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1 Department of Bioresource Science, Ibaraki University College of Agriculture, Ami-machi, Ibaraki 300-0393, Japan
2 Attic Laboratory, Aoba-ku, Sendai 980-0813, Japan
3 Graduate School of Life Science, Tohoku University, Aoba-ku, Sendai 980-8577, Japan
4 Faculty of Agriculture, Nagoya University, Chikusa-ku, Nagoya 464-8601, Japan
5 Department of Nursing, Yamagata University School of Medicine, Yamagata, Japan
6 Department of Anatomy, Yamagata University School of Medicine, Yamagata, Japan
Correspondence
Hiroyuki Ohta
hohta{at}mx.ibaraki.ac.jp
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Micrographs of the fine structures of strain S213T are available as supplementary material in IJSEM Online.
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). The low organic content of the media undoubtedly holds in check certain rapidly growing organisms that would prevent the growth of the more numerous but more slowly growing bacteria. In the 1970s and 1980s, a series of studies by Hattori and co-workers demonstrated that a number of soil bacteria isolated on low-nutrient media were not only slow growing but also highly sensitive to mineral salts and organic compounds (Hattori, 1976; Hattori & Hattori, 1980; Ohta & Hattori, 1980; Suwa & Hattori, 1984; Whang & Hattori, 1988). Such low-nutrient bacteria were classified as members of oligotrophic groups by their ability to grow on media containing trace amounts of organic nutrients (Ohta & Hattori, 1983a; Suwa & Hattori, 1984). Although members of the genus Arthrobacter (class Actinobacteria) are widespread in soil and are assumed to be examples of soil oligotrophic bacteria (Williams, 1985), a majority of oligotrophic isolates from paddy field soils in Japan belonged to the ‘Alphaproteobacteria’, ‘Betaproteobacteria’ or Cytophaga–Flexibacter–Bacteroides group (Mitsui et al., 1997a).
A soil bacterium, strain S213T, was isolated on a low-nutrient medium from Kashimadai paddy soil near Sendai in Japan (Hattori, 1976), and its growth was severely suppressed by full-strength nutrient broth (Hattori & Hattori, 1980). Strain S213T was tentatively identified as a Gram-negative aerobic bacterium close to Pseudomonas paucimobilis (now Sphingomonas paucimobilis) (Ohta, 1982). Strain S213T is able to grow rapidly with low concentrations (<1 mM) of lignin-related ferulic acid, but growth is inhibited at concentrations above this (Ohta, 2001). Because ferulic acid concentrations in normal paddy soils are low (Shindo & Kuwatsuka, 1977), it seems likely that strain S213T-related organisms play an important role in the process of lignin degradation. With respect to the salt sensitivity of soil oligotrophs, it was reported that a drastic change in the outer membrane structure of a soil bacterium, strain S34, related to the genus Deinococcus was induced by 0·2–0·4 % (w/v) NaCl, and that this change in structure was relieved by 6 mM CaCl2 and induced by 1 mM EGTA (Mitsui et al., 1997b). The aim of the present study was to determine the taxonomic relationships between strain S213T and related species in the Sphingomonas group, using phenotypic, chemotaxonomic and genomic analyses. In addition, we examined the effect of NaCl and CaCl2 on the cell morphology and ultrastructure of strain S213T to show its dependence on calcium.
Strain S213T was maintained as a stab culture in a 100-fold dilution (10–2 NB) of the nutrient broth (NB) containing 0·4 % (w/v) agar at room temperature. NB comprised 1 % (w/v) meat extract (Kyokuto Seiyaku), 1 % (w/v) polypeptone (Nihon Seiyaku) and 0·5 % (w/v) NaCl. pH was adjusted to 7·0 with 1 M NaOH. Cellular morphologies were examined after growth in the late-exponential phase at 27 °C by phase-contrast microscopy and electron microscopy (Mitsui et al., 1997b). The following liquid media were used: (1) 10–2 PM (peptone and meat extract), which comprised 0·01 % (w/v) each of peptone (Kyokuto Seiyaku) and meat extract; (2) 10–2 PM supplemented with 0·1, 0·2, 0·3, 0·4 or 0·5 % (w/v) NaCl; and (3) 10–1 PM, which comprised 0·1 % (w/v) each of peptone and meat extract. CaCl2 was added to media 2 and 3 to a final concentration of 6 mM to determine the effect of calcium ions.
Heat resistance was examined with 28-day-old cultures on 10–2 NB semi-solid agar medium by testing viability after standing for 10 min at 80 °C. Cultures surviving the heat treatment were regarded as spore-formers. To determine the ability of cells to grow anaerobically, cultures of 10–2 NB or 10–2 NB with 0·2 % (w/v) glucose both in the presence and in the absence of 0·1 % (w/v) NaNO3 were incubated in an atmosphere containing 80 % (v/v) N2, 10 % (v/v) H2 and 10 % (v/v) CO2.
Substrate utilization profile was tested in a 1000-fold diluted NB (10–3 NB) liquid medium supplemented with L-arabinose, D-xylose, D-glucose, D-galactose, D-mannose, D-fructose, cellobiose, maltose, lactose, raffinose, acetic acid, DL-lactic acid, gluconic acid, pyruvic acid, 2-oxoglutaric acid, citric acid, succinic acid, L-malic acid or methanol. All compounds were sterilized by filtration and were added to autoclaved 10–3 NB medium. Sugars were added at a concentration of 0·1 % (w/v), organic acids at 0·03 % (w/v) and methanol at 50 mM. Growth was measured over a 2-week period and utilization was assessed by comparing the growth both in the presence and in the absence of an added compound. To test the degradation profile of aromatic compounds, strain S213T was grown at 30 °C in a 10-fold dilution of Difco nutrient broth supplemented with one of the following compounds (1 mM): benzoic acid, ferulic acid, o-, m- and p-hydroxybenzoic acid, o-, m- and p-toluic acid, o- and p-anisic acid, o-, m- and p-cresol, cinnamic acid, m- and p-coumaric acid, phenylacetic acid, phenol, vanillic acid or caffeic acid. Cultures were left for 10 days and degradation of a compound was judged by a change in the UV absorption spectrum. Organic acids including aromatic acids were prepared as sodium salts. Assay for hydrolysis of starch, gelatin and casein and tests for oxidase, catalase and nitrate reduction were carried out as described by Ohta & Hattori (1983b).
Analyses of cellular fatty acids and isoprenoid quinones were performed as described by Komagata & Suzuki (1987). For detection of hydroxy fatty acids, TLC (Kieselgel F-254, Merck) was employed with a solvent system of n-hexane and diethyl ether (1 : 1, v/v). Fatty acid methyl ester analysis by GLC was carried out on a glass column (5 m) packed with 10 % diethyleneglycol succinate using standard fatty acid methyl esters, as described by Ohta & Hattori (1983b). Cellular lipids were analysed by the method of Hirai et al. (1995) using Sphingomonas paucimobilis JCM 7516T as the reference strain. For detection of alkaline-stable glycolipids, the total extractable lipids were incubated in 1 M KCl and methanol (2 : 1, v/v) for 2 h at 37 °C and analysed by TLC with a solvent system composed of chloroform, methanol and water (70 : 30 : 5, by volume).
Isolation of DNA (Saito & Miura, 1963) and determination of the DNA G+C content by the thermal denaturation method (Marmur & Doty, 1962) followed standard procedures. DNA–DNA relatedness was estimated by a chemiluminescence DNA–DNA hybridization method with photobiotin-labelled probes in microplate wells, as described by Ezaki et al. (1989). For enzymic development, alkaline phosphatase–streptavidin conjugate (Vector) was used with CDP-Star (Tropix) as the substrate and chemiluminescence was measured on a Wallac 1420 ARVOsx multilabel counter.
The 16S rRNA gene sequence of strain S213T was obtained by PCR amplification of genomic DNA using a universal primer set, and the nucleotide sequence (nucleotide positions 28–1390; Escherichia coli numbering) was determined as described by Hiraishi (1992). The DNA sequence was aligned with reference sequences of representative species of Sphingomonas sensu stricto, Novosphingobium, Sphingobium and Sphingopyxis. Multiple alignments, calculation of nucleotide substitution rates (Knuc values) as described by Kimura (1980) and construction of a phylogenetic tree by the neighbour-joining method (Saitou & Nei, 1987) were performed by using the CLUSTAL W program (Thompson et al., 1994). The robustness of tree topology was evaluated by a bootstrap analysis (1000 replications).
Strain S213T showed a range of phenotypic properties typical of members of the genus Sphingomonas (Yabuuchi et al., 1990; Takeuchi et al., 2001). Cells are strictly aerobic, Gram-negative, non-sporulating and catalase-positive rods (0·4–0·6x1·0–1·5 µm). Colonies are pale yellow on 10–2 NB agar and yellow on a 10-fold diluted NB agar medium. When ferulate-limited chemostat-cultured cells (Ohta, 2001) were used for analysis of acetone-soluble pigments (70 mg wet cells with 400 µl acetone), the spectrum of the acetone extract had peaks at 454 and 482 nm and a shoulder at 431 nm. Strain S213T grew at 4, 10, 25, 30 and 37 °C but not at 42 °C in 10–2 NB liquid cultures.
When grown in 10–2 PM, strain S213T clearly shows the typical cell wall structure of Gram-negative bacteria, as recognized from the presence of the outer membrane and the peptidoglycan layer (see Fig. A available as supplementary material in IJSEM Online). When 20 phase-contrast microscopic fields, each containing 50–70 cells, were observed, the ratios of aberrant to normal cells in 10–2 PM supplemented with 0, 0·1, 0·2 and 0·3 % (w/v) NaCl were 0 (Fig. 1A), 0·23, 0·64 and 0·83, respectively. With increasing NaCl concentration, cells became longer and, at 0·4 % (w/v) NaCl, all cells resembled long filaments and seemed to be aberrant in form (Fig. 1B). At 0·5 % (w/v) NaCl, faint ghost-like filaments were observed exclusively. When cells were grown in 10–1 PM, they became longer and aberrant but less remarkably so (data not shown). Calcium significantly relieved this effect of NaCl as in the case of strain S34, a highly halo-sensitive soil bacterium (Mitsui et al., 1997b). When 6 mM CaCl2 was added, cells of strain S213T grew quite normally and the ratio of aberrant to normal cells was 0 at every NaCl concentration tested (0·1–0·5 %, w/v) in 10–2 PM or in 10–1 PM. In the presence of 0·1 % (w/v) NaCl, deposition of electron-dense particles between the outer and inner membranes became apparent (supplementary Figs B and C in IJSEM Online). With the addition of 0·4 % (w/v) NaCl, three types of structural change were observed: (1) membrane-deposited particles were excluded from the cells (supplementary Fig. D), (2) membrane structure remained normal but division was inhibited (supplementary Fig. E), and (3) cell lysis occurred (supplementary Fig. D). These detrimental effects of NaCl on the cellular structure were not detected in the presence of CaCl2 (supplementary Fig. F).
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, the major polar lipids of RF values 0·57 and 0·78 corresponded to phosphatidyl ethanolamine and cardiolipin, respectively. In our preparation of polar lipids, the spot of phosphatidyl glycerol was not clearly detected in strain S213T. Mild alkaline hydrolysis of the total extractable lipids and subsequent TLC analysis revealed that the major lipid of RF value 0·41 was an alkaline-stable glycolipid, probably glucuronosyl ceramide reported with Sphingomonas paucimobilis JCM 7516T by Yabuuchi et al. (1990). A minor spot of alkaline-stable glycolipid of RF value 0·25 was also detected in strain S213T but its relation to the glycolipids GX1, GX2, GX3 and GL' of the Sphingomonas group (Yabuuchi et al., 1990) is currently unknown.
The 16S rRNA gene sequence (1306 bp) of strain S213T was used for searches in the GenBank, EMBL and DDBJ databases by the FASTA program (Pearson & Lipman, 1988). Strain S213T is a member of the Sphingomonadaceae, most closely related to the genus Sphingomonas. Sequence similarity calculations indicated that the nearest relatives of the strain are Sphingomonas mali IFO 15500T (98·3 %), Sphingomonas pruni IFO 15498T (98·0 %), Sphingomonas asaccharolytica IFO 15499T (97·9 %) and Sphingomonas echinoides DSM 1805T (97·8 %). Similarities of 95 to 97 % were found to the 16S rRNA gene sequences of Sphingomonas melonis DAPP-PG 224T (96·9 %), Sphingomonas adhaesiva GIFU 11458T (96·1 %), Sphingomonas sanguinis IFO 13937T (95·4 %) and Sphingomonas parapaucimobilis JCM 7510T (95·6 %). Construction of a 16S rRNA gene sequence-based phylogenetic tree indicated that strain S213T branched with Sphingomonas echinoides DSM 1805T with high bootstrap support (Fig. 2).
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). DNA–DNA relatedness between strain S213T and strains of phylogenetically related Sphingomonas species was analysed. Strain S213T showed very low DNA–DNA relatedness values to its closest phylogenetic neighbours, Sphingomonas echinoides NBRC 15742T (=DSM 1805T) (10 %), Sphingomonas asaccharolytica IFO 15499T (10 %), Sphingomonas mali IFO 15500T (12 %) and Sphingomonas pruni IFO 15498T (6 %), whereas relatedness values of 22, 17 and 16 % were found between Sphingomonas echinoides DSM 1805T and the type strains of Sphingomonas pruni, Sphingomonas asaccharolytica and Sphingomonas mali, respectively.
Takeuchi et al. (2001) have shown that polyamine patterns and nitrate reduction provide good diagnostic markers for differentiation of Sphingomonas, Sphingobium, Novosphingobium and Sphingopyxis species. Although polyamine was not analysed in this study, the assignment of strain S213T to the genus Sphingomonas is supported by its phylogenetic position and nitrate reduction data. As shown in Table 1
, strain S213T can be clearly differentiated from other phylogenetically related Sphingomonas species on the basis of major 2-hydroxy fatty acids and several phenotypic characteristics. The genomic and phenotypic evidence presented here clearly indicate that strain S213T is representative of a novel species of the genus Sphingomonas, for which the name Sphingomonas oligophenolica sp. nov. is proposed.
Description of Sphingomonas oligophenolica sp. nov.
Sphingomonas oligophenolica (o.li.go.phe.no'li.ca. Gr. adj. oligos little, scanty; N.L. n. phenol phenol; N.L. fem. adj. oligophenolica relating to small amounts of phenolic compounds).
Cells are Gram-negative, non-motile, non-sporulating rods (0·4–0·6 µm wide and 1·0–1·5 µm long). Colonies are circular and convex with entire margins, pale yellow and pinpoint after 3 days incubation on a 100-fold diluted nutrient broth medium and yellow and 0·6–0·8 mm in diameter after 3 days incubation on a 10-fold diluted nutrient broth medium. Growth is suppressed slightly in the presence of 0·1 % (w/v) NaCl; this suppression is enhanced with increasing NaCl concentration in cultures. In the presence of 0·5 % (w/v) NaCl cells become faint ghost-like filaments. NaCl-induced aberrant cell morphologies are significantly reduced by the addition of calcium (6 mM CaCl2). Able to grow at 4–37 °C but not at 42 °C. Strictly aerobic, catalase-positive and oxidase-positive. Nitrate is reduced to nitrite but not to N2. Hydrolyses gelatin, but not starch or casein. Acid is not produced from glucose. Assimilates L-arabinose, D-xylose, D-glucose, D-galactose, D-mannose, cellobiose, maltose, lactose, raffinose, acetic acid, DL-lactic acid, gluconic acid, pyruvic acid, 2-oxoglutaric acid, ferulic acid, p-hydroxybenzoic acid, p-coumaric acid and vanillic acid. The following compounds are not utilized: D-fructose, citric acid, succinic acid, L-malic acid, benzoic acid, o- and m-hydroxybenzoic acid, o-, m- and p-toluic acid, o- and p-anisic acid, o-, m- and p-cresol, cinnamic acid, m-coumaric acid, phenylacetic acid, phenol, caffeic acid and methanol. The major non-polar fatty acids are C18 : 1 and C16 : 0, and the major 2-hydroxy fatty acid is C14 : 0 2-OH. No 3-OH fatty acids are present. The major isoprenoid quinone is ubiquinone Q-10. Sphingoglycolipid is present. Acetone-soluble pigment is characterized by 
max at 454 and 482 nm. The DNA G+C content is 64·2 mol%.
The type strain, S213T (=JCM 12082T=CIP 107926T), was isolated from paddy soil near Sendai in Japan.
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