Abstract
The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain Gsoil 104T is AB245371.
Footnotes
,†,The genus Pedobacter was first described by Steyn et al. (1998) and currently comprises species isolated from soil (Pedobacter heparinus, P. africanus, P. saltans and P. sandarakinus), from a commercial nitrifying inoculum (Pedobacter caeni), from fish (Pedobacter piscium), from a glacier in the Tyrolean Alps (Pedobacter cryoconitis) and from glacial water in the Himalayan mountains of India (Pedobacter himalayensis) (Steyn et al., 1998; Margesin et al., 2003; Shivaji et al., 2005; Vanparys et al., 2005; Yoon et al., 2006). Two further species of the genus, Pedobacter roseus and Pedobacter aquatilis, have been described recently (Gallego et al., 2006; Hwang et al., 2006). The members of the genus Pedobacter have the following characteristics: they are Gram-negative rods, they are obligately aerobic, positive for catalase, oxidase and heparinase, they may or may not show gliding motility, they are negative for urease, lipase, gelatinase, indole production and nitrate reduction and they contain iso-C15 : 0, iso-C15 : 0 2-OH, iso-C15 : 0 3-OH, C16 : 0, C16 : 1ω5c, C16 : 1ω7c, C16 : 0 3-OH, iso-C17 : 0 3-OH and iso-C17 : 1ω9c fatty acids (Steyn et al., 1998).
During the course of a study on the culturable aerobic and facultative anaerobic bacterial community living in the soil of a ginseng field in Pocheon Province (South Korea), a large number of novel bacterial strains were isolated. In this study, we have characterized one of these isolates, strain Gsoil 104T. Our phenotypic, genotypic, chemotaxonomic and phylogenetic analyses have established the affiliation of the isolate to the genus Pedobacter. The data obtained also suggest that the isolate represents a novel species of the genus Pedobacter.
Strain Gsoil 104T was originally isolated from a soil sample from a ginseng field in Pocheon Province (South Korea). The soil sample was suspended in 50 mM phosphate buffer (pH 7.0) and spread on plates of 1/5-strength modified R2A agar (0.25 g tryptone, 0.25 g peptone, 0.25 g yeast extract, 0.125 g malt extract, 0.125 g beef extract, 0.25 g Casamino acids, 0.25 g soytone, 0.5 g glucose, 0.3 g soluble starch, 0.2 g xylan, 0.3 g sodium pyruvate, 0.3 g K2HPO4, 0.05 g MgSO4, 0.05 g CaCl2 and 15 g agar l1) after serial dilution with 50 mM phosphate buffer (pH 7.0). The plates were incubated at 25 °C for 1 month. Single colonies on the plates were purified by transferring them onto new plates and were incubated once again on modified R2A or on half-strength modified R2A. Purified colonies were tentatively identified from partial sequences of the 16S rRNA gene (Im et al., 2005). Gsoil 104T was one of the dominant isolates on the modified R2A agar plates under aerobic conditions. It was routinely cultured on R2A agar at 30 °C and was maintained as a glycerol suspension (20 %, w/v) at 70 °C.
A nearly-complete 16S rRNA gene sequence of strain Gsoil 104T was determined as described below. DNA was extracted using a commercial genomic DNA-extraction kit (Core Biosystem) and PCR-mediated amplification of the 16S rRNA gene and sequencing of the purified PCR product were carried out according to Kim et al. (2005). Full sequences of the 16S rRNA gene were compiled using SeqMan software (DNASTAR). The 16S rRNA gene sequences of related taxa were obtained from the GenBank database. Multiple alignments were performed with the CLUSTAL_X program (Thompson et al., 1997) and gaps were edited in the BioEdit program (Hall, 1999). Evolutionary distances were calculated using the Kimura two-parameter model (Kimura, 1983). Phylogenetic trees were constructed by using the neighbour-joining method (Saitou & Nei, 1987) and the maximum-parsimony method (Fitch, 1971) using the MEGA3 program (Kumar et al., 2004) with bootstrap values based on 1000 replications (Felsenstein, 1985).
Comparative 16S rRNA gene sequence analyses of strain Gsoil 104T (1430 bp) showed that the strain is phylogenetically affiliated to Pedobacter species. The phylogenetic tree (Fig. 1) based on the neighbour-joining algorithm showed strain Gsoil 104T to have a distinct phylogenetic position within the genus Pedobacter. The almost-complete 16S rRNA gene sequence of strain Gsoil 104T exhibits similarity levels of 97 % with respect to the type strains of six Pedobacter species with validly published names, namely P. africanus DSM 12126T (97.0 %), P. caeni LMG 22862T (96.9 %), P. cryoconitis DSM 14825T (96.8 %), P. heparinus DSM 2366T (96.6 %), P. piscium DSM 11725T (96.5 %) and P. himalayensis JCM 12171T (96.4 %). The levels of 16S rRNA gene sequence similarity with P. sandarakinus KCTC 12559T and P. saltans DSM 12145T are only 93.7 and 90.1 %, respectively. In the phylogenetic tree constructed, strain Gsoil 104T is clearly separated from P. sandarakinus and P. saltans as well as from P. roseus CL-GP80T and P. aquatilis AR107T. Strain Gsoil 104T and Pedobacter species (except P. saltans) form a monophyletic clade with a high bootstrap value (100 %) that was supported by the neighbour-joining and maximum-parsimony methods employed in this study for phylogenetic tree construction. The generally accepted criteria for delineating bacterial species state that strains with a DNADNA relatedness value below 70 % (as measured by hybridization), or strains with 16S rRNA gene sequence dissimilarity above 3 %, are considered as belonging to separate species (Wayne et al., 1987; Stackebrandt & Goebel, 1994; Stackebrandt et al., 2002). On this basis, our data indicate that strain Gsoil 104T is highly likely to represent a novel species of the genus Pedobacter.
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The Gram reaction was determined using the non-staining method, as described by Buck (1982). Cell morphology was observed under a Nikon light microscope at x1000, using cells grown for 6 days at 25 °C on R2A agar. Catalase activity was determined from bubble production in 3 % (v/v) H2O2 and oxidase activity was determined using 1 % (w/v) tetramethyl-p-phenylenediamine. To determine the assimilation of single carbon sources, a defined liquid medium containing basal salts was used, as follows (g l1): K2HPO4, 1.8 g; KH2PO4, 1.08 g; NaNO3, 0.5 g; NH4Cl, 0.5 g; KCl, 0.1 g; MgSO4, 0.1 g; and CaCl2, 0.05 g. A vitamin solution (Widdel & Bak, 1992), a trace element solution (SL-10; Widdel et al., 1983) and a selenite/tungstate solution (Tschech & Pfennig, 1984) were added to this medium, and the pH was adjusted to 6.8. This liquid medium was poured into 96 wells and 25x stock filter-sterilized carbon sources were added to each well. The wells were incubated at 25 °C for up to 7 days and were examined visually for growth. Negative-control wells did not contain any carbon sources. Positive-control wells comprised cultures grown in R2A broth. Some physiological characteristics were determined with API 20E galleries, according to the instructions of the manufacturer (bioMérieux). Anaerobic growth and anaerobic reduction of nitrate as the final electron acceptor were determined in serum bottles containing R2A broth to which thioglycolate (1 g l1) had been added and in which the upper air layer had been replaced with N2; for determination of nitrate reduction, nitrate was added as KNO3 at a concentration of 10 mM. Aerobic reduction of nitrate was later confirmed by inoculation into serum bottles (25 ml) containing 12 ml R2A media, with nitrate being added as KNO3 at 10 mM. The reduction of nitrate was monitored by ion chromatography on a model 790 personal IC (Metrohm) equipped with a conductivity detector and an anion exchange column (Metrosep Anion Supp 4; Metrohm). The degradation of DNA (using DNase agar from Scharlau, supplemented with 1 M HCl), casein, chitin, starch (Atlas, 1993), lipid (Kouker & Jaeger, 1987), xylan and cellulose (Ten et al., 2004) was also investigated; reactions were read after 7 days. Growth at different temperatures (4, 15, 25, 30, 37 and 42 °C) and various pH values (pH 4.510.0, using increments of 0.5 pH units) was assessed after 5 days incubation. Salt tolerance was tested on R2A medium supplemented with 110 % (w/v) NaCl after 5 days incubation. Growth on nutrient agar, trypticase soy agar (Difco) and MacConkey agar was also evaluated, at 25 °C.
The cells of strain Gsoil 104T were Gram-negative, aerobic, non-spore-forming, non-motile and rod-shaped. After 6 days incubation at 25 °C on R2A, colonies were 25 mm in diameter, smooth, convex, round, glossy and white. On R2A agar, the optimal growth temperature for Gsoil 104T was 25 °C; the strain was able to grow at 430 °C, but not at 37 °C. The strain grew between pH 5.0 and 8.5, with an optimum between pH 6.5 and 7.5. Growth occurred in the absence of NaCl and in the presence of 1 % (w/v) NaCl, but not in the presence of 2 % (w/v) NaCl. The biochemical characteristics of strain Gsoil 104T were found to be similar to those reported for members of the genus Pedobacter (Steyn et al., 1998), i.e. positive for oxidase and catalase, able to assimilate D-mannose, D-glucose, N-acetyl-D-glucosamine and amygdalin, negative for H2S production, indole production, urease, lipase and nitrate reduction and unable to produce acid from a large number of substrates. The phenotypic and chemotaxonomic characteristics that differentiate strain Gsoil 104T from related Pedobacter species are listed in Table 1. In contrast to all other Pedobacter species, Gsoil 104T does not hydrolyse aesculin.
Table 1. Physiological and biochemical characteristics of strain Gsoil 104T and related Pedobacter species Taxa: 1, strain Gsoil 104T; 2, P. africanus; 3, P. caeni; 4, P. cryoconitis; 5, P. heparinus; 6, P. piscium; 7, P. himalayensis; 8, P. sandarakinus; 9, P. saltans. Data for reference species are from Steyn et al. (1998), Margesin et al. (2003), Shivaji et al. (2005), Vanparys et al. (2005) and Yoon et al. (2006). All taxa are positive for the following: aerobic growth, catalase, oxidase and utilization of D-mannose, D-glucose, N-acetyl-D-glucosamine, amygdalin (not done for P. himalayensis), D-lactose, D-melibiose (variable for P. saltans), sucrose (variable for P. saltans) and D-trehalose (variable for P. saltans) as sole carbon sources. All strains are negative for the following: Gram stain, sporulation, production of indole and H2S, urease, reduction of nitrate to nitrite and utilization of L-sorbose, D-lyxose (not done for P. himalayensis), D-fucose (not done for P. himalayensis), dulcitol, inositol, citrate, L-lysine (not done for P. sandarakinus), gluconate (not done for P. himalayensis), adipate (not done for P. himalayensis), caprate (not done for P. himalayensis), phenylacetate (not done for P. himalayensis) and malate as sole carbon sources. Symbols: +, positive; , negative; V, variable; ND, no data available.
For measurement of the G+C content of chromosomal DNA, the genomic DNA of the strain was extracted and purified as described by Moore & Dowhan (1995) and enzymically degraded into nucleosides. The G+C content of the DNA was then determined as described by Mesbah et al. (1989), using reversed-phase HPLC. Isoprenoid quinones were extracted with chloroform/methanol (2 : 1, v/v), evaporated under a vacuum and re-extracted in n-hexane/water (1 : 1, v/v). The crude quinone in n-hexane was purified using Sep-Pak Vac Cartridges Silica (Waters) and subsequently analysed by HPLC, as described previously (Hiraishi et al., 1996).
Cellular fatty acids were analysed after culture on trypticase soy agar for 2 days. The cellular fatty acids were saponified, methylated and extracted according to the protocol of the Sherlock Microbial Identification System (MIDI). The fatty acids were then analysed by GC (model 6890; Hewlett Packard) using the Microbial Identification software package (Sasser, 1990). Summed features, which are mixtures of two or three fatty acids, were analysed further using GC/MS.
The cellular fatty acid profiles of strain Gsoil 104T and related Pedobacter species are presented in Table 2. The major components were C16 : 1ω7c, iso-C15 : 0, iso-C17 : 0 3-OH and iso-C15 : 0 2-OH, which is a profile typical of members of the genus Pedobacter (Steyn et al., 1998). However, some differences in the proportions of the fatty acids could be observed between strain Gsoil 104T and the phylogenetically closest relatives. One of the major fatty acids found in strain Gsoil 104T was C16 : 0 (15.6 % of total). This value is generally much higher than that reported for other Pedobacter species; only P. cryoconitis DSM 14825T (9.1 %) and P. himalayensis HHS 22T (7.3 %) have comparable levels of C16 : 0. The DNA G+C content for the genus Pedobacter ranges from 36.9 mol% (reported for P. saltans) to 44.2 mol% (reported for P. africanus) (Steyn et al., 1998). The G+C content of the DNA of strain Gsoil 104T was within this range (43.6 mol%). The predominant respiratory quinone of strain Gsoil 104T was MK-7.
Table 2. Fatty acid composition (%) of strain Gsoil 104T and related Pedobacter species Strains: 1, strain Gsoil 104T; 2, P. africanus DSM 12126T (data from Steyn et al., 1998); 3, P. caeni LMG 22862T (Vanparys et al., 2005); 4, P. cryoconitis DSM 14825T (Shivaji et al., 2005); 5, P. heparinus DSM 2366T (Steyn et al., 1998); 6, P. piscium DSM 11725T (Steyn et al., 1998); 7, P. himalayensis HHS 22T (Shivaji etal., 2005); 8, P. sandarakinus KCTC 12559T (Yoon et al., 2006); 9, P. saltans DSM 12145T (Steyn et al., 1998). tr, Trace amount (<1 %); , not detected.
To clarify the taxonomic position of strain Gsoil 104T, DNADNA hybridization was performed with the four members of the genus most closely related to strain Gsoil 104T. DNADNA hybridization was performed fluorometrically according to the method of Ezaki et al. (1989), using photobiotin-labelled DNA probes (Sigma) and microdilution wells (Greiner), with five replications for each sample. The highest and lowest values obtained for each sample were excluded and the means of the remaining three values are quoted as the DNA hybridization values. Strain Gsoil 104T exhibited relatively low levels of DNADNA relatedness with respect to P. africanus KACC 11389T (36 %), P. cryoconitis KACC 11394T (30 %), P. caeni DSM 16990T (25 %) and P. heparinus DSM 2366T (19 %), indicating that it is not related to them at the species level (Wayne et al., 1987).
The results obtained from the phenotypic and phylogenetic characterizations indicated that strain Gsoil 104T belongs to the genus Pedobacter. The phylogenetic distinctiveness of strain Gsoil 104T, together with the DNADNA hybridization data, confirmed that this isolate represents a species that is distinct from recognized Pedobacter species. There are some phenotypic differences between strain Gsoil 104T and phylogenetically related Pedobacter species (Table 1). Therefore, on the basis of the data presented, strain Gsoil 104T should be classified within the genus Pedobacter as the type strain of a novel species, for which the name Pedobacter ginsengisoli sp. nov. is proposed.
Description of Pedobacter ginsengisoli sp. nov.
Pedobacter ginsengisoli (gin.sen.gi.so'li. N.L. n. ginsengum ginseng; L. n. solum soil; N.L. gen. n. ginsengisoli of soil from a ginseng field, the source of the type strain).
Cells are Gram-negative, aerobic, non-spore-forming, non-motile and rod-shaped (0.51.0x2.54.5 µm). After 6 days incubation at 25 °C on R2A, colonies are 25 mm in diameter, smooth, convex, round, glossy and white. Grows at 430 °C; the optimum temperature for growth is 25 °C. The minimum pH for growth lies between 4.5 and 5.0, the optimum pH is 6.57.5 and the maximum pH lies between 8.5 and 9.0. Tolerates 1 % (w/v) NaCl, but not 2 %. Growth occurs on trypticase soy agar, but not on MacConkey agar. Positive for catalase and oxidase, but negative for lipase. Negative for hydrolysis of chitin, starch, cellulose, xylan, casein and aesculin and positive for hydrolysis of DNA. The following substrates are utilized for growth: D-glucose, D-galactose, D-mannose, D-fructose, D-xylose, L-xylose, N-acetyl-D-glucosamine, salicin, D-cellobiose, D-lactose, D-maltose, D-melibiose, sucrose, D-trehalose, D-raffinose, amygdalin, glycerol, inulin and dextran. The following substrates are not utilized for growth: D-arabinose, L-arabinose, D-fucose, ethanol, L-rhamnose, L-sorbose, D-lyxose, D-ribose, pyruvate, formate, acetate, propionate, DL-3-hydroxybutyrate, valerate, caprate, maleate, fumarate, phenylacetate, benzoate, 3-hydroxybenzoate, 4-hydroxybenzoate, citrate, lactate, malate, malonate, succinate, glutarate, tartrate, itaconate, adipate, suberate, oxalate, gluconate, dulcitol, inositol, D-adonitol, D-mannitol, D-sorbitol, xylitol, methanol, glycogen, L-alanine, L-arginine, L-asparagine, L-aspartic acid, L-cysteine, L-glutamic acid, L-glutamine, L-histidine, glycine, L-isoleucine, L-leucine, L-lysine, L-methionine, L-phenylalanine, L-proline, L-serine, L-threonine, L-tryptophan, L-tyrosine and L-valine. In API 20E tests, the VogesProskauer test is positive and tests for arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, tryptophan deaminase, urease, gelatinase, β-galactosidase and production of hydrogen sulphide and indole are all negative. Acid is not produced from D-glucose, D-melibiose, amygdalin, L-arabinose, D-mannitol, inositol, D-sorbitol, L-rhamnose or sucrose. The major fatty acids are C16 : 1ω7c, iso-C15 : 0, C16 : 0, iso-C17 : 0 3-OH and iso-C15 : 0 2-OH. The G+C content of the genomic DNA is 43.6 mol%. The predominant respiratory quinone is MK-7.
The type strain, Gsoil 104T (=KCTC 12576T=LMG 23399T), was isolated from a soil sample from a ginseng field in Pocheon Province (South Korea).
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