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1 DSMZ – German Collection of Microorganisms and Cell Cultures GmbH, 38124 Braunschweig, Germany
2 Department of Microbiology, Technical University Munich, 85350 Freising, Germany
3 Institute of Biotechnology, National Technical University, 8093 Zürich, Switzerland
Correspondence
Elke Lang
ela{at}dsmz.de
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). Metabolism of dibenzofuran by these bacteria is initiated by angular dioxygenation of the compound (Engesser et al., 1989). Three distinct extradiol dioxygenases are involved in further degradation of the resulting metabolite 2,2',3-trihydroxybiphenyl (Schmid et al., 1997). In 1989, one of the dibenzofuran-degrading strains, DPO 1361, was assigned to the genus Brevibacterium on the basis of its cell-wall composition and biochemical properties (Strubel et al., 1989). Based on the results of 16S rDNA analysis and DNA–DNA hybridization, Schmid et al. (1997) proposed that strains DPO 360 and DPO 1361 were representatives of the same novel species within the genus Terrabacter. In the same year, Terrabacter (Collins et al., 1989) was grouped with the genus Intrasporangium (Kalakoutskii et al., 1967) in the novel family Intrasporangiaceae (Stackebrandt et al., 1997). Three novel genera were described within the family: Janibacter, with the sole species Janibacter limosus (Martin et al., 1997), Terracoccus (Prauser et al., 1997) and Tetrasphaera (Maszenan et al., 2000). Knoellia (Groth et al., 2002) is a genus that is very close to the family Intrasporangiaceae. A soil isolate and two trichloroethylene-degrading strains isolated from groundwater were described, respectively, as the novel Janibacter species Janibacter terrae (Yoon et al., 2000) and Janibacter brevis (Imamura et al., 2000). These recent developments in the taxonomy of bacteria closely related to [Terrabacter sp.] DPO 360 and DPO 1361 led us to reinvestigate the taxonomic position of the dibenzofuran-degrading isolates. Eight other dibenzofuran-degrading strains were included in the study. The 16S RNA gene sequences of the strains showed highest similarity to those of J. terrae and J. brevis. Reassessment of the J. terrae and J. brevis sequences suggested that J. brevis may be a synonym of J. terrae.
Isolation sources and geographical areas of the dibenzofuran-degrading strains are shown in Table 1. Strains were isolated by enrichment cultures with dibenzofuran as the sole source of carbon and energy in the laboratory of K.-H. Engesser, University of Stuttgart. Type strains were obtained from the DSMZ (Deutsche Sammlung von Mikroorganismen und Zellkulturen). For morphological and physiological characterizations, standard methods were used. The API 50CH galleries (bioMérieux) were inoculated with AUX medium for testing utilization of substrates, and with CHB medium (both media by bioMérieux) for testing acid production from carbohydrates. API 20NE galleries (bioMérieux) were read after 1 and 3 days and API 50CH after 1, 2, 3, 6 and 14 days incubation at 28 °C. Results were scored as positive when turbidity was visible after 6 days at the latest and was confirmed after 14 days. Utilization of carbon sources was tested in a mineral medium (Stanier et al., 1966) with 2 g l-1 of the respective carbon source. Cultures were read after incubation for up to 28 days.
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and separated by HPLC (Kroppenstedt, 1985). Polar lipids were extracted, examined by two-dimensional TLC and identified according to procedures described by Minnikin et al. (1984). For analysis of fatty acids, cells were grown on tryptic soy broth agar (TSBA) for 24 h. Fatty acid methyl esters were obtained from 40 mg (wet wt) cells by saponification, methylation and extraction, as described previously (Kämpfer & Kroppenstedt, 1996) and separated by a model 5898A gas chromatograph (Hewlett Packard). Peaks were integrated automatically and fatty acid names and percentages were determined by using the Microbial Identification standard software package (Sasser, 1990). Preparation of cell walls and determination of peptidoglycan structure were carried out by using methods described by Schleifer & Kandler (1972), with the modification that TLC on cellulose sheets was used instead of paper chromatography. Riboprinting was done by the RiboPrinter Microbial Characterization system (Qualicon) according to the manufacturer's instructions, after cleavage with endonuclease PvuII.
DNA base composition was determined by HPLC. DNA was isolated after cell disruption with a French pressure cell and purified on hydroxyapatite, according to Cashion et al. (1977). P1 hydrolysis and nucleotide dephosphorylization with alkaline phophatase were done as described by Mesbah et al. (1989). HPLC conditions (LKB equipment with Shimadzu CR-3A integrator) on a Nucleosil 100-5C18 column were chosen according to Tamaoka & Komagata (1984). DNA–DNA hybridization was carried out at 66 °C as described by De Ley et al. (1970) with the modifications described by Huss et al. (1983), by using a GILFORD system model 2600 spectrophotometer equipped with a GILFORD model 2527-R thermoprogrammer and plotter. Renaturation rates were computed with the TRANSFER.BAS program (Jahnke, 1992). After amplification of the 16S rDNA of DSM 13876T, purified PCR products were sequenced and electrophoresed and the sequences were aligned as decribed previously (Rainey et al., 1996). The following 16S rDNA sequences were used for alignments (Rainey et al., 1996; Schmid et al., 1997): strain [Terrabacter sp.] DPO 1361 (Y08853), J. brevis IAM 14781T (AB016438), J. terrae KCCM 80001T (AF176948) and J. limosus DSM 11140T (Y08539).
All ten dibenzofuran-degrading strains formed one cluster with high similarities in their physiology and chemotaxonomically relevant cell components. On TSBA, the DPO strains formed opaque, yellow-whitish colonies with entire edges. Colony diameter varied between 0·1 and 0·4 mm after 3 days and between 0·6 and 1 mm after 6 days incubation at 28 °C. Cells were Gram-positive, non-motile, non-spore-forming cocci or rods. Cells of strain DPO 360 were irregular cocci of 0·6–1·4 µm that occurred singly or in pairs. Cells of strain DPO 1361 were egg-shaped rods of 0·7–0·8x1·4–2·3 µm. The strains grew aerobically at 28 and 35 °C. Growth at 37 °C on TSBA was poorer than at lower temperatures. Physiological properties, as determined in API 20NE and 50CH galleries, were highly similar for all ten strains. The strains reduced nitrate to nitrite, hydrolysed gelatin and utilized malate, fructose and turanose. Oxidase reaction of young cultures was negative and of 3-day-old cultures was delayed and weak. Inositol and sucrose (with one exception) and gluconate and trehalose (with two exceptions) were used. Variable results were achieved for the utilization of glucose, N-acetylglucosamine, maltose and adipate. All other tests in the API galleries were negative. No acid was produced from carbohydrates in the API 50CH system. The Biolog carbon source utilization test system was not applicable to the strains, as they gave a relatively strong reaction without a carbon source (reference vial). Physiological properties of strains DPO 360 and DPO 1361, which were selected as reference strains, and of J. brevis DSM 13953T, J. terrae DSM 13876T and J. limosus strains are shown in Table 2.
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). The fatty acid pattern of the Janibacter strains tested was composed of the same main components, with the exception that J. limosus DSM 11140T contained 15 % heptadecanoic acid as one main component. The type strain of Terrabacter tumescens differed in having only 3 % 14-methylpentadecanoic acid and high proportions (14 %) of hexadecanoic acid and cis 9-hexadecenoic acid (data not shown).
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m-Dpm-direct. On the molecular side, unity of the DPO strains was confirmed by RiboPrinter patterns. All DPO strains and J. brevis DSM 13953T showed two main fragments with molecular masses of about 7·5 and 10·5 kbp after cleavage with PvuII. The patterns of J. terrae DSM 13876T and J. limosus DSM 11140T were also dominated by two fragments that, however, had different molecular masses.
The 16S rDNA sequence of DPO 1361 was>99 % similar to the deposited sequences of J. brevis IAM 14781T and J. terrae KCCM 80001T. The deposited sequences of J. brevis IAM 14781T and J. terrae KCCM 80001T showed 99·8 % similarity to each other. Resequencing of the 16S rDNA of the type strain of J. brevis (AJ310085) gave a sequence that was 99·9 % similar to those of J. terrae and strain DPO 1361.
DNA–DNA reassociation of the type strains of J. brevis and J. terrae resulted in 80·6 % relatedness. Strain DPO 360 showed 82, 94·5, 78·9 and 86·2 % relatedness to DPO 1361, DPO 400, J. brevis DSM 13953T and J. terrae DSM 13876T, respectively. DNA–DNA relatedness between DPO 360 and J. limosus DSM 11140T and DSM 11141 was 14·7 and 5·4 %, respectively. The DNA G+C content of strain DPO 360 was 72·8 mol%.
Whole-cell fatty acid analysis and riboprinting, together with Gram-staining, cell morphology and biochemical properties, revealed that all dibenzofuran-degrading strains belonged to one cluster. When fatty acid data were compared by Ward's method, fatty acid composition of the DPO strains was more similar within the group than to those of other bacteria included in this study or registered in the MIDI database. DPO 210 and DPO 360 showed the most atypical fatty acid patterns within the group; the fatty acid patterns of the DPO strains were most similar to those of J. brevis DSM 13953T, J. terrae DSM 13876T, J. limosus DSM 11141, Nocardioides jensenii DSM 20641T and Nocardioides simplex DSM 20130T. Iso-hexadecanoic acid was the predominant fatty acid in these strains. The fatty acid pattern of the type strain of J. limosus was less similar, with a Euclidian distance of more than 30 units to the DPO cluster, and was dominated by straight-chain unsaturated acids. The group of J. brevis, J. terrae and DPO strains may be differentiated from J. limosus by the presence of iso-cis 8-heptadecenoic and anteiso-heptadecanoic acids, which are absent in J. limosus.
Like the fatty acid patterns, the carbohydrate pattern showed high homogeneity within the DPO group and between the DPO group and the type strains of J. brevis, J. terrae and J. limosus. All utilized a limited range of the carbohydrates tested (Table 2
). Forty substrates (mostly carbohydrates) that are not mentioned in Table 2 were tested in the API 50 CH and API 20NE galleries and gave no growth. Only fructose, turanose and inositol were metabolized by all strains. Additionally, almost all strains utilized gluconate and sucrose (with the exception of J. limosus DSM 11141) and trehalose (with the exception of strain DPO 360) (Table 2). Of the carbon acids and amines additionally tested, benzoate, DL-malate, L-glutamine, L-histidine and L-proline were utilized (Table 2). Strains of the DPO–J. brevis–J. terrae cluster may be differentiated from J. limosus by their ability to grow at 37 °C on TSBA and to hydrolyse gelatin.
RiboPrinter patterns are generally species-specific and, in some cases, specific even to the subspecies level. Therefore, the patterns can be used for identification at the species level and, for some taxa, for clustering of strains that belong to the same species. RiboPrinter patterns of the DPO strains homogeneously showed the same two main bands (Fig. 1). The pattern of J. brevis DSM 13953T also showed the same main fragments. Only the patterns of DSM 11219 and J. brevis DSM 13953T displayed minor differences when compared to the patterns of the other strains. Nevertheless, the RiboPrints of the strains mentioned were highly similar (similarity>0·90, as computed by the RiboPrinter system) and belonged to one cluster. The patterns of J. terrae DSM 13876T and J. limosus DSM 11140T corresponded to the patterns of the DPO cluster in being dominated by only two fragments. One band of the DSM 13876T pattern corresponded to the DPO pattern, but its second fragment was shifted towards a lower molecular mass. Neither of the bands of J. limosus DSM 11140T corresponded to those of the DPO cluster. The RiboPrinter data suggest that the DPO strains and J. brevis DSM 13953T form a homogeneous cluster. As physiological tests, 16S rDNA sequence analysis and DNA–DNA similarity data (see below) support the affiliation of the DPO strains and the type strains of J. brevis and J. terrae to the same species, the difference of one band in the RiboPrinter pattern of strain J. terrae DSM 13876T should be considered as a strain-specific feature.
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, as their 16S rDNA sequences were most related (95·9 %) to the sequence of T. tumescens at that time. Because of their DNA–DNA reassociation results, the authors stated that the two strains belonged to one novel species that was different from T. tumescens. It is only since then that the genus Janibacter (Martin et al., 1997) and the family Intrasporangiaceae (Stackebrandt et al., 1997) have been described. Sanguibacter (Fernández-Garayzábal et al., 1995) and Ornithinicoccus (Groth et al., 1999) are related closely to the family Intrasporangiaceae, but now are reclassified as a family on its own or as a genus separate from the Intrasporangiaceae, respectively (Stackebrandt & Schumann, 2000). The results of our polyphasic approach consistently suggest that the DPO strains belong to the genus Janibacter and are indistinguishable from the species J. brevis and J. terrae. These two species and the DPO strains showed the same biochemical and chemotaxonomic features [directly cross-linked meso-diaminopimelic acid as the peptidoglycan type, diphosphatidylglycerol, phosphatidylglycerol and phosphatidylinositol as polar lipids and menaquinone MK-8(H4)]. Correspondence of chemotaxonomic and biochemical data was confirmed by the high similarity of 16S rDNA sequences and DNA–DNA reassociation values>78 % between DPO 360, DPO 1361 and the type strains of J. terrae and J. brevis.
The species J. brevis and J. terrae were described at the same time by different working groups (Imamura et al., 2000; Yoon et al., 2000). Both were isolated from environmental samples. Our hybridization of the DPO strains and the type strains of the two species revealed>78 % relatedness to each of them. This prompted us to hybridize the DNA of the type strains of J. brevis DSM 13953T and J. terrae DSM 13876T. These two were also about 80 % similar. After resequencing the 16S rDNA of J. terrae DSM 13876T, the 16S rDNA sequence similarity between J. brevis IAM 14781T and J. terrae DSM 13876T was 99·9 %. Therefore, we suggest that J. brevis and J. terrae are synonyms for one species. The effective description of J. terrae was published on pp. 1821–1827 of volume 50 of the International Journal of Systematic and Evolutionary Microbiology, whereas J. brevis was published on pp. 1899–1904 of the same volume (Imamura et al., 2000; Yoon et al., 2000). According to Rule 24b of the International Code of Nomenclature of Bacteria, the name J. terrae has priority and J. brevis should be recognized as the later synonym of the species.
Emended description of Janibacter terrae Yoon, Lee, Kang, Kho, Kang and Park 2000 (syn. Janibacter brevis Imamura, Ikeda, Yoshida and Kuraishi 2000)
Cells are Gram-positive, non-motile, non-spore-forming cocci or short rods that occur singly, in short chains or in clumps. Colonies on complex media are white, cream or yellowish, opaque, glistening and convex with entire margins. Optimal growth temperature is 25–30 °C. Maximum growth temperature on solid TSBA medium is 37 °C and in liquid R medium is 40 °C. Young cultures are oxidase-negative; a weakly positive reaction may occur with older cultures or on special media. Catalase-positive. Decomposes casein, gelatin and starch. H2S may be produced from cysteine. Grows in brain heart infusion in the presence of 10 % NaCl. Reduces nitrate to nitrite. Negative results for indole production from tryptophan, acetoin production, arginine dihydrolase, urease, 
-galactosidase and decomposition of Tween 80 and aesculin. No acid is produced from glucose or other carbohydrates. Variable results with glucose, mannose, maltose, N-acetylglucosamine, benzoate, acetate, adipate and putrescine as substrate. Most or all strains utilize fructose, turanose, sucrose, trehalose, inositol, malate and gluconate. Chemotaxonomic characteristics are as described by Yoon et al. (2000) and Imamura et al. (2000). DNA G+C content is 69·0–72·8 mol%.
The type strain is CS12T (=KCCM 80001T=JCM 10705T=DSM 13876T). All strains are isolated from environmental samples such as soil and water. Many strains are able to degrade environmental pollutants.
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ACKNOWLEDGEMENTS |
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REFERENCES |
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TOPABSTRACTMAIN TEXTREFERENCES |
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