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1 Molecular Biology Laboratory, Department of Zoology, University of Delhi, Delhi – 110007, India
2 Center for Cellular and Molecular Biology, Hyderabad – 500007, India
3 Department of Genetics, University of Kaiserslautern, 67663 Kaiserslautern, Germany
4 EPFL, ENAC-ISTE, Laboratory of Environmental Biotechnology, CH 1015 Lausanne, Switzerland
Correspondence
Rup Lal
duzdel{at}vsnl.com
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ABSTRACT |
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 TOP ABSTRACT Introduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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Published online ahead of print on 29 April 2005 as DOI 10.1099/ijs.0.63201-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of Sphingobium indicum sp. nov. MTCC 6364T and Sphingobium francense sp. nov. MTCC 6363T are AY519129 and AY519130, respectively.
A table showing DNA–DNA relatedness values for strains B90A, UT26, Sp+ and Sphingomonas paucimobilis ATCC 29837T is available as supplementary material in IJSEM Online.
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Introduction |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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). Three such strains of Sphingomonas paucimobilis, SS86 (UT26), Sp+ and B90A, have been isolated from different geographical locations (Senoo & Wada, 1989; Sahu et al., 1990; Dogra et al., 2004). The mutant strain UT26 is resistant to nalidixic acid and is derived from the original SS86 strain that was isolated in 1989 from upland fields in Japan where gamma-HCH had been applied for 15 years (Senoo & Wada, 1989; Wada et al., 1989). Strain Sp+ was isolated from French soils contaminated with gamma-HCH presumably for only a few years (Dogra et al., 2004). Both UT26 and Sp+ were found to degrade alpha-, gamma- and delta-HCH, but neither strain was able to degrade beta-HCH. Strain B90A, isolated in 1989 from rice rhizosphere soil in India under repeated treatment with technical HCH (Sahu et al., 1990), degraded all HCH isomers, including beta-HCH, but at different rates (Sahu et al., 1990; Johri et al., 1998; Kumari et al., 2002; Dogra et al., 2004). The catabolic genes responsible for the degradation of HCH isomers found in the three strains are almost identical (Nagata et al., 1999; Kumari et al., 2002; Dogra et al., 2004). These genes, linA, linB, linC (linX), linD and linE, encode HCH dehydrochlorinase, halidohydrolase, dehydrogenase, dechlorinase and ring cleavage dioxygenase, respectively. Interestingly, B90A was found to contain multiple copies of linA and linX, compared with only one copy of each gene in Sp+ and UT26 (Kumari et al., 2002; Dogra et al., 2004). All lin genes in these strains are associated with IS6100 insertion sequences (Dogra et al., 2004). This prompted us to determine the taxonomic position of these three strains. A polyphasic investigation was conducted using 16S rRNA gene sequences, DNA–DNA hybridization, fatty acid and polar lipid analyses and biochemical parameters. The data obtained show that each of these three strains constitutes a different species of Sphingobium and that they do not represent any currently known species. The novel species are characterized and described. While classifying the three novel strains, we noticed that [Sphingomonas] chungbukensis IMSNU 11152T also clustered with species of the recently described genus Sphingobium. Thus, we also propose to transfer [Sphingomonas] chungbukensis to Sphingobium chungbukense comb. nov. |
16S rRNA gene sequencing and analysis |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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. PCR amplification of 16S rRNA genes and DNA sequencing were carried out as described by Reddy et al. (2000). The CLUSTAL_X program (Thompson et al., 1997) from the European Bioinformatics Institute website (http://www.ebi.ac.uk/) was used to align the sequences. The 16S rRNA gene sequences of the three strains, B90A, UT26 and Sp+, showed similarity values of 91·9–92·7 % when compared with that of the type strain of S. paucimobilis, ATCC 29837T. This indicated that they are probably not members of the species Sphingomonas paucimobilis. Between the three strains, 16S rRNA gene sequence similarity was 99·1–99·4 %. Similarity searches showed that the 16S rRNA gene sequences of B90A, UT26 and Sp+ were most similar to those of [Sphingomonas] chungbukensis IMSNU 11152T (98·5–98·8 %) and Sphingobium chlorophenolicum ATCC 33790T (98·1–98·4 %).
The nearly full-length 16S rRNA gene sequences of the 25 species with validly published names of the genera Sphingomonas and Sphingobium, as well as the sequence of Rhodanobacter lindaniclasticus RP 5557T (Nalin et al., 1999), which also contains lin genes, were retrieved from GenBank. These sequences and those of the three study strains were aligned using CLUSTAL_X. The alignment was checked manually for quality and the terminal nucleotides not common to all 29 sequences were removed. Phylogenetic analysis was carried out using the PHYLIP package, version 3.5 (Felsenstein, 1993). The evolutionary distance matrix was calculated using the distance model of Jukes & Cantor (1969). The evolutionary tree (Fig. 1) was constructed using the neighbour-joining method (Saitou & Nei, 1987) and the resultant tree topologies were evaluated by bootstrap analysis based on 100 resamplings, using the SEQBOOT and CONSENSE programs in the PHYLIP package (Fig. 1). Strains B90A, UT26 and Sp+ were in a monophyletic clade represented by species of the genus Sphingobium as well as [Sphingomonas] chungbukensis IMSNU 11152T. Strains B90A, UT26 and Sp+ showed 16S rRNA gene sequence similarity to [Sphingomonas] chungbukensis IMSNU 11152T and Sphingobium chlorophenolicum ATCC 33790T ranging from 98·5 to 98·8 % and 98·1 to 98·4 %, respectively. 16S rRNA gene sequence similarity between [Sphingomonas] chungbukensis IMSNU 11152T and species of Sphingobium in the monophyletic cluster ranged between 95·6 and 98·1 % (Kim et al., 2000), with a similarity of 98·1 % between [Sphingomonas] chungbukensis IMSNU 11152T and Sphingobium chlorophenolicum ATCC 33790T. Parsimony analysis was also performed for the aligned sequence data using DNAPARS including bootstrap analysis with 100 resamplings. This gave a tree topology very similar to that obtained with the distance method (data not shown).
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DNA–DNA hybridization |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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). DNA–DNA relatedness between the strains was determined according to Bala et al. (2004). DNA (10 µg) of each strain was transferred onto a positively charged nylon membrane (Hybond-N; Amersham) using a dot blot apparatus (Bio-Rad). The membrane was air-dried and cross-linked. The DNA probe for each strain was labelled with [
-P32]-ATP (BRIT) using a nick-translation kit (Amersham Pharmacia). Hybridization was performed overnight at 65 °C. After hybridization, the filter was washed with SSC and SDS to remove unbound probe. The amount of the probe bound to the DNA was estimated using a scintillation counter (Beckman Instruments) and hybridization values obtained were expressed as percentage of the probe bound relative to the homologous reaction. DNA from each of the seven strains was bound to the filters and hybridized with DNA probes prepared from each strain. The DNA–DNA hybridization data (Supplementary Table S1 in IJSEM Online) showed that B90A, UT26 and Sp+ had DNA–DNA relatedness values of 13, 10 and 8 % respectively with the type strain Sphingomonas paucimobilis ATCC 29837T. The DNA–DNA relatedness values between B90A, UT26 and Sp+ varied from 19 to 59 %. [Sphingomonas] chungbukensis IMSNU 11152T and Sphingobium chlorophenolicum ATCC 33790T were not only more closely related to B90A, UT26 and Sp+ based on 16S rRNA gene sequence (Fig. 1
), but the genomic DNA–DNA relatedness values also indicated that these strains are more closely related to [Sphingomonas] chungbukensis IMSNU 11152T and Sphingobium chlorophenolicum ATCC 33790T than to Sphingomonas paucimobilis ATCC 29837T (see Supplementary Table S1 in IJSEM Online). All DNA–DNA hybridization values were below the threshold value (70 %) that has been suggested as delineating a bacterial species (Wayne et al., 1987). These data support the results of 16S rRNA gene sequence analysis and lend support to the view that B90A, UT26 and Sp+ represent three distinct species of Sphingobium.
Primarily based on the phylogenetic analysis of 16S rRNA gene sequences of the then known species of Sphingomonas and some chemotaxonomic and phenotypic differences among them, Takeuchi et al. (2001) proposed the creation of three new genera, Sphingobium, Novosphingobium and Sphingopyxis, in addition to the genus Sphingomonas sensu stricto. The genus Sphingobium was proposed to accommodate a group of species that formed a monophyletic cluster, including Sphingobium chlorophenolicum, Sphingobium herbicidivorans and Sphingobium yanoikuyae. However, the 16S rRNA gene sequence and description of [Sphingomonas] chungbukensis IMSNU 11152T (Kim et al. 2000) were not available at the time that Takeuchi et al. (2001) made their proposal for the new genus Sphingobium. Since [Sphingomonas] chungbukensis IMSNU 11152T falls within a monophyletic cluster represented exclusively by species of the genus Sphingobium, it also appears to belong to the genus Sphingobium (Fig. 1).
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DNA profiling, IS6100 and evolution of lin genes |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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. Electrophoresis was conducted in 0·5x TBE buffer at 14 °C using a CHEF DR III system (Bio-Rad). Lambda DNA concatemers (Amersham) were used as molecular mass standards. Digests were performed with the rarely cutting restriction enzymes XbaI and AseI. XbaI produced ranges of fragment sizes which could be resolved well by PFGE. XbaI digests of the six strains were distinctly different (data not shown) with no discernible resemblance between them (data not shown). Although the results of PFGE profiling alone cannot be used to describe the strains as three different species of Sphingobium, they provide additional support to the results of 16S rRNA gene sequencing and DNA–DNA hybridization.
While there are differences between the strains as regards 16S rRNA gene sequences, DNA–DNA relatedness and PFGE profiling, each strain possesses highly similar lin genes, which are associated with copies of IS6100 insertion sequences (Kumari et al., 2002; Dogra et al., 2004). Strains B90A, UT26 and Sp+ contain 11, 5 and 6 copies of IS6100, respectively, at different chromosomal positions. We therefore decided to investigate the presence of IS6100 and lin genes in Sphingomonas paucimobilis ATCC 29837T, [Sphingomonas] chungbukensis IMSNU 11152T, Sphingobium chlorophenolicum ATCC 33790T and Sphingomonas xenophaga DSM 6383T by Southern blot hybridization and PCR amplification. None of these strains carried linA, linB, linC (linX), linD or linE (data not shown). Interestingly, the linA genes of B90A, UT26 and Sp+, while nearly identical, showed a strange mosaic configuration (Dogra et al., 2004). It has been suggested that linA was transferred into the common ancestor by IS6100, followed by geographical dispersion (Kumari et al., 2002; Dogra et al., 2004). However, the present work shows that the three strains differ from each other so much that they should be considered to represent separate species. This makes it more likely that the lin genes have been transferred into the three strains as a result of independent events from an, as-yet unknown, host strain.
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Polar lipid and fatty acid analyses |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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, b). Fatty acid methyl esters were analysed from 40 mg cells scraped from a Petri dish and subjected to saponification, methylation and extraction using the method of Miller (1982) and Kuykendall et al. (1988). The fatty acid methyl ester mixtures were separated using the Sherlock Microbial Identification System (Microbial ID) which consisted of a gas chromatograph (model 5980; Agilent) fitted with a 5 % phenyl-methyl silicone column (0·2 mmx25 m) and FID detector. Identification and comparison were made using the Aerobe (TSBA50, version 5) database of the Sherlock Microbial Identification System. As shown in Table 1, the polar lipid profiles of B90A, UT26 and Sp+ were almost identical. While phosphatidylmonomethylethanolamine (PMME) and phosphatidylethanolamine (PE) were abundant in all three strains, diphosphatidylglycerol (DPG) was a major polar lipid in B90A, but not in Sp+ or UT26. The major sphingoglycolipid SGL1 was present in all the strains and SGL2 was present in small amounts. SGL1 and SGL2 correspond to SGL and GL2, respectively, of Sphingomonas paucimobilis DSM 1098T (Busse et al., 1999). Several polar lipids (PDE and PL3) reported as present in Sphingomonas paucimobilis DSM 1098T (Busse et al., 1999), Sphingomonas xenophaga DSM 6383T (Busse et al., 1999) and Sphingobium chlorophenolicum ATCC 33790T (Busse et al., 1999) were absent in B90A, UT26 and Sp+. With respect to fatty acid profiles, B90A, UT26 and Sp+ again showed minor qualitative and quantitative differences. Fatty acid 18 : 1
7c predominated, with relatively high levels of 16 : 0 and a major 2-hydroxy fatty acid 14 : 0 (Table 2), features common to most of the Sphingobium species (Takeuchi et al., 2001). Additionally, a similarity index of all the isolates produced from the Aerobe TSBA50 library showed that the three strains fell within the group represented by the genus Sphingobium. The cellular fatty acid compositions of B90A, UT26 and Sp+ were similar to those of other Sphingobium species (Takeuchi et al., 2001). Qualitative and quantitative differences in fatty acid composition between the three strains and larger qualitative and quantitative differences when they were compared with Sphingomonas paucimobilis ATCC 29837T further suggest that the three strains possibly represent three distinct species of the genus Sphingobium.
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), further distinguishing [Sphingomonas] chungbukensis IMSNU 11152T from the genus Sphingomonas. |
Phenotypic properties |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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). The morphological characteristics (colour, shape, size and contour of colonies) of B90A, UT26 and Sp+ were studied on nutrient agar, SM agar medium and LB agar plates. Growth at different temperatures and catalase tests were carried out as described by McCarthy & Cross (1984). All three strains were non-motile, Gram-negative rods (Table 3). The cell size of B90A, UT26 and Sp+ varied from 1·0 to 2·5 µm. The optimum temperature for growth was 28 °C. UT26 and Sp+ produced yellow colonies. Colonies of strain B90A were initially yellow, with later production of a dark-brown soluble pigment which diffused into the LB agar plates. The dark-brown pigment was analysed by spectrophotometry and the peak absorbance was found at 532·0 nm. The production of brownish water-soluble pigment appears to be an interesting feature and has been reported earlier for Sphingobium herbicidovorans DSM 11019T (Zipper et al., 1996), which is located at the Sphingobium chlorophenolicum ATCC 33790T branch.
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. Acid production from carbohydrates and degradation of xanthine and hypoxanthine were tested according to Gordon et al. (1974). Urease activity was detected as in Christensen (1946). The other physiological tests and methods were as described by Collins et al. (1989). To determine antibiotic sensitivity, the bacterial strains were grown in SM broth supplemented with 100 µg ampicillin ml–1, 25 µg chloramphenicol ml–1, 50 µg kanamycin ml–1, 15 µg tetracycline ml–1 and 10 µg erythromycin ml–1. A comparison was made (Table 3), wherever possible, with previously described test results for [Sphingomonas] chungbukensis IMSNU 11152T (Kim et al., 2000), Sphingobium chlorophenolicum ATCC 33790T (Nohynek et al., 1996) and Sphingomonas xenophaga DSM 6383T (Stolz et al., 2000). The degradation of HCH was studied as described previously (Kumari et al., 2002; Dogra et al., 2004). Table 3 shows that B90A, UT26 and Sp+ can be differentiated from each other on the basis of several tests. The phenotypic features of B90A, UT26 and Sp+, were more common to [Sphingomonas] chungbukensis IMSNU 11152T and Sphingobium chlorophenolicum ATCC 33790T (Table 3); the study strains, including [Sphingomonas] chungbukensis IMSNU 11152T, differed in several features from Sphingomonas species (data not shown) Based on the results described above, we conclude that the three HCH-degrading strains of Sphingomonas paucimobilis represent three novel species of the genus Sphingobium. The names Sphingobium indicum sp. nov., Sphingobium japonicum sp. nov. and Sphingobium francense sp. nov. are proposed for strains B90A, UT26 and Sp+, respectively. We also propose to transfer [Sphingomonas] chungbukensis to Sphingobium chungbukense comb. nov.
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Description of Sphingobium indicum sp. nov. |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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Gram-negative, rod-shaped, aerobic, mesophilic, non-spore-forming, non-motile bacterium. Colonies (0·2–1·0 mm in diameter) are yellow, smooth and circular. Slimy growth and produces water-soluble brown pigment on LB as well as on nutrient medium. It degrades all the isomers (alpha-, beta-, gamma- and delta-) of HCH. The degradation of alpha- and gamma-HCH is nearly 100 % (complete mineralization), but incomplete degradation of delta- and beta-HCH. Resistant to ampicillin (100 µg ml–1). Catalase-, urease- and oxidase-positive. Acid is produced from glucose, arabinose, trehalose and galactose. No acid production from sucrose, lactose, rhamnose, inositol or adonitol. The following sugars are assimilated: glucose, galactose, trehalose, arabinose, ribose, xylose and fructose. The following sugars are not assimilated: sucrose, lactose, rhamnose, erythritol, inositol, adonitol, cellobiose, mannitol, sorbitol, mannose and raffinose. No degradation of aesculin, Tween 80, xanthine, hypoxanthine or casein. No production of H2S, citrate or methyl red. Sensitive to 5 % NaCl. Contains two and three copies of the linA and linX genes, respectively. Also contains 11 copies of IS6100 and one copy of each of the linB, linC, linD and linE and linR genes. The major polar lipids are phosphatidylmonomethylethanolamine, phosphatidylethanolamine and diphosphatidylglycerol. Major fatty acids are 18 : 17c, saturated 16 : 0 and 2-hydroxy fatty acid 14 : 0 (Table 2).
The type strain, B90AT (=MTCC 6364T=CCM 7286T), was isolated from the rice rhizosphere, Cuttack, India.
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Description of Sphingobium japonicum sp. nov. |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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Gram-negative, rod-shaped, aerobic, mesophilic, non-spore-forming, non-motile bacterium. Colonies (0·2–1·0 mm in diameter) are yellow, smooth and circular. Slimy growth and does not produce pigment on LB or on nutrient medium. Utilizes alpha-, gamma- and delta-HCH as a source of carbon, but not beta-HCH. Resistant to ampicillin (100 µg ml–1), erythromycin (10 µg ml–1) and nalidixic acid. Catalase- and oxidase-positive. Acid is produced from glucose, arabinose, trehalose and galactose. The following compounds are assimilated: fructose, sucrose, galactose, cellobiose and ribose. Aesculin, Tween 20 and Tween 80 are hydrolysed. Contains one copy of each of the linA, linB, linC, linD, linR genes and five copies of IS6100. The major polar lipids are phosphatidylmonomethylethanolamine (PMME) and phosphatidylethanolamine (PE). Major fatty acids are 18 : 17c, saturated 16 : 0 and 2-hydroxy fatty acid 14 : 0.
The type strain, UT26T (=MTCC 6362T=CCM 7287T), was isolated from upland soils in Japan that had been treated repeatedly with gamma-HCH for 15 years.
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Description of Sphingobium francense sp. nov. |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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Gram-negative, rod-shaped, aerobic, mesophilic, non-spore-forming, non-motile bacterium. Degrades all isomers of HCH. Colonies (0·2–1·0 mm in diameter) are yellow, smooth and circular. Resistant to ampicillin (100 µg ml–1). Catalase- and oxidase-positive. Acid is produced from glucose, arabinose, galactose, cellobiose and ribose. Assimilates cellobiose and ribose. Aesculin and Tween 20 are hydrolysed. The major polar lipids are phosphatidylmonomethylethanolamine and phosphatidylethanolamine. Major fatty acids are 18 : 17c, saturated 16 : 0 and 2-hydroxy fatty acid 14 : 0 (Table 2). Contains one copy of each of the linA, linB, linD and linE genes, two copies of linC and six copies of IS6100.
The type strain, Sp+T (=MTCC 6363T=CCM 7288T), was isolated from gamma-HCH-contaminated soils in France.
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Description of Sphingobium chungbukense (Kim et al. 2000) comb. nov.
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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Basonym: Sphingomonas chungbukensis Kim et al. 2000.
The description is identical to the description given for Sphingomonas chungbukensis by Kim et al. (2000). The type strain is DJ77T (=KCTC 2955T=IMSNU 11152T=JCM 11454T).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTIntroduction16S rRNA gene sequencing...DNA-DNA hybridizationDNA profiling, IS6100 and...Polar lipid and fatty...Phenotypic propertiesDescription of Sphingobium...Description of Sphingobium...Description of Sphingobium...Description of Sphingobium...REFERENCES |
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