular fatty acid compositions (%) of strain SF-1T and B. jeotgali JCM 10885T

Data for strain SF-1T were obtained in this study, whereas data for B. jeotgali JCM 10885T were taken from Yoon et al. (2001)Go.

 
Although the 16S rRNA gene sequence of strain SF-1T was more than 99 % similar to that of B. jeotgali JCM 10885T, the DNA–DNA reassociation value between strain SF-1T and B. jeotgali JCM 10885T was 14 % (mean from three independent determinations), which is lower than the threshold value (70 %) recommended for delimiting different species (Wayne et al., 1987Go). Thus, strain SF-1T can be classified as representing a novel species of the genus Bacillus. The DNA G+C content of strain SF-1T (42.8 mol%) was comparable to that of B. jeotgali JCM 10885T (41 mol%) (Yoon et al., 2001Go).

The results from biochemical characterizations and DNA–DNA hybridization strongly indicated that strain SF-1T can be distinguished from its closest phylogenetic relative, although they were not differentiated on the basis of cellular fatty acid profiles or 16S rRNA gene sequence analysis. Based on the evidence presented above, we describe a novel species within the genus Bacillus, Bacillus selenatarsenatis sp. nov.

Description of Bacillus selenatarsenatis sp. nov.
Bacillus selenatarsenatis (se'le.nat.ar.se.na'tis. N.L. gen. n. selenatis of selenate; N.L. gen. n. arsenatis of arsenate; N.L. gen. n. selenatarsenatis of selenate and arsenate).

The following description is based on data from this study and from Fujita et al. (1997)Go and Yamamura et al. (2003)Go. Cells stain Gram-positive and are spore-forming, motile rods (1x3–6 µm). Colonies are round and white. Growth occurs at 25–40 °C and at pH 7.5–9.0. Growth occurs in the presence of 2–5 % NaCl, but not in the presence of 7 % NaCl. Positive results are obtained for catalase, beta-galactosidase, H2S production and nitrate reduction and negative results are obtained for oxidase, the Voges–Proskauer test, indole production and phenylalanine deamination. Gelatin and starch are hydrolysed. Acid is produced from D-xylose, glucose, fructose, amygdalin, arbutin, aesculin, salicin, cellobiose, maltose, sucrose, trehalose, starch, glycogen, gentiobiose and 5-ketogluconate, but not from glycerol, erythritol, D-arabinose, L-arabinose, ribose, L-xylose, adonitol, methyl beta-D-xyloside, galactose, mannose, sorbose, rhamnose, dulcitol, inositol, mannitol, sorbitol, methyl {alpha}-D-mannoside, methyl {alpha}-D-glucoside, N-acetylglucosamine, lactose, melibiose, inulin, melezitose, raffinose, xylitol, D-turanose, D-lyxose, D-tagatose, D-fucose, L-fucose, D-arabitol, L-arabitol, gluconate or 2-ketogluconate. Cells are resistant to 3 µg kanamycin ml–1, 3 µg tetracycline ml–1 and 5 µg chloramphenicol ml–1, but highly sensitive to ampicillin and erythromycin. The bacterium is a facultative anaerobe that respires oxygen, selenate, arsenate and nitrate as terminal electron acceptors. Selenate is reduced to elemental selenium via the intermediate selenite, arsenate to arsenite and nitrate to ammonia via the intermediate nitrite. The dominant fatty acids are iso-C15 : 0 (47.3 mol%), iso-C17 : 1{omega}10c (10.1 mol%) and C16 : 1{omega}7c alcohol (8.6 mol%). The DNA G+C content of the type strain is 42.8 mol%.

The type strain, SF-1T (=JCM 14380T=DSM 18680T), was isolated from an effluent drain in a glass-manufacturing plant in Japan.


   ACKNOWLEDGEMENTS
 
This work was supported by a Grant-in-Aid for Scientific Research (no. 15310056) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. We would like to thank Dr H. Kawasaki and Dr N. Esaki for their assistance with nomenclature and phylogenetic analyses.


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