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1 Centre for Cellular and Molecular Biology, Uppal Road, Hyderabad – 500 007, India
2 Indian Institute of Chemical Technology, Uppal Road, Hyderabad – 500 007, India
3 Otsuma Women's University, Department of Environment Science, School of Social Information Studies, Karakida 2-7-1, Tama-Shi, Wakazawa, Tokyo 206-0036, Japan
Correspondence
S. Shivaji
shivas{at}ccmb.res.in
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The EMBL accession numbers for the 16S rRNA gene sequences of strains CMS 76rT and CMS 81yT are AJ438585 and AJ438586.
A UPGMA phenogram including more reference sequences and a table of differences revealed by a comparison of almost-complete 16S rRNA gene sequences of all members of the genus Leifsonia are available as supplementary material in IJSEM Online.
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TOPABSTRACTMAIN TEXTREFERENCES |
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to accommodate Gram-positive, non-spore-forming, irregular rod- or filament-shaped, motile, mesophilic and catalase-positive bacteria containing DL-2,4-diaminobutyric acid in the peptidoglycan, MK-11 as the major menaquinone, phosphatidylglycerol and diphosphatidylglycerol as the major phospholipids, a high content of anteiso- and iso-branched fatty acids and a DNA G+C content of 66–73 mol%. Currently, five species belonging to the genus Leifsonia have been described: Leifsonia poae, isolated from a nematode gall on Poa annua roots (Evtushenko et al., 2000), Leifsonia aquatica, isolated from distilled water (Leifson, 1962), Leifsonia xyli subsp. xyli and L. xyli subsp. cynodontis, respectively isolated from a Saccharum interspecific hybrid and Cynodon dactylon (Davis et al., 1984) and Leifsonia naganoensis and Leifsonia shinshuensis, isolated from soil (Suzuki et al., 1999). All five species reported so far are mesophilic. In the present study, we report two psychrophilic strains of Leifsonia isolated from a cyanobacterial mat sample growing luxuriously in a pond in Wright Valley, McMurdo, Antarctica. Both isolates, CMS 76rT and CMS 81yT, were psychrophilic; they could be assigned to the genus Leifsonia on the basis of their phenotypic characteristics, chemotaxonomic features and phylogeny based on 16S rRNA gene sequences. Furthermore, strains CMS 76rT and CMS 81yT differed from the five reported species of Leifsonia with respect to many characteristics and are designated as the type strains of the novel species Leifsonia rubra sp. nov. (CMS 76rT) and Leifsonia aurea sp. nov. (CMS 81yT).
Source of the organisms, media and growth conditions
Seven bacterial cultures (CMS 73y, CMS 74y, CMS 76rT, CMS 77y, CMS 78y, CMS 79y and CMS 81yT) were isolated from a cyanobacterial mat sample collected from pond L9 of Wright Valley in McMurdo, Antarctica (Matsumoto, 1993). For this purpose, a fragment of the cyanobacterial mat sample (about 200 mg) was suspended in 1 ml sterile saline (150 mM NaCl) and an aliquot (100 µl) was plated on Antarctic bacterial medium (ABM) containing 0·5 % (w/v) peptone, 0·2 % (w/v) yeast extract and 1·5 % (w/v) agar (pH 6·9) and incubated at 5 °C (Shivaji et al., 1989). Representative colonies were selected and regrown on ABM plates to obtain pure cultures of the bacteria. The optimum temperature, pH and salt concentration for growth of the cultures were determined using ABM plates.
All seven isolates could grow on either ABM or nutrient agar and colonies were circular, convex, smooth, butyrous and opaque. Furthermore, except for CMS 76rT (which was red-pigmented), the isolates were yellow-pigmented. These six yellow-pigmented isolates were also identical with respect to their morphology, biochemical and chemotaxonomic characteristics, randomly amplified polymorphic DNA profile and 16S rRNA gene sequence, indicating that they are clonal in origin. Therefore, CMS 81yT was chosen as a representative strain for all six yellow-pigmented isolates.
Randomly amplified polymorphic DNA analysis was carried out as described previously (Shivaji et al., 2000) using the primers OPA-02 (5'-TGCCGAGCT-3') and OPA-03 (5'-AGTGCGCCAC-3').
Morphology, motility and biochemical characteristics
The morphology of the bacterial cultures during growth and motility were observed by phase-contrast microscopy (1000x). All of the biochemical tests described below were performed by growing the cultures at 18 or 22 °C in the appropriate medium (Hugh & Leifson, 1953; Stanier et al., 1966; Holding & Collee, 1971; Stolp & Gadkari, 1981). For oxidase testing, the method of Kovacs (1956) was used. In this test, stationary-phase cells grown in ABM were used. The ability of the cultures to utilize carbon compounds as sole carbon sources, sensitivity to different antibiotics and the G+C content of the DNA were determined as described previously (Shivaji et al., 1991).
Both strains CMS 76rT and CMS 81yT were found to be Gram-positive, curved, rod-shaped bacteria that are non-motile, aerobic and positive for catalase. Other details relating to optimal growth conditions, pigment characteristics, utilization of carbon compounds as sole carbon sources, ability to oxidize or ferment sugars, sensitivity to antibiotics and other phenotypic characteristics are included below in the species descriptions (see Tables 1 and 2 for diagnostic characteristics). Pigments were extracted from lyophilized bacterial cell pellets by using methanol and their absorption spectra were recorded in a Hitachi 330 spectrophotometer (Jagannadham et al., 1991).
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) and aligned with reference sequences that included all the genera of the family using the multiple sequence alignment program CLUSTAL V (Higgins et al., 1992). The program DNADIST, with the Kimura-2 parameter, was used to compute pairwise evolutionary distances for the above aligned sequences (Kimura, 1980). The original sequence dataset was resampled 1000 times using SEQBOOT and subjected to bootstrap analysis. Phylogenetic trees were constructed using parsimony analysis (DNAPARS) and using various distance matrix-based clustering algorithms such as FITCH, KITCH and UPGMA (Felsenstein, 1993). Majority-rule (50 %) consensus trees were also constructed using CONSENSE (Felsenstein, 1993). In all cases, input order of species added to the topology of the tree was randomized with the jumble option of 7 and 10 replications.
The different algorithms gave consistent results. On the basis of the 16S rRNA gene sequence, it was clear that strains CMS 76rT and CMS 81yT are closely related to one another (97·5 % similarity) and to the reported species of Leifsonia (95–96 %) with an evolutionary distance of 2·5 % between themselves and 4–5 % from the reported species, as calculated by the Kimura-2 parameter of the DNADIST program. In fact, the phylogenetic tree clearly demonstrated that CMS 76rT and CMS 81yT are closely related; they formed a robust and separate clade with a bootstrap value of 100 % and clustered with the other five species of Leifsonia (Fig. 1) with a bootstrap value of 62 %. Furthermore, the topology of the tree was similar to the one reported previously (Evtushenko et al., 2000).
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as described previously (Reddy et al., 2002a), was only 30 %.
Chemotaxonomic studies
The methods used for the identification of fatty acids (Sato & Murata, 1988), quinones (Collins et al., 1977; Dunphy et al., 1971), polar lipids (Komagata & Suzuki, 1987), peptidoglycan (Rosenthal & Dziarski, 1994; Schleifer & Kandler, 1972) and cell-wall sugars (Komagata & Suzuki, 1987) and determination of the DNA G+C content were described previously (Reddy et al., 2002b). For fatty acid analysis, strains CMS 76rT, CMS 81yT and L. aquatica ATCC 14665T were cultured in CB liquid medium (Zgurskaya et al., 1993) at 25 °C.
The phylogenetic affiliation of strains CMS 76rT and CMS 81yT to the genus Leifsonia is supported further by their chemotaxonomic properties, such as the presence of glycine, glutamic acid, 2,4-diaminobutyric acid and alanine in the cell-wall peptidoglycan, MK-11 as the major menaquinone, phosphatidylglycerol and diphosphatidylglycerol as the principal phospholipids and anteiso-C15 : 0, anteiso-C17 : 0 and iso-C16 : 0 as the predominant fatty acids and the DNA G+C content of 64–66 mol%.
Conclusions
Strains CMS 76rT and CMS 81yT conform to the description of the genus Leifsonia in that they are Gram-positive, curved rods, non-motile and catalase-positive, contain 2,4-diaminobutyric acid in the peptidoglycan, contain menaquinone MK-11, phosphatidylglycerol and diphosphatidylglycerol, have a high content of anteiso- and iso-branched fatty acids and have a DNA G+C content of 64–66 mol%. In addition, CMS 76rT is closely related to CMS 81yT with respect to many phenotypic and chemotaxonomic characteristics (Tables 1 and 2
). However, it differed from CMS 81yT in that it was red-pigmented, did not grow at temperatures above 22 °C, gave a negative Voges–Proskauer test, did not utilize arginine or erythritol as sole carbon sources and contained rhamnose as an additional cell-wall sugar (Table 1). Furthermore, CMS 76rT had higher proportions of C15 : 0 (3·6 %), iso-C15 : 0 (7·8 %) and iso-C16 : 0 (11·5 %) and lower levels of anteiso-C17 : 0 (20·3 %) and iso-C17 : 0 (1·8 %) (Table 2). In addition, there was a difference of 2·5 % at the 16S rDNA sequence level between the two isolates and they were related by only 30 % at the whole-genome level, as evidenced by DNA–DNA relatedness studies. These characteristics clearly establish that CMS 76rT and CMS 81yT represent two separate species.
Strain CMS 76rT is different from all the other reported species of the genus Leifsonia (including CMS 81yT) in that it is red-pigmented and psychrophilic (with a growth temperature of 0–22 °C). Furthermore, it had higher proportions of C15 : 0 and iso-C15 : 0 compared with CMS 81yT, L. aquatica and L. poae, which were analysed following growth in CB liquid medium at 25 °C. Data for L. aquatica ATCC 14665T were acquired in the present study, whereas data for L. poae were from Evtushenko et al. (2000). The fatty acids C14 : 0, C15 : 0, C18 : 0, C15 : 1 and C18 : 1 were absent from L. xyli subsp. cynodontis, L. naganoensis and L. shinshuensis (Suzuki et al., 1999). In addition, CMS 76rT showed a number of distinct differences from the reported species of Leifsonia, as listed in Table 1. Furthermore, at the 16S rRNA gene sequence level, CMS 76rT differed from L. aquatica, L. poae, L. xyli subsp. xyli, L. xyli subsp. cynodontis, L. naganoensis and L. shinshuensis by 4·2, 3·8, 4·6, 4·5, 4·1 and 4·9 %, respectively. Thus, on the basis of differences in phenotypic traits (Table 1), distinct fatty acid types (Table 2) and the >3 % difference at the 16S rRNA gene sequence level (except for CMS 81yT, for which the value was 
2·5 %), CMS 76rT has been assigned the status of a novel species, for which the name L. rubra sp. nov. is proposed. It is worthwhile to mention that strains with more than a 3 % difference at the 16S rDNA level are unlikely to have a DNA–DNA relatedness of more than 70 % (Stackebrandt & Goebel, 1994).
Strain CMS 81yT can also be differentiated from CMS 76rT and L. aquatica, L. poae, L. xyli subsp. xyli, L. xyli subsp. cynodontis, L. naganoensis and L. shinshuensis on the basis of phenotypic traits and chemotaxonomic properties (Tables 1 and 2). In addition, its 16S rRNA gene sequence differs from those of L. poae, L. aquatica, L. xyli subsp. xyli, L. xyli subsp. cynodontis, L. naganoensis and L. shinshuensis by 3·9, 4·3, 4·6, 4·2, 4·9 and 4·8 % (but by only 2·5 % from that of CMS 76rT). Therefore, CMS 81yT has also been assigned the status of a novel species, for which the name L. aurea sp. nov. is proposed.
Despite the fact that strains CMS 76rT and CMS 81yT formed a coherent cluster with the clade of Leifsonia species, a high level of dissimilarity was observed at the 16S rDNA sequence level. The reason for this is that, when 1407 bp (positions 110–1517 according to Escherichia coli numbering) of the 16S rRNA gene sequences of all species of the genus Leifsonia were compared, a total of 115 nucleotide changes were observed, spanning the entire region (details available as supplementary material in IJSEM Online). Contributing to this change is an insertion of 14 bp from positions 461 to 474 observed only in CMS 76rT and CMS 81yT. In addition, two variable regions were observed, spanning positions 148 to 226 (around 31 variable positions) and positions 613 to 631 (7 variable positions). The significance of these insertions or variable regions is not clear, but the occurrence of the insertion in only the psychrophilic species may prove useful as a signature for these isolates; this awaits clarification in future studies.
Description of Leifsonia rubra sp. nov.
Leifsonia rubra (rub'ra. L. fem. adj. rubra reddish, referring to the reddish pigment that the bacterium produces).
Colonies are circular, convex, smooth, butyrous, opaque, red-pigmented and 1–2 mm in diameter. Cells are aerobic, Gram-positive, non-motile, curved rods. The pigment is insoluble in water but soluble in methanol and exhibits characteristic peaks at 420, 443, 490 and 520 nm in methanol. Grows between 0 and 22 °C and between pH 6 and 12 and tolerates up to 3 % NaCl. Optimum growth is observed at 15 °C, pH 7 and in the absence of NaCl. Positive for catalase and 
-galactosidase and reduces nitrate to nitrite. Negative for oxidase, urease, lipase, gelatinase, phosphatase and indole, gives negative results in methyl red and Voges–Proskauer tests, is negative for H2S production and does not hydrolyse aesculin or starch. Does not produce acid from L-arabinose, D-fructose, D-galactose, glucosamine, lactose, D-maltose, D-mannose, L-rhamnose, sucrose or D-xylose. Utilizes D-fructose, D-glucose, D-galactose, glucosamine, glycerol, D-mannose, pyruvate, L-rhamnose, D-ribose, sodium acetate, D-sorbose, trehalose, L-glutamic acid and L-phenylalanine as sole carbon sources, and fails to utilize L-arabinose, adonitol, ammonium acetate, D-cellobiose, cellulose, creatinine, dextran, dulcitol, meso-erythritol, glycogen, -hydroxybutyric acid, inositol, inulin, lactose, lactic acid, D-maltose, D-mannitol, D-melibiose, melezitol, myristic acid, polyethylene glycol, potassium hydrogen phthalate, D-raffinose, sodium citrate, sodium succinate, sorbitol, sucrose, D-xylose, L-alanine, L-arginine, L-glycine, L-glutamine, L-lysine, L-methionine, L-serine, L-tyrosine and L-tryptophan. Sensitive to novobiocin, cefaperazone, cefazoline, kanamycin, amoxycillin, tobramycin, roxithromycin, vancomycin, cephatoxime, streptomycin, erythromycin, amikacin, ampicillin, lincomycin, tetracycline and rifampicin and resistant to penicillin, colistin, cefuroxime, nitrofurantoin, ciprofloxacin, cotrimoxazole, norfloxacin and chloramphenicol. The peptidoglycan contains DL-diaminobutyric acid as the diamino acid, along with glycine, glutamic acid and alanine. The cell-wall sugars are galactose, glucose, ribose and rhamnose. The major menaquinone is MK-11. Fatty acid methyl esters are listed in Table 2. The G+C content of the DNA of the type strain is 66 mol%.
The type strain is strain CMS 76rT (=MTCC 4210T =DSM 15304T =CIP 107783T).
Description of Leifsonia aurea sp. nov.
Leifsonia aurea (au're.a. L. fem. adj. aurea golden, referring to the yellowish pigment that the bacterium produces).
Colonies are yellowish, circular, convex, smooth, butyrous, opaque, yellow-pigmented and 1–2 mm in diameter. Cells are aerobic, Gram-positive, curved, non-motile rods. The pigment is insoluble in water but soluble in methanol and exhibits four characteristic peaks, at 390, 414, 438 and 468 nm. Grows between 0 and 30 °C and between pH 6 and 11 and tolerates up to 3 % NaCl. Optimum growth occurs at 22 °C, pH 7 and in the absence of salt. Positive for catalase and -galactosidase, gives a positive result in the Voges–Proskauer test and reduces nitrate to nitrite. Negative for oxidase, urease, lipase, gelatinase, phosphatase and indole, gives a negative result in the methyl red test, is negative for H2S production and does not hydrolyse aesculin or starch. Does not produce acid from L-arabinose, D-fructose, D-galactose, D-glucose, lactose, D-maltose, D-mannose, L-rhamnose, sucrose or D-xylose. Does not grow on minimal medium containing L-arabinose, adonitol, ammonium acetate, D-cellobiose, cellulose, creatinine, dextran, dulcitol, glycogen, -hydroxybutyric acid, inositol, inulin, lactose, lactic acid, D-maltose, D-mannitol, D-melibiose, melezitol, myristic acid, polyethylene glycol, potassium hydrogen phthalate, D-raffinose, sodium citrate, sodium succinate, sorbitol, sucrose, D-xylose, L-alanine, L-glycine, L-glutamine, L-lysine, L-methionine, L-serine, L-tyrosine or L-tryptophan. Can grow on erythritol, D-fructose, D-glucose, D-galactose, glucosamine, glycerol, D-mannose, pyruvate, L-rhamnose, D-ribose, sodium acetate, D-sorbose, trehalose, L-arginine, L-glutamic acid and L-phenylalanine as sole carbon sources. Resistant to colistin, nitrofurantoin, cotrimoxazole, erythromycin, norfloxacin, lincomycin and chloramphenicol and sensitive to novobiocin, cefaperazone, cefazoline, penicillin, kanamycin, cefuroxime, amoxycillin, ciprofloxacin. tobramycin, roxithromycin, vancomycin, cephatoxime, streptomycin, amikacin, ampicillin, tetracycline and rifampicin. The peptidoglycan contains DL-diaminobutyric acid as the diamino acid, along with glycine, glutamic acid and alanine, and the cell-wall sugars are galactose, glucose and ribose. The major menaquinone is MK-11. Fatty acid methyl esters are listed in Table 2. The G+C content of the DNA of the type strain is 64 mol%.
The type strain is strain CMS 81yT (=MTCC 4657T =DSM 15303T =CIP 107785T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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