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1 Department of Biological Sciences, Korea Advanced Institute of Science and Technology, 373-1, Guseong-dong, Yuseong-gu, Daejeon 305-701, Korea
2 Department of Biological Sciences, 331 Life Sciences Building, LSU, Baton Rouge, LA 70803, USA
3 Institute of Molecular and Cellular Biosciences, University of Tokyo, 1-1, Yayoi 1-chome, Bunkyo-ku, Tokyo, 113-0032, Japan
Correspondence
Sung Taik Lee
e_stlee{at}kaist.ac.kr
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession number for the 16S rDNA sequence of strain CPW301T (=KCTC 12096T=IAM 15024T) is AB094401.
A phylogenetic tree and DNA–DNA relatedness data are available as supplementary material in IJSEM Online.
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TOPABSTRACTMAIN TEXTREFERENCES |
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). Later, a mild plant pathogen, formerly named Pseudomonas rubrisubalbicans, was reclassified as H. rubrisubalbicans LMG 2286T (=IAM 14976T) (Baldani et al., 1996). Kirchhof et al. (2001) identified a nitrogen-fixing bacterium, isolated from C4-fibre plants, as H. frisingense GSF30T (=IAM 14974T). More recently, H. lusitanum LMG 21710T was isolated from root nodules of Phaseolus vulgaris plants and proposed as a novel species by Valverde et al. (2003). Although the unnamed Herbaspirillum species 3 (Baldani et al., 1996) did not fix nitrogen, all type strains of species with validly published names have been recognized as nitrogen-fixing micro-organisms.
Chlorophenols are common environmental pollutants that arise from extensive use of wood preservatives, herbicides and fungicides and they are found frequently in pulp-bleaching effluents and industrial wastewater (Kringstad & Lindström, 1984; Valo et al., 1984, 1985). Due to the environmentally hazardous properties of chlorophenols, intensive attention has been paid to processes of microbial chlorophenol degradation. Many micro-organisms have been reported to degrade chlorophenols as their sole carbon and energy source, including a Pseudomonas species (Knackmuss & Hellwig, 1978; Radehaus & Schmidt, 1992), Arthrobacter species (Stanlake & Finn, 1982; Li et al., 1991), Rhodococcus chlorophenolicus (Apajalahti et al., 1986) and some Flavobacterium strains (Saber & Crawford, 1985). In our laboratory, Bae et al. (1996) previously reported a 4-chlorophenol-degrading bacterium, strain CPW301T, that was isolated from soil sediment collected in a stream near an industrial region in Cheongju, Korea, via selective enrichment with 4-chlorophenol as the sole carbon and energy source. It was identified tentatively as a strain of Comamonas testosteroni on the basis of its morphological and physiological characteristics. In the present study, phylogenetic analysis on the basis of 16S rDNA sequences was performed and DNA–DNA relatedness and some important phenotypic characteristics were examined to determine the precise taxonomic position of this strain. On the basis of the results obtained in this study, it is proposed that strain CPW301T should be placed in the genus Herbaspirillum as the type strain of a novel species, namely Herbaspirillum chlorophenolicum sp. nov.
Strain CPW301T was originally isolated from soil sediment that was collected in a stream near an industrial region (Cheongju, Korea) (Bae et al., 1996) and deposited in the Korean Collection for Type Cultures as KCTC 12096T (=IAM 15024T). H. seropedicae IAM 14977T, H. rubrisubalbicans IAM 14976T and H. frisingense IAM 14974T were obtained from the IAM Culture Collection, Institute of Molecular and Cellular Bioresources, University of Tokyo, Tokyo, Japan. Flagellation and morphological characteristics were determined by transmission electron microscopy after staining cells negatively with 1 % (w/v) phosphotungstic acid. Gram-staining and catalase and oxidase tests were performed according to procedures outlined by Smibert & Krieg (1981). Substrate utilization and some physiological characteristics were determined with API 20 NE, ID 32 GN and API 50 CHB kits (bioMérieux).
Phenol- and 4-chlorophenol-degradation ability was assessed in a 500 ml Erlenmeyer flask that contained 50 ml mineral salts medium (Bae et al., 1996) with 0·5 mM phenol or 0·5 mM 4-chlorophenol as the sole carbon source in a shaking incubator at 30 °C. Nitrogen-fixing ability was determined by growth in 50 ml nitrogen-free medium (DSMZ medium no. 3) in a 500 ml Erlenmeyer flask. The medium contained [(l distilled water)–1]: 5·0 g glucose; 5·0 g mannitol; 0·1 g CaCl2.2H2O; 0·1 g MgSO4.7H2O; 5·0 mg Na2MoO4.2H2O; 0·9 g K2HPO4; 0·1 g KH2PO4; 0·01 g FeSO4.7H2O; 5·0 g CaCO3; and 1 ml trace element mixture. The trace element mixture (SL-6, DSMZ medium no. 27) contained [(l distilled water)–1]: 0·1 g ZnSO4.7H2O; 0·03 g MnCl2.4H2O; 0·3 g H3BO3; 0·2 g CoCl2.6H2O; 0·01 g CuCl2.2H2O; and 0·02 g NiCl2.6H2O. Growth was determined after 2 weeks at 30 °C in a shaking incubator.
Ubiquinones were extracted from cells that had been grown on nutrient broth (Difco) and were analysed as described by Komagata & Suzuki (1987), using reverse-phase HPLC. Cellular fatty acids were analysed in strains CPW301T, H. frisingense IAM 14974T, H. rubrisubalbicans IAM 14976T and H. seropedicae IAM 14977T, grown on trypticase soy agar (Difco) for 1–2 days. Cellular fatty acids were saponified, methylated and extracted according to the protocol of the Sherlock Microbial Identification system (MIDI). Fatty acids were analysed by GC (Hewlett Packard 6890) and identified by the Microbial Identification software package (Sasser, 1990).
Chromosomal DNA was extracted from cells that had been grown on a nutrient agar plate (Difco) as described by Ausubel et al. (1995). RNA in the DNA solution was removed by incubation with a mixture of ribonucleases A and T1 (each at 20 U ml–1) at 30 °C for 1 h. Chromosomal DNA G+C content was analysed as described by Mesbah et al. (1989), using reverse-phase HPLC. DNA–DNA relatedness was determined as described by Ezaki et al. (1989), using photobiotin-labelled DNA probes and micro-dilution wells.
Two pairs of primer systems, Fdb261–Fdb260 (Stoltzfus et al., 1997) and PolF–PolR (Poly et al., 2001), were used to amplify the nifD and nifH genes, respectively. PCR was run for 35 cycles with a DNA thermal cycler (model 2400; Perkin-Elmer). The following thermal profiles were used for PCR: denaturation at 94 °C for 45 s, primer annealing at 50 °C for 45 s and extension at 72 °C for 45 s. The final cycle included an extension for 7 min. PCR products were separated by electrophoresis on an agarose gel (0·8 %, w/v) and stained with ethidium bromide. Band size was determined by comparison with a 100 bp ladder standard (Bio-Rad).
16S rDNA was amplified from chromosomal DNA of strain CPW301T by using a universal eubacterial primer set, 9F [5'-GAGTTTGATCCTGGCTCAG-3'; positions 9–27 (Escherichia coli 16S rDNA numbering)] and 1512R [5'-ACGG(H)TACCTTGTTACGACTT-3'; positions 1512–1492] (Weisburg et al., 1991). The PCR product, purified with a GFX PCR DNA and Gel Band Purification kit (Amersham Biosciences), was sequenced with an ABI Prism BigDye Terminator Cycle Sequencing Ready Reaction kit (Applied Biosystems) and an automatic DNA sequencer (model 310; Applied Biosystems). Primers used for full sequencing were 9F, 1512R, 341F [5'-CCTACGGGAGGCAGCAG-3'; positions 341–357 (E. coli 16S rDNA numbering)], 519F [5'-CAGCAGCCGCGGTAATAC-3'; positions 519–536], 907F [5'-AAACTCAAAKGAATTGACGG-3'; positions 907–926], 536R [5'-GTATTACCGCGGCTGCTG-3'; positions 536–519] and 1100R [5'-GGGTTGCGCTCGTTG-3'; positions 1114–1110]. The partial 16S rDNA sequences were combined in the program BioEdit (Hall, 1999). 16S rDNA sequences of related taxa were obtained from GenBank. Multiple alignments were performed by using CLUSTAL_X (Thompson et al., 1997). Gaps were edited in BioEdit (Hall, 1999). Evolutionary distances were calculated by using the Kimura two-parameter model (Kimura, 1983). A phylogenetic tree was constructed by using the neighbour-joining method (Saitou & Nei, 1987) in the program MEGA2 (Kumar et al., 2001). A neighbour-joining bootstrap method was used to obtain confidence levels for the neighbour-joining analysis, with a bootstrap dataset of 1000 (Felsenstein, 1985).
Strain CPW301T is an aerobic, Gram-negative, motile and slightly curved rod (0·7 µm in diameter and 2·3 µm long) with one unipolar flagellum. Colonies that form on nutrient agar plates (Difco) are smooth, circular, non-glossy, brownish and convex. The strain gave positive results for catalase, oxidase and urease. Nitrate was not reduced to nitrite. The strain grew well at 30 °C and pH 6–8, but did not grow well at 45 °C. These morphological and physiological characteristics are summarized in Table 1, along with data for Herbaspirillum species with validly published names. nifD and nifH are genes that encode key enzymes in nitrogen-fixing pathways in various micro-organisms (Yong, 1992). An attempt was made to detect these genes in strain CPW301T by a PCR amplification approach using two primer systems [Fdb261–Fdb260 for nifD (Stoltzfus et al., 1997) and PolF–PolR for nifH (Poly et al., 2001)], in order to determine whether the strain has the genetic capability to fix nitrogen. These genes, nifD (about 390 bp) and nifH (about 360 bp), were clearly amplified in nitrogen-fixing type strains, whereas they were not amplified in strain CPW301T (Table 1). Strain CPW301T did not grow in a nitrogen-free liquid medium, whereas Herbaspirillum species with validly published names grew well (Table 1).
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7c (13·4 %). Although the proportions are slightly different, these fatty acids are also observed in the type strains of Herbaspirillum species (Table 1
). The DNA G+C content of strain CPW301T was 61·3 mol%; this value is similar to those of the type strains of Herbaspirillum species (60–65 %). Almost all of the 16S rDNA sequence (1474 nt) of strain CPW301T was determined in this study. Phylogenetic analysis of 16S rDNA sequences showed that strain CPW301T fell in a cluster that comprised Herbaspirillum species (a phylogenetic tree is available as supplementary material in IJSEM Online). The 16S rDNA sequence similarities of strain CPW301T to H. frisingense IAM 14974T, H. rubrisubalbicans IAM 14976T, H. seropedicae IAM 14977T and H. lusitanum LMG 21710T are 98·9, 98·7, 98·8 and 97·5 %, respectively. Strain CPW301T exhibited DNA–DNA relatedness levels of <15·7 % to H. frisingense IAM 14974T, H. rubrisubalbicans IAM 14976T and H. seropedicae IAM 14977T (hybridization data are available as supplementary material in IJSEM Online).
Phylogenetic analysis based on 16S rDNA sequences indicates clearly that strain CPW301T is placed in the radiation of the cluster that contains Herbaspirillum species. The names of three species of Herbaspirillum, H. seropedicae (Baldani et al., 1986), H. rubrisubalbicans (Baldani et al., 1996) and H. frisingense (Kirchhof et al., 2001), have been validly published and another species (H. lusitanum) has recently been proposed as a member of the genus Herbaspirillum by Valverde et al. (2003). Strain CPW301T has similar morphological features to the type strains of these species and it also shares many physiological characteristics with them (Table 1). Furthermore, chemotaxonomic characteristics of CPW301T determined in this study, e.g. ubiquinone, fatty acids and DNA G+C content, are well-matched to those of other Herbaspirillum species (Table 1). The phylogenetic, phenotypic and chemotaxonomic results described in this study support classification of strain CPW301T in the genus Herbaspirillum.
It is worthwhile to compare the phenotypic characteristics of strain CPW301T with those of the type strain of C. testosteroni, as our strain was originally classified in this species (Bae et al., 1996). Our strain differs from C. testosteroni in meso-inositol and glycerol utilization and fatty acid profile (Table 1). Thus, in addition to phylogenetic data, phenotypic characteristics support reclassification of strain CPW301T in the genus Herbaspirillum.
Strain CPW301T showed 98·7–98·9 % 16S rDNA similarity to the type strains of Herbaspirillum species. Where 16S rDNA sequence similarity is >97 %, DNA–DNA relatedness values play an important role in clarifying intergeneric relationships between species (Stackebrandt & Goebel, 1994). Strain CPW301T exhibited <15·7 % DNA–DNA relatedness to species of Herbaspirillum with validly published names. This level is low enough for strain CPW301T to be classified in a novel Herbaspirillum species (Wayne et al., 1987). Furthermore, strain CPW301T can also be distinguished from Herbaspirillum species with validly published names with respect to some important physiological characteristics. For example, all the type strains of described Herbaspirillum species are nitrogen-fixing organisms (Baldani et al., 1986, 1996; Kirchhof et al., 2001), whereas strain CPW301T did not grow in a nitrogen-free liquid medium and did not have the nifD or nifH genes, suggesting that it may not have a nitrogen-fixing ability. Substrate-utilization properties (Table 1) also differ between strain CPW301T and the type strains of Herbaspirillum species. On the basis of the data and observations described above, strain CPW301T should be assigned to the genus Herbaspirillum as the type strain of a novel species, for which the name Herbaspirillum chlorophenolicum sp. nov. is proposed.
Description of Herbaspirillum chlorophenolicum sp. nov.
Herbaspirillum chlorophenolicum (chlo.ro.phen.o'li.cum. Gr. n. adj. chloros greenish-yellow, containing chloride; N.L. adj. phenolicus relating to phenol; N.L. neut. adj. chlorophenolicum relating to chlorophenols).
Gram-negative, aerobic, motile, slightly curved rods, 0·7 µm in diameter and 2·3 µm long, after culture for 1 day on nutrient agar. Cells have one unipolar flagellum. Colonies grown on nutrient agar (Difco) for 1–2 days are smooth, circular, non-glossy, brownish and convex. Grows well at 30 °C and pH 6–8, but does not grow at 45 °C. Substrate utilization, enzyme production, acid production and other physiological characteristics are indicated in Table 1. Does not have nifD or nifH genes. Q-8 is the predominant ubiquinone. C16 : 0 and cyclo-C17 : 0 are the major cellular fatty acids. DNA G+C content of the type strain is 61·3 mol% (as determined by HPLC).
The type strain, CPW301T (=KCTC 12096T=IAM 15024T), was isolated from soil sediment that was collected at a stream near an industrial region in Cheongju, Korea.
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ACKNOWLEDGEMENTS |
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