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1 Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad 500 007, India
2 Geological Survey of India, GSI Complex, DK-6, Sector-II, Bidhannagar, Kolkata 700 091, India
Correspondence
S. Shivaji
shivas{at}ccmb.res.in
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Published online ahead of print on 12 September 2003 as DOI 10.1099/ijs.0.02758-0.
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain Wt/1aT is AJ549111.
A table showing survival of Deinococcus species under UV light and a figure showing one-dimensional TLC of total lipid extracts from Deinococcus species are available as supplementary material in IJSEM Online.
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) and the reduction of ferrous-coated sand grains (Nickson et al., 1998). Diverse microbial flora that is resistant to arsenic, including Pseudomonas fluorescens (de Vicente et al., 1990; Prithivirajsingh et al., 2001), Bacillus subtilis (Sato & Kobayashi, 1998), Thermus aquaticus and Thermus thermophilus (Gihring et al., 2001), Yersinia enterocolitica and Yersinia intermedia (Bansal et al., 2000), Streptomyces noursei (Friedrich et al., 1984) and Desulfitobacterium sp. (Niggemyer et al., 2001), has been reported from various habitats. Arsenic-contaminated water that was collected in sterile tubes from various aquifers in July 2001, when plated directly onto a nutrient agar plate and incubated at 30 °C for 2 days, yielded 2·21x103 c.f.u. ml-1. These colonies represented 13 different morphotypes. Based on protein profiles, these 13 morphotypes were categorized into four groups (data not shown), as follows: group I (Wt/1aT, Wt/1b and Wt/1c); group II (Wt/2a, Wt/2b, Wt/2c and Wt/2d); group III (Wt/3a, Wt/3b, Wt/3c, Wt/3d and Wt/3e); and group IV (Wt/4a and Wt/4b). All strains within each group had identical protein profiles, indicating that they were clonal in origin. In the present study, isolate Wt/1aT, which was chosen as a representative strain of the three isolates that belong to group I, is subjected to polyphasic taxonomic studies. This red-pigmented bacterium was identified as a novel species of the genus Deinococcus and was assigned the name Deinococcus indicus sp. nov.
Strain Wt/1aT was isolated from a shallow aquifer in the Bengal basin, Chakdah district, West Bengal, India (88° 35' S 23° 3' E). The medium used for isolation of the bacterium was nutrient agar [0·5 % (w/v) peptone, 0·3 % (w/v) beef extract, 0·5 % NaCl and 1·5 % (w/v) agar, pH 6·5]. Nutrient agar was used for growth, maintenance and biochemical tests. Optimum pH and temperature for growth were 6·5 and 30 °C, respectively. Cultures were grown in nutrient broth that contained either sodium arsenate (Na2HAsO4) or arsenic trioxide (As2O3) to determine the tolerance of the culture to arsenate and arsenite.
The bacterial culture was observed in the lag, exponential and stationary phases of growth under a phase-contrast microscope (x1000) to ascertain the shape and motility of the bacterium. Biochemical tests were performed as described by Lanyi (1987), Reddy et al. (2002a, b) and Smibert & Krieg (1994). Single carbon source assimilation tests were performed in a minimal basal salts medium [which contained 10·5 g K2HPO4, 4·5 g KH2PO4, 1 g (NH4)2SO4 and 15 g agar (l medium prepared in distilled water)-1]. Organic substrates were filter-sterilized (Millipore; catalogue no. PHWP02500) and added to the medium at a final concentration of 5 g l-1 before plates were poured. The sensitivity of the culture to different antibiotics was checked by using antibiotic discs that were supplied by HiMedia. SDS-PAGE was performed according to the method of Laemmli (1970). Isolation of DNA and determination of its G+C content were performed as described previously (Shivaji et al., 1989; Reddy et al., 2000). DNA–DNA hybridization was performed by the membrane filter method (Tourova & Antonov, 1987) as described previously (Shivaji et al., 1992; Reddy et al., 2000). To determine tolerance of the culture to UV radiation, the culture was grown to late-exponential phase and harvested at 5000 g for 5 min at 4 °C; the cell pellet was suspended in 10 ml phosphate buffer (pH 7·2), diluted serially and 0·1 ml was spread on nutrient agar plates. Plates (with their lids open) were then exposed to UV light (UV-B, 15 W x4; Sanyo Denki) at a distance of 30 cm from the UV source for the required dose and were incubated subsequently at 30 °C for 5 days. The UV dose was monitored with a model RX003 UV detector (UVI Tech). Deinococcus radiodurans DSM 20539T, D. grandis IAM 13005T and Escherichia coli DH5
were used as controls to evaluate the effect of UV radiation on the growth of the micro-organisms.
Cells were grown in nutrient broth at 30 °C and the fatty acid methyl esters (Sato & Murata, 1988) were analysed as described previously (Reddy et al., 2002a). Isoprenoid quinones were extracted, separated by HPLC and identified as described previously (Reddy et al., 2003). Peptidoglycan was prepared and analysed according to the method described by Komagata & Suzuki (1987). Polar lipids were extracted and analysed according to the method described by Counsell & Murray (1986). In this method, the bacterial cell pellet is extracted with chloroform : methanol (2 : 1) and separated by one-dimensional TLC, using a pre-coated silica gel TLC plate (Merck; catalogue no. 5721) and chloroform : acetone : methanol : acetic acid : water (10 : 4:2 : 2:1, v/v) as the solvent system. Total lipids were detected by spraying with 25 % H2SO4 in ethanol, followed by charring at 150 °C for 5 min and compared with phosphatidylinositol (PI), phosphatidylcholine (PC), phosphatidylglycerol (PG) and diphosphatidylglycerol (DPG), which were run under similar conditions. Phosphoglycolipids were detected by staining with -naphthol [a mixture of 10·5 ml 15 % (w/v) -naphthol in ethanol, 6·5 ml concentrated H2SO4 and 4·0 ml water], whereas ninhydrin (0·25 % in acetone) was used to detect aminoglycolipids.
The 16S rRNA gene was amplified (Shivaji et al., 2000), purified with a QIAquick PCR purification kit (Qiagen) and sequenced by using an ABI PRISM BigDye Terminator cycle sequencing kit and an automatic DNA sequencer (ABI PRISM model 3700) (both from Applied Biosystems). The partial 16S rDNA sequence (1456 bp) was aligned with those of species of the genera Deinococcus, Kocuria and Arthrobacter by using CLUSTAL W (Thompson et al., 1994). Pairwise evolutionary distances were computed by using the DNADIST program with the Kimura two-parameter model, as developed by Kimura (1980). Phylogenetic trees were constructed by using two tree-making algorithms: UPGMA and parsimony (DNAPARS; Felsenstein, 1993). Stability among the clades of a phylogenetic tree was assessed by taking 1000 replicates of the dataset, which were analysed by using the programs SEQBOOT, DNADIST, NEIGHBOR (upgma algorithm) and CONSENSE of the PHYLIP package.
Cells of Wt/1aT stain Gram-negative and are rod-shaped, non-motile, non-sporulating and red-pigmented. Cell-wall peptidoglycan contains ornithine as the diamino acid (A3
variant), MK-8 is the organism's major respiratory quinone, C15 : 1 and C16 : 1 are the major fatty acids and the DNA G+C content is 65·8 mol%. Based on the above characteristics, strain Wt/1aT was identified as a member of the genus Deinococcus (Murray & Brooks, 1986; Rainey et al., 1997). A BLAST sequence similarity search and phylogenetic studies corroborated the above data and confirmed that strain Wt/1aT belongs to the genus Deinococcus. Furthermore, the 16S rRNA gene sequence of strain Wt/1aT possessed all the signature nucleotides, namely C, G, T, G, T, A, G, C and C at positions 657, 749, 757, 1050, 1208, 1421, 1429, 1471 and 1479, respectively, that are characteristic features of the genus Deinococcus (Rainey et al., 1997).
Phylogenetic analysis based on the 16S rRNA gene sequence indicated that strain Wt/1aT is related closely to D. grandis IAM 13005T (Oyaizu et al., 1987; Rainey et al., 1997), with 95 % sequence similarity. The topology of the phylogenetic tree (Fig. 1) indicated that strain Wt/1aT forms a robust clade with D. grandis IAM 13005T, with a bootstrap resampling value of 100 %. Furthermore, the phylogenetic affiliation of strain Wt/1aT with D. grandis IAM 13005T is confirmed by its rod shape and Gram-staining (both isolates stain Gram-negative), whereas other species of the genus are Gram-positive and spherical in shape. However, when the 16S rRNA gene sequence of strain Wt/1aT (1453 bp) is compared with that of D. grandis IAM 13005T, 73 bases were observed to be different and strain Wt/1aT shared only 14 % DNA–DNA reassociation with D. grandis IAM 13005T. Furthermore, strain Wt/1aT showed low 16S rRNA gene sequence similarity values of 91·94, 91·67, 93·51, 91·6, 89·39 and 91·5 % with Deinococcus radiopugnans, Deinococcus murrayi, D. radiodurans, Deinococcus radiophilus, Deinococcus geothermalis and Deinococcus proteolyticus, respectively.
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). It had higher amounts of the fatty acids C16 : 0 and C16 : 1 and reduced amounts of C14 : 0 and C15 : 1 (Table 2). In addition, lipid analysis indicated that strain Wt/1aT had seven lipids with Rf values of 0·21, 0·27, 0·42, 0·70, 0·76, 0·84 and 0·89 (identical to the lipid profile of D. grandis IAM 13005T), but differed in that it did not contain lipids 1–3, with Rf values of 0·11, 0·12 and 0·17, respectively, as observed in D. grandis IAM 13005T (see Supplementary Figure, available in IJSEM Online). Furthermore, none of the lipids matched with PI, PC, PG or DPG, although one of the phosphoglycolipids (lipid 4, with an Rf value of 0·21) showed similar (but not identical) chromatographic behaviour to PI. The fact that lipid 4 and PI are different is also evident from the fact that unlike lipid 4, which stains positively with -naphthol, PI does not stain [see Supplementary Fig. (B), available in IJSEM Online]. In addition to the above differences, strain Wt/1aT grew in the presence of 10 and 0·2 mM arsenate and arsenite, respectively, whereas D. grandis IAM 13005T is highly sensitive to both arsenate and arsenite (Table 1). Cultures of D. radiodurans DSM 20539T, D. grandis IAM 13005T and strain Wt/1aT were found to be more resistant to UV radiation than E. coli DH5. When the cultures were exposed to varying doses of UV radiation, it was observed that the survival of E. coli decreased by 99 % when exposed to 0·32 J cm-2, whereas at the same dose, survival in strain Wt/1aT, D. grandis IAM 13005T and D. radiodurans DSM 20539T was 66, 81 and 85 %, respectively. At higher UV doses, E. coli DH5 did not survive, but 2–4 % survival was observed in the remaining three cultures, even when they were exposed to 5·87 J cm-2 (see Supplementary Table in IJSEM Online). Thus, based on physiological, chemotaxonomic and phylogenetic differences, it is proposed to assign novel species status to strain Wt/1aT, for which the name Deinococcus indicus sp. nov. is proposed, with Wt/1aT (=MTCC 4913T=DSM 15307T) as the type strain.
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Cells stain Gram-negative and are non-motile and rod-shaped. Colonies on nutrient agar medium are red-pigmented, smooth, convex, circular, uniform-edged and 1–2 mm in diameter. Optimum growth occurs at 30 °C; growth occurs at 20–37 °C and pH 6–7. Tolerates up to 1·0 % NaCl and is resistant to UV radiation (5·87 J cm-2). Strictly aerobic and positive for catalase, gelatinase, amylase, arginine dihydrolase, aesculin and casein hydrolysis and reduction of nitrate to nitrite, but negative for oxidase, lipase, urease, indole production, Voges–Proskauer test and citrate utilization. A number of compounds are utilized as sole carbon sources (Table 1
), including D-maltose, sucrose, D-ribose and L-tyrosine, but not acetate, cellulose, D-fructose, D-galactose, D-glucose, meso-inositol, pyruvate, D-sorbose, L-glycine, creatinine, L-alanine or L-cysteine. Sensitive to the antibiotics bacitracin, chloramphenicol, kanamycin, nalidixic acid, neomycin, penicillin, rifampicin, rifamycin, streptomycin and tetracycline, but resistant to ampicillin and amoxycillin. Fatty acid composition of the type strain is given in Table 2; there are seven unknown polar lipids. Major respiratory quinone is MK-8 and cell-wall peptidoglycan contains ornithine as the diamino acid. DNA G+C content is 65·8 mol%.
The type strain is Wt/1aT (=MTCC 4913T=DSMZ 1537T).
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ACKNOWLEDGEMENTS |
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