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Microbacterium oleivorans sp. nov. and Microbacterium hydrocarbonoxydans sp. nov., novel crude-oil-degrading Gram-positive bacteria

¹ Referat Geomikrobiologie, Bundesanstalt für Geowissenschaften und Rohstoffe, Stilleweg 2, D-30655 Hannover, Germany
² Deutsche Sammlung von Mikroorganismen und Zellkulturen, Mascheroder Weg 1b, D-38124 Braunschweig, Germany

Correspondence
Axel Schippers
A.Schippers{at}bgr.de

	ABSTRACT

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A taxonomic study of two crude-oil-degrading, Gram-positive bacterial strains, designated BAS69^T and BNP48^T, revealed that they represent two novel Microbacterium species. 16S rRNA gene sequence similarity to their closest phylogenetic neighbours was 98·5 % for BAS69^T (Microbacterium paraoxydans DSM 15019^T and Microbacterium saperdae DSM 20169^T) and 99 % for BNP48^T (Microbacterium luteolum DSM 20143^T). Levels of DNA–DNA relatedness to the closest phylogenetic neighbours of both strains were between 11 and 38 %. According to phylogenetic analysis, the two strains are distinguishable from all recognized species of Microbacterium. Morphological and physiological characteristics of strains BAS69^T and BNP48^T were different from those of phylogenetically closely related Microbacterium species. The diamino acid in the cell-wall peptidoglycan of BAS69^T is lysine and of BNP48^T is ornithine. The major menaquinones are MK-11 and MK-12 for both strains. Based on their ability to degrade crude oil, the name Microbacterium oleivorans sp. nov. is proposed for strain BAS69^T (=DSM 16091^T=NCIMB 14003^T) and Microbacterium hydrocarbonoxydans is proposed for strain BNP48^T (=DSM 16089^T=NCIMB 14002^T).

	MAIN TEXT

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Crude oil consists of various hydrocarbons, which can be degraded by micro-organisms, and several hydrocarbon-oxidizing bacterial genera have been described (Jobson et al., 1972; Bosecker et al., 1991; Rueter et al., 1994; Zengler et al., 1999; Rosenberg, 2000; Van Hamme et al., 2003). Here we describe the classification of two crude-oil-degrading, Gram-positive bacteria that showed characteristics of members of the genus Microbacterium. The genus Microbacterium comprises more than 30 physiologically versatile species isolated from various environments (Yokota et al., 1993; Takeuchi & Hatano, 1998a, b; Collins & Bradbury, 1999; Schumann et al., 1999; Behrendt et al., 2001; Zlamala et al., 2002; Laffineur et al., 2003).

The two strains were isolated from different oil-containing environments. Strain BAS69^T was isolated from oil storage cavern 126 near Etzel, Germany (Bock et al., 1994). Strain BNP48^T was isolated from an oil-contaminated soil in Germany. For enrichment, medium supplemented with 1–5 % crude oil as carbon source in Erlenmeyer flasks was inoculated and incubated on a rotary shaker at 30 °C in the dark for several weeks. For growth of strain BAS69^T, we prepared an artificial sea water medium (Fedorak & Westlake, 1981) consisting of (l^–1) 23·4 g NaCl, 0·75 g KCl, 7·0 g MgSO₄.7H₂O, 1·0 g NH₄NO₃, 0·7 g K₂HPO₄ and 0·3 g KH₂PO₄ (pH 7·3), and for strain BNP48^T we used a salt-poor medium (BNP; modified from Jobson et al., 1972) consisting of (l^–1) 2·0 g Na₂SO₄, 0·2 g MgSO₄.7H₂O, 2·0 g KNO₃, 1·0 g NH₄Cl, 0·5 g K₂HPO₄ and traces of FeSO₄ (pH 7·3). For isolation via subculturing on agar plates different media without oil were used. Strain BAS69^T was isolated on a basal medium (BAS) consisting of (l^–1) 23·4 g NaCl, 0·75 g KCl, 7·0 g MgSO₄.7H₂O, 0·5 g peptone from meat, 0·5 g peptone from casein, 1·0 g yeast extract and 18 g agar (pH 7·3). Strain BNP48^T was isolated on a modified BNP medium consisting of (l^–1) 2·0 g Na₂SO₄, 0·2 g MgSO₄.7H₂O, 2·0 g KNO₃, 1·0 g NH₄Cl, 0·5 g K₂HPO₄, traces of FeSO₄, 1·5 g sodium lactate, 1·0 g yeast extract and 18 g agar (pH 7·3).

Cell morphology, cell motility and the occurrence of spores were examined by phase-contrast light microscopy. Gram-staining and catalase testing was performed according to Burghardt (1992) and Gerhardt et al. (1994). Anaerobic growth was investigated by incubation in the presence and absence of oxygen using the Anaerocult system (Merck). Further physiological tests were carried out as described by Kämpfer et al. (1991). Briefly, use of various carbon sources as the only substrate and hydrolysis of various compounds were studied using a complex medium containing trace elements and vitamins in microplates. To confirm oil degradation, 40 ml medium (modified from Kämpfer et al., 1991) in 100 ml Erlenmeyer flasks was supplemented with 1 ml crude oil as the only carbon source, inoculated and incubated on a rotary shaker (120 r.p.m.) at 25 °C. Cell growth was checked after 3 weeks. The modified medium (pH 7·0) comprised (l^–1): 1·0 g NaCl, 0·1 g MgSO₄.7H₂O, 1·0 g (NH₄)₂SO₄, 3·2 g K₂HPO₄, 6·18 g Na₂HPO₄.2H₂O, 0·17 g CaSO₄.2H₂O, 0·001 g H₃BO₃, 0·002 g CuSO₄.5H₂O, 0·003 g ZnI₂.8H₂O, 0·2 g FeSO₄.7H₂O, 0·002 g NiCl₂.6H₂O, 0·004 g CoCl₂.6H₂O, 0·01 g MnCl₂.5H₂O, 0·003 g Na₂MoO₄.2H₂O, 0·5 g EDTA dihydrate and vitamins according to Kämpfer et al. (1991).

The occurrence of diaminopimelic acid in the cell wall and the peptidoglycan type were determined as described by Schleifer (1985) and Schleifer & Kandler (1972), using plates of cellulose for TLC. Menaquinones were extracted as described by Collins et al. (1977) and were analysed by HPLC according to the method of Groth et al. (1996). The acyl type of the peptidoglycan was determined as described by Uchida et al. (1999).

Genomic DNA extraction, PCR-mediated amplification of the 16S rRNA gene and purification of PCR products were carried out as described by Rainey et al. (1996). Purified PCR products were sequenced with Taq Dyedeoxy terminator cycle sequencing kits (Applied Biosystems) according to the manufacturer's protocol. An Applied Biosystems 373A DNA sequencer was used for electrophoresis of the sequence reaction products. The ae2 editor (Maidak et al., 1999) was used to align the 16S rRNA gene sequences determined here against those of representatives of the main bacterial lineages available from the public databases. Pairwise evolutionary distances were computed using the correction of Jukes & Cantor (1969). The least-squares distance method of De Soete (1983) contained in the PHYLIP package (Felsenstein, 1993) was used in the construction of the phylogenetic dendrogram from distance matrices.

For DNA–DNA reassociation experiments, DNA was isolated using a French pressure cell (Thermo Spectronic) followed by purification by chromatography on hydroxyapatite as described by Cashion et al. (1977). DNA–DNA hybridization was carried out by the method described by De Ley et al. (1970), with the modifications described by Huß et al. (1983) and Escara & Hutton (1980), using a model 2600 spectrophotometer equipped with a model 2527-R thermoprogrammer and plotter (Gilford). Renaturation rates were computed with the TRANSFER.BAS program (Jahnke, 1992).

The almost complete 16S rRNA gene sequences of strains BAS69^T and BNP48^T, consisting of 1490 and 1495 nt, respectively, were compared to sequences of members of the genus Microbacterium, which were their closest phylogenetic neighbours (Fig. 1).

View larger version (48K): [in this window] [in a new window]   Fig. 1. Phylogenetic dendrogram based on 16S rRNA gene sequence analysis showing the phylogenetic position of Microbacterium oleivorans sp. nov. BAS69T and Microbacterium hydrocarbonoxydans sp. nov. BNP48T compared to closely related recognized species of the genus Microbacterium. The sequences of Curtobacterium luteum DSM 20542T and Clavibacter michiganensis subsp. michiganensis DSM 46364T served as external references. Bar, 3 nucleotide substitutions per 100 nucleotides.

For strain BNP48^T, maximum pairwise similarity values of 99·0 % were obtained for M. luteolum DSM 20143^T, 98·9 % for M. foliorum DSM 12966^T and 98·8 % for M. oxydans DSM 20578^T, M. maritypicum ATCC 19260^T, M. phyllosphaerae DSM 13468^T and M. saperdae DSM 20169^T. Pairwise similarity values above 98 % were also found for M. liquefaciens DSM 20638^T and M. paraoxydans DSM 15019^T (98·6 % each), strain BAS69^T (98·2 %), M. schleiferi DSM 20489^T (98·2 %), M. testaceum DSM 20166^T and M. keratanolyticum DSM 8606^T (98·1 % each).

Based on these high pairwise 16S rRNA gene sequence similarity values, DNA–DNA relatedness of strains BAS69^T and BNP48^T to several closest phylogenetic neighbours was determined. Levels of DNA–DNA relatedness of strain BAS69^T to M. saperdae, M. foliorum and M. phyllosphaerae were 18, 21 and 19 %, respectively. Those of strain BNP48^T to M. maritypicum, M. oxydans, M. luteolum, M. foliorum and M. phyllosphaerae were 23, 16, 38, 36 and 11 %, respectively. DNA–DNA relatedness between the two novel strains was 41 %. These low values demonstrate that strains BAS69^T and BNP48^T each represent members of single novel species of the genus Microbacterium.

Morphological, physiological and chemotaxonomic characteristics of the two strains are different from those of phylogenetically closely related Microbacterium species (Table 1). The two strains were obligately aerobic, Gram-positive, irregular rods without spores. Cells of strain BAS69^T were immotile, whereas those of strain BNP48^T were motile. Cells were small, varying in size from 0·3 to 1·1 µm for strain BAS69^T and from 0·3 to 1·5 µm for strain BNP48^T. Colonies of both strains were circular, smooth, translucent and pigmented. Maximum colony diameters were 3 and 5 mm after 2 weeks of growth for strains BAS69^T and BNP48^T, respectively. Neither strain contained meso-diaminopimelic acid in the cell wall. The peptidoglycan type of strain BAS69^T was B1, [L-glu] D-glu(hyg)–gly_1–2–L-Lys and that of strain BNP48^T was B2, [L-hsr] D-glu(hyg)–gly–D-Orn (Schleifer & Kandler, 1972). The major menaquinones were MK-11 and MK-12, with minor amounts of MK-9, MK-10 and MK-13 for both strains.

Cells are obligate aerobic, Gram-positive, non-spore-forming, immotile, irregular rods 0·3–1·1 µm in size. Colonies are circular, smooth, translucent and orange pigmented with a maximum colony diameter of 3 mm after 2 weeks. Growth occurs at 30 and 37 °C and at 2 and 4 % NaCl. Catalase-positive and oxidase-negative. Crude oil is used as substrate. H₂S is not produced, arginine is not hydrolysed, urease is not present and the Voges–Proskauer reaction is negative. Acid is produced from sucrose and xylose. Acid is not produced from D-glucose, rhamnose, adonitol, inositol or sorbitol. The following are utilized: L-arabinose, D-cellobiose, D-fructose, D-galactose, gluconate, D-glucose, D-maltose, D-mannose, -D-melibiose, L-rhamnose, D-ribose, D-sucrose, salicin, D-trehalose, L-xylose, D-mannitol, sorbitol, fumarate, DL-lactate, L-malate, pyruvate, L-aspartate, L-histidine, putrescine and 4-hydroxybenzoate. The following are not utilized: N-acetyl-D-glucosamine, -D-galacturonate, glycogen, adonitol, i-inositol, acetate, propionate, trans-aconitate, adipate, citrate, DL-3-hydroxybutyrate, suberate, L-alanine, L-hydroxyproline, L-proline, L-serine, 3-hydroxybenzoate, phenylacetate, N-acetyl-D-galactosamine and L-ornithine. The following are hydrolysed: aesculin, p-nitrophenyl (pNP) N-acetyl--D-galactosaminide, pNP N-acetyl--D-glucosaminide, pNP -L-arabinopyranoside, pNP -D-cellobioside, pNP -D-galactopyranoside, pNP -D-glucopyranoside, pNP -D-glucopyranoside, pNP -D-mannoside, pNP -D-maltoside, pNP -D-xyloside, bis-pNP phosphate, benzolphosphonacid-pNP ester, L-alanine p-nitroanilide (pNA), glycine pNA, L-leucine pNA, L-lysine pna and L-proline pNA. The following are not hydrolysed: pNP -D-glucuronide, pNP -D-lactoside, pNP phosphocholine, 2-deoxythymidine-5'-pNP phosphate, -L-glutamate pNA, L-glutamate--3-carboxy pna and L-valine pNA. The type strain does not contain meso-diaminopimelic acid in its cell wall and the peptidoglycan-type is B1, [L-glu] D-glu(hyg)–gly_1–2–L-Lys. The major menaquinones are MK-11 and MK-12.

The type strain, BAS69^T(=DSM 16091^T=NCIMB 14003^T), was isolated from oil storage cavern 126 near Etzel, Germany (Bock et al., 1994).

Description of Microbacterium hydrocarbonoxydans sp. nov.
Microbacterium hydrocarbonoxydans (hy'dro.car.bon.ox'y.dans. N.L. part. adj. hydrocarbonoxydans oxidizing hydrocarbons).

Cells are obligate aerobic, Gram-positive, non-spore-forming, motile, irregular rods 0·3–1·5 µm in size. Colonies are circular, smooth, translucent and yellow pigmented with a maximum colony diameter of 5 mm after 2 weeks. Growth occurs at 30 and 37 °C and at 2 and 4 % NaCl. Catalase-positive and oxidase-negative. Crude oil is used as substrate. H₂S is not produced, arginine is not hydrolysed, urease is not present and the Voges–Proskauer reaction is negative. Acid is produced from rhamnose, sucrose and xylose. Acid is not produced from D-glucose, adonitol, inositol or sorbitol. The following are utilized: N-acetyl-D-glucosamine, L-arabinose, D-cellobiose, D-fructose, D-galactose, gluconate, D-glucose, glycogen, D-maltose, D-mannose, L-rhamnose, D-ribose, D-sucrose, salicin, D-trehalose, L-xylose, D-mannitol, acetate, propionate, citrate, fumarate, DL-lactate, L-malate, pyruvate, L-alanine, L-aspartate, L-histidine, L-hydroxyproline, L-proline, L-serine, putrescine, phenylacetate and N-acetyl-D-galactosamine. The following are not utilized: -D-galacturonate, -D-melibiose, adonitol, i-inositol, sorbitol, trans-aconitate, adipate, DL-3-hydroxybutyrate, suberate, 3-hydroxybenzoate, 4-hydroxybenzoate and L-ornithine. The following are hydrolysed: pNP N-acetyl--D-galactosaminide, pNP N-acetyl--D-glucosaminide, pNP -L-arabinopyranoside, pNP -D-cellopyranoside, pNP -D-galactopyranoside, pNP -D-glucopyranoside, pNP -D-glucopyranoside, pNP -D-lactoside, pNP -D-mannoside, pNP -D-maltoside, pNP -D-xyloside, bis-pNP phosphate, benzolphosphonacid-pNP ester, pNP phosphocholine, 2-deoxythymidine-5'-pNP phosphate, L-alanine pNA, glycine pNA, L-leucine pNA, L-lysine pna and L-proline pNA. The following are not hydrolysed: pNP -D-glucuronide, -L-glutamate pNA, L-glutamate--3-carboxy pna and L-valine pNA. The type strain does not contain meso-diaminopimelic acid in its cell wall and the peptidoglycan-type is B2, [L-hsr] D-glu(hyg)–gly–D-Orn. The major menaquinones are MK-11 and MK-12.

The type strain, BNP48^T (=DSM 16089^T=NCIMB 14002^T), was isolated from an oil-contaminated soil in Germany.

	ACKNOWLEDGEMENTS

 
We thank Cornelia Haveland, Ina Kramer, Marie-Anne Lepler and Daniela Zoch for excellent technical assistance.

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